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a forward genetic screen that used ethylnitrosourea (ENU) to induce mutations in a founder animal whose offspring were then screened for abnormal whole body metabolism [19,20], we found a family of mice that urinated and drank excessively. Serum and urine analysis showed that plasma glucose levels were normal and there was no glucose in the urine (unpublished data). Hence, this was an example of diabetes insipidus.\nThe disorder in these mice segregated in a monogenic, autosomal recessive manner, making Aqp2 a candidate gene. Sequencing of Aqp2 coding region of affected mice identified a thymine to guanine (T to G) transversion (Figure 1A), which is predicted to lead to a valine for phenylalanine substitution at amino acid 204 of the protein (F204V).\nFigure 1 Analysis of Aqp2 Sequence and Phenotype in Mutant Mice\n(A) Chromatographic traces of Aqp2 F204V mutation. The box shows the mutated codon, TTC (Phe) to GTC (Val) at position 204.\nWT, wild type; Mut, mutant.\n(B) Amino acid conservation of mouse AQP2 (residues 194–214). The boxed residue indicates phenylalanine at position 204.\nhAQP2, human AQP2; mAQP1, mouse AQP1; mAQP2, mouse AQP2; rAQP2, rat AQP2; xAQP2, Xenopus AQP2.\n(C) Urine production (ml) and water consumption (ml) of 58 F2 mice over a 24-h period (both sexes, aged 10–22 wk). Mutant mice (black squares) exhibit overt polyuria and polydipsia compared to littermate wild-type (white triangles) and heterozygous (grey circles) mice.\n(D) Urine osmolality and concentrating ability in Aqp2 mutant and their littermates (10–22 wk, both sexes), before (white bars) and after (black bars) dDAVP treatment. Wild type (WT; n = 12); heterozygote (Het; n = 20); mutant (Mut; n = 9). Data represent averages ± standard error of the mean, **p \u003c 0.01; ***p \u003c 0.001. AQP2 is a six-transmembrane water channel, and F204 lies near the extracellular face of the sixth membrane spanning domain, a region rich in hydrophobic amino acids. This and the other membrane-spanning domains are conserved among vertebrate species. The phenylalanine at position 204 is particularly well conserved (Figure 1B), not only among vertebrate AQP2 proteins, but also among others members of this family.\nAqp2F204V/F204V mice have dramatically increased urine production, in some cases producing an amount of urine in 24 h that exceeds their body weight, compared to their heterozygous or wild-type littermates. Such loss of water would rapidly lead to dehydration were it not compensated by increased water intake. Indeed, mutant mice also dramatically increase their water intake (Figure 1C) compared to their heterozygous or wild-type littermates. This phenotype—increased urinary output and water intake—showed complete concordance with homozygosity of the F204V mutation in the 58 animals tested.\nDiabetes insipidus can be defined as an inability to concentrate urine where appropriate. Compared to wild-type or heterozygous littermates, Aqp2F204V/F204V mice produce very dilute urine (Figure 1D). Basal urine concentration in mutant mice is about 161 mOsm, compared to about 1,293 mOsm in wild-type mice (p \u003c 0.001). Normally, urine concentration is under the control of the hypothalamus, which, in response to hypovolemia or hypernatremia [21], secretes AVP. The synthetic AVP analog, 1-deamino-8-D-arginine vasopressin (dDAVP; also called desmopressin), is a potent agonist of AVPR2. When administered to wild-type mice, dDAVP leads to a dramatic increase in urine concentration, from 1,293 to 5,885 mOsm (4.6-fold; Figure 1D). With similar treatment, mutant mice concentrate their urine to a lesser but still significant extent, from 161 to 470 mOsm (2.9-fold), indicating that these animals are not only unable to concentrate their urine properly but are also defective in their response to dDAVP. The smaller response to dDAVP indicates some residual activity of the mutant AQP2 channel, which must be sufficient to allow survival of the individual, in contrast to the T126M knock-in mouse [18].\nMultiple heterozygous matings yielded 101 animals, which appeared at a ratio of 26:49:26, near the expected Mendelian wild type, heterozygote, and mutant frequencies, respectively, indicating that there is no reduced viability associated with this mutation. Other than the increased urine production and water intake, there was no overt phenotype in mutant mice, save distended kidneys, which appeared variably in adult animals (Figure 2A). Although not specifically measured, mutant mice seem to have a normal lifespan. The one animal that was followed lived to 18 mo, typical for animals in our colony.\nFigure 2 Anatomy and Histology of Mouse Kidneys\n(A) Gross anatomy of an affected mouse (8-mo-old male). This shows the enlargement and cystic dilatation of the renal pelvis. There is thinning of the overlying renal parenchyma imparting a translucent appearance to portions of the kidney and collecting system. The bladder is also dilated.\n(B) Left kidney from mutant mouse (right) shown in (A) compared to a kidney from an age-sex matched unaffected littermate (left).\n(C) Hematoxylin and eosin stained section of ureter from a mutant mouse, showing normal histology despite bloating of the kidney.\n(D) Hematoxylin and eosin stained histologic section of a kidney from a 4-wk-old female mutant mouse. The mutant kidney shows marked dilatation of the renal pelvis with blunting of the papilla. There is preservation of the cortex and medulla. Aqp2F204V/F204V mice suffer from severe hydronephrosis (Figure 2A and 2B), presumably as a consequence of an inability to cope with the extreme polyuria. We found distended kidneys in all Aqp2F204V/F204V mice; however, the degree of inflation was variable in affected mice and worsened with age. Severe hydronephrosis has previously been observed in double Aqp1/Aqp3 knock-out mice [17], and appears at 6 wk. Even at 4 wk, Aqp2F204V/F204V mice had hydronephrosis. Histologic sections from Aqp2F204V/F204V mice demonstrated marked dilatation of the renal pelvis yet normal morphology of the ureter (Figure 2C and 2D). In particular, the muscularis propria was neither hypertrophied nor thinned. There was the normal festooned appearance of the urothelium, and this transitional epithelium was of normal thickness. There was thinning of the kidney as measured from renal capsule to renal pelvis. However, the morphologic features of the glomeruli and proximal/distal tubules were unremarkable (Figure 2D).\nAs shown previously [18,22], immunoblotting revealed three different forms of AQP2, due to different degrees and forms of glycosylation (Figure 3A). Previous reports have demonstrated that nonglycosylated protein appears as a 29 kDa band, while complex glycosylated protein runs as a smear between 35 and 45 kDa. A short-lived intermediate form of 31 kDa representing core, high-mannose glycosylation of AQP2 is apparent from pulse-chase labeling experiments [22]. Compared to that from the kidneys of wild-type animals, AQP2 from mutant animals was reduced in both the high molecular weight, diffuse form and the lowest molecular weight form, but enriched in the intermediate molecular weight form (Figure 3A). Heterozygous animals showed intermediate amounts of all three forms. The nature of these glycosylated forms was revealed by digestion with endoglycosidase H, which specifically cleaves mannose-rich carbohydrate from the protein backbone. Treatment of endogenous AQP2 from kidneys of wild-type, heterozygous, and mutant animals specifically affected the intermediate molecular weight form (Figure 3B). The presence of some mature glycosylated proteins (35–45 kDa) in Aqp2F204V/F204V mice presumably permits their survival compared to Aqp2T126M/T126M mice, and is consistent with a diminished response to dDAVP.\nFigure 3 Immunoblot Analyses of AQP2 from Mouse Kidneys\n(A) Western blot analyses of total kidney membranes from littermate mice. An intermediate form of AQP2 at 31 kDa was identified in kidney membranes from a mutant mouse (Mut) and partially in a heterozygous mouse (Het).\n(B) Total kidney membranes were subjected to endoglycosidase H treatment (Endo H) prior to Western blotting. High-mannose (h.m.) glycosylated proteins that have not exited the ER are sensitive to endoglycosidase H digestion. In humans, recessive alleles of Aqp2 are postulated to cause NDI because they do not properly translocate to the apical cell surface in response to AVP. This postulate comes solely from in vitro studies in which mutant Aqp2 cDNAs corresponding to human disease mutations are transfected into kidney cell lines. In general, such recessive alleles, when visualized immunocytochemically, fail to localize to AVP-responsive vesicles. Rather, they get trapped in the endoplasmic reticulum (ER). Our mouse model of NDI affords the first opportunity to test this hypothesis in a mature animal. As shown in Figure 4A (top row of photomicrographs), AQP2 (stained red) normally localized to the subapical region of collecting duct cells in kidneys of wild-type mice. Upon stimulation with dDAVP, AQP2 translocated to or near the cell surface (Figure 4A, second row). In kidneys taken from mutant animals, however, AQP2 was distributed randomly throughout the cell in the basal state (Figure 4A, third row), while AQP3 (green) appropriately localized to the basolateral surface [23]. Furthermore, upon dDAVP stimulation, AQP2-F204V failed to translocate to the cell surface (Figure 4A, bottom row). To confirm these findings, the staining was repeated in kidneys taken from two further mice for each class, wild-type or mutant, with or without dDAVP treatment, with identical results.\nFigure 4 AQP2 Subcellular Localization and Translocation in Mouse Kidney Collecting Ducts and MDCK Cell Lines\n(A) Immunohistochemistry on collecting ducts in kidney sections from an AQP2-F204V mutant (Mut) mouse and an age-sex matched wild-type (WT) littermate. Mice were injected intraperitoneally with PBS (NT) or dDAVP before sacrificing and fixation of the kidneys. Kidneys sections were immunostained for AQP2 (red) and the basolateral marker AQP3 (green). The images were merged and an area of the cytoplasm was magnified (zoom). Note that mutant AQP2 is not properly localized to the subapical compartment, nor does it respond to dDAVP.\n(B) MDCK cell lines, stably transfected with constructs encoding mouse WT or AQP2-F204V, were treated with and without 150 μM forskolin for 90 min, after which cells were fixed, permeabilized, and subjected to immunocytochemistry. AQP2 is shown in green, and the basolateral marker Na+/K+-ATPase is shown in red, alongside the nuclear stain DAPI. The z-profile images were reconstructed from multiple z-sections, along the dotted line. Mutant AQP2 fails to localize to the cell surface upon forskolin stimulation. Rather, the perinuclear staining is consistent with an ER localization of mutant AQP2.\n(C) The MDCK cell line expressing AQP2-F204V was grown on fibronectin-coated coverslips until tight junctions formed, at which point the cells were treated with 150 μM forskolin for 90 min. Cells were fixed, permeabilized, and sequentially immunoblotted for AQP2 (green) and calnexin (red), an ER marker. The merged image shows that AQP2-F204V colocalizes with the endoplasmic reticulum marker. Scale bar refers to 10 μm. To investigate the mechanism of defective translocation of AQP2-F204V, we turned to transfection of MDCK cells. Stable cell lines expressing mouse wild-type AQP2 and AQP2-F204V were established. Immunoblots of protein extracts from stable cell lines showed that MDCK cells recapitulate the glycosylation defect seen in mutant mice (unpublished data). The wild-type protein was again present in three different forms. Cells expressing AQP2-F204V lacked the 35–45 kDa form and were enriched in the core-glycosylated 31 kDa form.\nIn transfected, unstimulated MDCK cells, wild-type AQP2 (stained green) appeared in a punctate pattern distributed throughout the subapical region (Figure 4B, left column photomicrographs), consistent with vesicular compartmentalization. AQP2-F204V, on the other hand, appeared in a punctate but perinuclear pattern (Figure 4B, third column). Upon stimulation with forskolin, a cAMP-dependent protein kinase activator, wild-type AQP2 translocated to the apical surface of polarized MDCK cells (Figure 4B, second column). Along the z-axis, the perinuclear distribution of AQP2-F204V was clearly seen, and this distribution is not altered by forskolin (Figure 4B, bottom row, two right columns). The perinuclear distribution of AQP2-F204V is consistent with an ER compartmentalization. To test the idea that AQP2-F204V localizes to the ER, we co-stained cells transfected with Aqp2F204V (cDNA) for AQP2 and an ER marker, calnexin (Figure 4C). Colocalization of calnexin with AQP2 was investigated directly, and it was found that 80% of all AQP2-F204V protein colocalized with calnexin. The remaining 20% appeared at the periphery of the ER, representing AQP2-F204V that had potentially progressed beyond the ER. This “ER escape” was consistent with the small proportion of mature, complex glycosylated, AQP2-F204V in mutant kidneys (see Figure 3A).\nAnimals heterozygous for the Aqp2F204V mutation were not affected in their urine production or urine osmolality (see Figure 1C and 1D). It has also been shown that a recessive NDI allele, AQP2-R187C, does not interact with wild-type protein in oocytes [24], nor does it homo-oligomerize in MDCK cells [22]. Therefore, kidneys from heterozygous animals were examined for evidence of two populations of AQP2 protein. Surprisingly, immunohistochemical staining of kidney collecting ducts from Aqp2F204V/+ mice revealed a pattern remarkably similar to wild type (Figure 5A). AQP2 translocated completely to the apical cell surface upon dDAVP stimulation. This wild-type staining pattern may simply reflect the fact that decreasing the amount of mutant protein by half makes it undetectable by immunocytochemistry. Alternatively, the presence of wild-type protein may alter the localization of the mutant protein. Indeed, Hendriks et al. proposed a “piggy-back” mechanism to explain the transport of nonglycosylated subunits of AQP2 to the cell surface by glycosylated subunits [22]. It has also been shown that wild-type AQP2 protein can rescue a translocation-defective mutant protein, AQP2-P262L, when the two are coexpressed in MDCK cells [25].\nFigure 5 AQP2-F204V Rescue in Heterozygous Mouse Collecting Ducts and in Cotransfected MDCK Cells\n(A) In heterozygous animals, AQP2 localizes and responds to dDAVP normally. Immunohistochemistry was carried out on kidney sections from an Aqp2F204V/+ mouse, after injection with dDAVP. Kidney sections were sequentially immunostained for AQP2 (red) and the basolateral marker AQP3 (green).\n(B) Mutant and wild-type AQP2 physically interact. MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP tagged wild-type AQP2, AQP2-F204V, or GFP alone. Solubilized membranes were immunoprecipitated with a GFP antibody. Total membranes and immunoprecipitates (GFP-IP) were Western blotted using an antibody against AQP2 (arrow) or AQP2-GFP fusions (arrowhead).\n(C) Wild-type AQP2 rescues the localization defect of mutant AQP2. GFP fusions of either wild-type AQP2 (WT-GFP, top photomicrographs) or F204V AQP2 (F204V-GFP, bottom photomicrographs) were expressed in polarized MDCK stable cell lines expressing vector alone (vector, left photomicrographs) or AQP2-WT (right photomicrographs). Cells were stimulated with forskolin, processed for immunocytochemistry, and used to generate z-sectional images.\n(D) Mutant AQP2 is present at the cell surface in cells coexpressing wild-type AQP2 (AQP2-WT). GFP fused to AQP2-F204V was expressed in MDCK cells expressing wild-type AQP2 or vector alone. Cells were stimulated with forskolin, and cell surface biotinylated proteins were precipitated then analyzed for the presence of wild-type AQP2 (arrow) and AQP2-F204V (arrowhead) by Western blot. In the collecting ducts from Aqp2F204V/+ mice, the wild type may rescue the mutant protein as suggested by the subcellular distribution of AQP2 protein. To test this idea, we first looked for an interaction between mutant and wild-type proteins in transfected MDCK cells (Figure 5B). MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP expression constructs encoding GFP-tagged wild-type AQP2, AQP2-F204V, or GFP alone. Antibodies against GFP coimmunoprecipitated wild-type AQP2 when AQP2-GFP or AQP2-F204V-GFP was transiently transfected, but not when GFP by itself was transiently transfected into MDCK cells stably expressing wild-type AQP2 (Figure 5B, upper blots). Western blot of total membranes showed that wild-type AQP2 is equivalently expressed in all three cases (Figure 5B, lower blots).\nIf wild-type and mutant proteins are indeed interacting in the cell, is this interaction sufficient to rescue the localization of mutant protein? To answer this question, we used MDCK cells stably transfected with wild-type AQP2 expressing vector or with empty vector. On top of these, we transiently transfected AQP2-GFP or AQP2-F204V-GFP expression constructs. AQP2-GFP localized to the apical surface upon forskolin stimulation whether it was transiently transfected into vector-only cells (Figure 5C, upper left images) or into wild-type AQP2 cells (Figure 5C, upper right). AQP2-F204V-GFP, when expressed by transient transfection into vector only cells, showed a diffuse cytoplasmic distribution pattern (Figure 5C, lower left). When expressed in wild-type AQP2 cells, however, AQP2-F204V-GFP localized to the apical surface to varying degrees (Figure 5C, lower right images [i–iii]). The lower right images of Figure 5C shows three cells from a single transfection. The first is a nontransfected cell that shows the localization of the stably expressing wild-type AQP2, which is apical upon forskolin stimulation. The next two show expression of both the stable wild-type AQP2 and the transient AQP2-F204V-GFP. In cell (ii), localization of wild-type AQP2 was indistinguishable from AQP2-F204V-GFP; both were apical upon forskolin stimulation. Although the effect was subtle in cell (iii), AQP2-F204V-GFP was partly localized to the apical surface. Generally, the localization of AQP2-F204V-GFP was clearly more apical when wild-type AQP2 was also expressed.\nTo confirm these results biochemically, we transfected the same cell lines (wild-type AQP2 or vector) with F204V-GFP, biotinylated surface proteins after forskolin stimulation, and precipitated the biotinylated proteins (Figure 5D). AQP2-F204V-GFP is expressed approximately equally in both cell lines (Figure 5D, total cells), but is biotinylated only when wild-type AQP2 is also expressed (Figure 5D, surface biotinylated). Since only cell surface proteins are accessible to biotin, these results indicate that AQP2-F204V is transported to the cell surface when wild-type AQP2 is present, but not on its own."}

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a forward genetic screen that used ethylnitrosourea (ENU) to induce mutations in a founder animal whose offspring were then screened for abnormal whole body metabolism [19,20], we found a family of mice that urinated and drank excessively. Serum and urine analysis showed that plasma glucose levels were normal and there was no glucose in the urine (unpublished data). Hence, this was an example of diabetes insipidus.\nThe disorder in these mice segregated in a monogenic, autosomal recessive manner, making Aqp2 a candidate gene. Sequencing of Aqp2 coding region of affected mice identified a thymine to guanine (T to G) transversion (Figure 1A), which is predicted to lead to a valine for phenylalanine substitution at amino acid 204 of the protein (F204V).\nFigure 1 Analysis of Aqp2 Sequence and Phenotype in Mutant Mice\n(A) Chromatographic traces of Aqp2 F204V mutation. The box shows the mutated codon, TTC (Phe) to GTC (Val) at position 204.\nWT, wild type; Mut, mutant.\n(B) Amino acid conservation of mouse AQP2 (residues 194–214). The boxed residue indicates phenylalanine at position 204.\nhAQP2, human AQP2; mAQP1, mouse AQP1; mAQP2, mouse AQP2; rAQP2, rat AQP2; xAQP2, Xenopus AQP2.\n(C) Urine production (ml) and water consumption (ml) of 58 F2 mice over a 24-h period (both sexes, aged 10–22 wk). Mutant mice (black squares) exhibit overt polyuria and polydipsia compared to littermate wild-type (white triangles) and heterozygous (grey circles) mice.\n(D) Urine osmolality and concentrating ability in Aqp2 mutant and their littermates (10–22 wk, both sexes), before (white bars) and after (black bars) dDAVP treatment. Wild type (WT; n = 12); heterozygote (Het; n = 20); mutant (Mut; n = 9). Data represent averages ± standard error of the mean, **p \u003c 0.01; ***p \u003c 0.001. AQP2 is a six-transmembrane water channel, and F204 lies near the extracellular face of the sixth membrane spanning domain, a region rich in hydrophobic amino acids. This and the other membrane-spanning domains are conserved among vertebrate species. The phenylalanine at position 204 is particularly well conserved (Figure 1B), not only among vertebrate AQP2 proteins, but also among others members of this family.\nAqp2F204V/F204V mice have dramatically increased urine production, in some cases producing an amount of urine in 24 h that exceeds their body weight, compared to their heterozygous or wild-type littermates. Such loss of water would rapidly lead to dehydration were it not compensated by increased water intake. Indeed, mutant mice also dramatically increase their water intake (Figure 1C) compared to their heterozygous or wild-type littermates. This phenotype—increased urinary output and water intake—showed complete concordance with homozygosity of the F204V mutation in the 58 animals tested.\nDiabetes insipidus can be defined as an inability to concentrate urine where appropriate. Compared to wild-type or heterozygous littermates, Aqp2F204V/F204V mice produce very dilute urine (Figure 1D). Basal urine concentration in mutant mice is about 161 mOsm, compared to about 1,293 mOsm in wild-type mice (p \u003c 0.001). Normally, urine concentration is under the control of the hypothalamus, which, in response to hypovolemia or hypernatremia [21], secretes AVP. The synthetic AVP analog, 1-deamino-8-D-arginine vasopressin (dDAVP; also called desmopressin), is a potent agonist of AVPR2. When administered to wild-type mice, dDAVP leads to a dramatic increase in urine concentration, from 1,293 to 5,885 mOsm (4.6-fold; Figure 1D). With similar treatment, mutant mice concentrate their urine to a lesser but still significant extent, from 161 to 470 mOsm (2.9-fold), indicating that these animals are not only unable to concentrate their urine properly but are also defective in their response to dDAVP. The smaller response to dDAVP indicates some residual activity of the mutant AQP2 channel, which must be sufficient to allow survival of the individual, in contrast to the T126M knock-in mouse [18].\nMultiple heterozygous matings yielded 101 animals, which appeared at a ratio of 26:49:26, near the expected Mendelian wild type, heterozygote, and mutant frequencies, respectively, indicating that there is no reduced viability associated with this mutation. Other than the increased urine production and water intake, there was no overt phenotype in mutant mice, save distended kidneys, which appeared variably in adult animals (Figure 2A). Although not specifically measured, mutant mice seem to have a normal lifespan. The one animal that was followed lived to 18 mo, typical for animals in our colony.\nFigure 2 Anatomy and Histology of Mouse Kidneys\n(A) Gross anatomy of an affected mouse (8-mo-old male). This shows the enlargement and cystic dilatation of the renal pelvis. There is thinning of the overlying renal parenchyma imparting a translucent appearance to portions of the kidney and collecting system. The bladder is also dilated.\n(B) Left kidney from mutant mouse (right) shown in (A) compared to a kidney from an age-sex matched unaffected littermate (left).\n(C) Hematoxylin and eosin stained section of ureter from a mutant mouse, showing normal histology despite bloating of the kidney.\n(D) Hematoxylin and eosin stained histologic section of a kidney from a 4-wk-old female mutant mouse. The mutant kidney shows marked dilatation of the renal pelvis with blunting of the papilla. There is preservation of the cortex and medulla. Aqp2F204V/F204V mice suffer from severe hydronephrosis (Figure 2A and 2B), presumably as a consequence of an inability to cope with the extreme polyuria. We found distended kidneys in all Aqp2F204V/F204V mice; however, the degree of inflation was variable in affected mice and worsened with age. Severe hydronephrosis has previously been observed in double Aqp1/Aqp3 knock-out mice [17], and appears at 6 wk. Even at 4 wk, Aqp2F204V/F204V mice had hydronephrosis. Histologic sections from Aqp2F204V/F204V mice demonstrated marked dilatation of the renal pelvis yet normal morphology of the ureter (Figure 2C and 2D). In particular, the muscularis propria was neither hypertrophied nor thinned. There was the normal festooned appearance of the urothelium, and this transitional epithelium was of normal thickness. There was thinning of the kidney as measured from renal capsule to renal pelvis. However, the morphologic features of the glomeruli and proximal/distal tubules were unremarkable (Figure 2D).\nAs shown previously [18,22], immunoblotting revealed three different forms of AQP2, due to different degrees and forms of glycosylation (Figure 3A). Previous reports have demonstrated that nonglycosylated protein appears as a 29 kDa band, while complex glycosylated protein runs as a smear between 35 and 45 kDa. A short-lived intermediate form of 31 kDa representing core, high-mannose glycosylation of AQP2 is apparent from pulse-chase labeling experiments [22]. Compared to that from the kidneys of wild-type animals, AQP2 from mutant animals was reduced in both the high molecular weight, diffuse form and the lowest molecular weight form, but enriched in the intermediate molecular weight form (Figure 3A). Heterozygous animals showed intermediate amounts of all three forms. The nature of these glycosylated forms was revealed by digestion with endoglycosidase H, which specifically cleaves mannose-rich carbohydrate from the protein backbone. Treatment of endogenous AQP2 from kidneys of wild-type, heterozygous, and mutant animals specifically affected the intermediate molecular weight form (Figure 3B). The presence of some mature glycosylated proteins (35–45 kDa) in Aqp2F204V/F204V mice presumably permits their survival compared to Aqp2T126M/T126M mice, and is consistent with a diminished response to dDAVP.\nFigure 3 Immunoblot Analyses of AQP2 from Mouse Kidneys\n(A) Western blot analyses of total kidney membranes from littermate mice. An intermediate form of AQP2 at 31 kDa was identified in kidney membranes from a mutant mouse (Mut) and partially in a heterozygous mouse (Het).\n(B) Total kidney membranes were subjected to endoglycosidase H treatment (Endo H) prior to Western blotting. High-mannose (h.m.) glycosylated proteins that have not exited the ER are sensitive to endoglycosidase H digestion. In humans, recessive alleles of Aqp2 are postulated to cause NDI because they do not properly translocate to the apical cell surface in response to AVP. This postulate comes solely from in vitro studies in which mutant Aqp2 cDNAs corresponding to human disease mutations are transfected into kidney cell lines. In general, such recessive alleles, when visualized immunocytochemically, fail to localize to AVP-responsive vesicles. Rather, they get trapped in the endoplasmic reticulum (ER). Our mouse model of NDI affords the first opportunity to test this hypothesis in a mature animal. As shown in Figure 4A (top row of photomicrographs), AQP2 (stained red) normally localized to the subapical region of collecting duct cells in kidneys of wild-type mice. Upon stimulation with dDAVP, AQP2 translocated to or near the cell surface (Figure 4A, second row). In kidneys taken from mutant animals, however, AQP2 was distributed randomly throughout the cell in the basal state (Figure 4A, third row), while AQP3 (green) appropriately localized to the basolateral surface [23]. Furthermore, upon dDAVP stimulation, AQP2-F204V failed to translocate to the cell surface (Figure 4A, bottom row). To confirm these findings, the staining was repeated in kidneys taken from two further mice for each class, wild-type or mutant, with or without dDAVP treatment, with identical results.\nFigure 4 AQP2 Subcellular Localization and Translocation in Mouse Kidney Collecting Ducts and MDCK Cell Lines\n(A) Immunohistochemistry on collecting ducts in kidney sections from an AQP2-F204V mutant (Mut) mouse and an age-sex matched wild-type (WT) littermate. Mice were injected intraperitoneally with PBS (NT) or dDAVP before sacrificing and fixation of the kidneys. Kidneys sections were immunostained for AQP2 (red) and the basolateral marker AQP3 (green). The images were merged and an area of the cytoplasm was magnified (zoom). Note that mutant AQP2 is not properly localized to the subapical compartment, nor does it respond to dDAVP.\n(B) MDCK cell lines, stably transfected with constructs encoding mouse WT or AQP2-F204V, were treated with and without 150 μM forskolin for 90 min, after which cells were fixed, permeabilized, and subjected to immunocytochemistry. AQP2 is shown in green, and the basolateral marker Na+/K+-ATPase is shown in red, alongside the nuclear stain DAPI. The z-profile images were reconstructed from multiple z-sections, along the dotted line. Mutant AQP2 fails to localize to the cell surface upon forskolin stimulation. Rather, the perinuclear staining is consistent with an ER localization of mutant AQP2.\n(C) The MDCK cell line expressing AQP2-F204V was grown on fibronectin-coated coverslips until tight junctions formed, at which point the cells were treated with 150 μM forskolin for 90 min. Cells were fixed, permeabilized, and sequentially immunoblotted for AQP2 (green) and calnexin (red), an ER marker. The merged image shows that AQP2-F204V colocalizes with the endoplasmic reticulum marker. Scale bar refers to 10 μm. To investigate the mechanism of defective translocation of AQP2-F204V, we turned to transfection of MDCK cells. Stable cell lines expressing mouse wild-type AQP2 and AQP2-F204V were established. Immunoblots of protein extracts from stable cell lines showed that MDCK cells recapitulate the glycosylation defect seen in mutant mice (unpublished data). The wild-type protein was again present in three different forms. Cells expressing AQP2-F204V lacked the 35–45 kDa form and were enriched in the core-glycosylated 31 kDa form.\nIn transfected, unstimulated MDCK cells, wild-type AQP2 (stained green) appeared in a punctate pattern distributed throughout the subapical region (Figure 4B, left column photomicrographs), consistent with vesicular compartmentalization. AQP2-F204V, on the other hand, appeared in a punctate but perinuclear pattern (Figure 4B, third column). Upon stimulation with forskolin, a cAMP-dependent protein kinase activator, wild-type AQP2 translocated to the apical surface of polarized MDCK cells (Figure 4B, second column). Along the z-axis, the perinuclear distribution of AQP2-F204V was clearly seen, and this distribution is not altered by forskolin (Figure 4B, bottom row, two right columns). The perinuclear distribution of AQP2-F204V is consistent with an ER compartmentalization. To test the idea that AQP2-F204V localizes to the ER, we co-stained cells transfected with Aqp2F204V (cDNA) for AQP2 and an ER marker, calnexin (Figure 4C). Colocalization of calnexin with AQP2 was investigated directly, and it was found that 80% of all AQP2-F204V protein colocalized with calnexin. The remaining 20% appeared at the periphery of the ER, representing AQP2-F204V that had potentially progressed beyond the ER. This “ER escape” was consistent with the small proportion of mature, complex glycosylated, AQP2-F204V in mutant kidneys (see Figure 3A).\nAnimals heterozygous for the Aqp2F204V mutation were not affected in their urine production or urine osmolality (see Figure 1C and 1D). It has also been shown that a recessive NDI allele, AQP2-R187C, does not interact with wild-type protein in oocytes [24], nor does it homo-oligomerize in MDCK cells [22]. Therefore, kidneys from heterozygous animals were examined for evidence of two populations of AQP2 protein. Surprisingly, immunohistochemical staining of kidney collecting ducts from Aqp2F204V/+ mice revealed a pattern remarkably similar to wild type (Figure 5A). AQP2 translocated completely to the apical cell surface upon dDAVP stimulation. This wild-type staining pattern may simply reflect the fact that decreasing the amount of mutant protein by half makes it undetectable by immunocytochemistry. Alternatively, the presence of wild-type protein may alter the localization of the mutant protein. Indeed, Hendriks et al. proposed a “piggy-back” mechanism to explain the transport of nonglycosylated subunits of AQP2 to the cell surface by glycosylated subunits [22]. It has also been shown that wild-type AQP2 protein can rescue a translocation-defective mutant protein, AQP2-P262L, when the two are coexpressed in MDCK cells [25].\nFigure 5 AQP2-F204V Rescue in Heterozygous Mouse Collecting Ducts and in Cotransfected MDCK Cells\n(A) In heterozygous animals, AQP2 localizes and responds to dDAVP normally. Immunohistochemistry was carried out on kidney sections from an Aqp2F204V/+ mouse, after injection with dDAVP. Kidney sections were sequentially immunostained for AQP2 (red) and the basolateral marker AQP3 (green).\n(B) Mutant and wild-type AQP2 physically interact. MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP tagged wild-type AQP2, AQP2-F204V, or GFP alone. Solubilized membranes were immunoprecipitated with a GFP antibody. Total membranes and immunoprecipitates (GFP-IP) were Western blotted using an antibody against AQP2 (arrow) or AQP2-GFP fusions (arrowhead).\n(C) Wild-type AQP2 rescues the localization defect of mutant AQP2. GFP fusions of either wild-type AQP2 (WT-GFP, top photomicrographs) or F204V AQP2 (F204V-GFP, bottom photomicrographs) were expressed in polarized MDCK stable cell lines expressing vector alone (vector, left photomicrographs) or AQP2-WT (right photomicrographs). Cells were stimulated with forskolin, processed for immunocytochemistry, and used to generate z-sectional images.\n(D) Mutant AQP2 is present at the cell surface in cells coexpressing wild-type AQP2 (AQP2-WT). GFP fused to AQP2-F204V was expressed in MDCK cells expressing wild-type AQP2 or vector alone. Cells were stimulated with forskolin, and cell surface biotinylated proteins were precipitated then analyzed for the presence of wild-type AQP2 (arrow) and AQP2-F204V (arrowhead) by Western blot. In the collecting ducts from Aqp2F204V/+ mice, the wild type may rescue the mutant protein as suggested by the subcellular distribution of AQP2 protein. To test this idea, we first looked for an interaction between mutant and wild-type proteins in transfected MDCK cells (Figure 5B). MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP expression constructs encoding GFP-tagged wild-type AQP2, AQP2-F204V, or GFP alone. Antibodies against GFP coimmunoprecipitated wild-type AQP2 when AQP2-GFP or AQP2-F204V-GFP was transiently transfected, but not when GFP by itself was transiently transfected into MDCK cells stably expressing wild-type AQP2 (Figure 5B, upper blots). Western blot of total membranes showed that wild-type AQP2 is equivalently expressed in all three cases (Figure 5B, lower blots).\nIf wild-type and mutant proteins are indeed interacting in the cell, is this interaction sufficient to rescue the localization of mutant protein? To answer this question, we used MDCK cells stably transfected with wild-type AQP2 expressing vector or with empty vector. On top of these, we transiently transfected AQP2-GFP or AQP2-F204V-GFP expression constructs. AQP2-GFP localized to the apical surface upon forskolin stimulation whether it was transiently transfected into vector-only cells (Figure 5C, upper left images) or into wild-type AQP2 cells (Figure 5C, upper right). AQP2-F204V-GFP, when expressed by transient transfection into vector only cells, showed a diffuse cytoplasmic distribution pattern (Figure 5C, lower left). When expressed in wild-type AQP2 cells, however, AQP2-F204V-GFP localized to the apical surface to varying degrees (Figure 5C, lower right images [i–iii]). The lower right images of Figure 5C shows three cells from a single transfection. The first is a nontransfected cell that shows the localization of the stably expressing wild-type AQP2, which is apical upon forskolin stimulation. The next two show expression of both the stable wild-type AQP2 and the transient AQP2-F204V-GFP. In cell (ii), localization of wild-type AQP2 was indistinguishable from AQP2-F204V-GFP; both were apical upon forskolin stimulation. Although the effect was subtle in cell (iii), AQP2-F204V-GFP was partly localized to the apical surface. Generally, the localization of AQP2-F204V-GFP was clearly more apical when wild-type AQP2 was also expressed.\nTo confirm these results biochemically, we transfected the same cell lines (wild-type AQP2 or vector) with F204V-GFP, biotinylated surface proteins after forskolin stimulation, and precipitated the biotinylated proteins (Figure 5D). AQP2-F204V-GFP is expressed approximately equally in both cell lines (Figure 5D, total cells), but is biotinylated only when wild-type AQP2 is also expressed (Figure 5D, surface biotinylated). Since only cell surface proteins are accessible to biotin, these results indicate that AQP2-F204V is transported to the cell surface when wild-type AQP2 is present, but not on its own."}

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a forward genetic screen that used ethylnitrosourea (ENU) to induce mutations in a founder animal whose offspring were then screened for abnormal whole body metabolism [19,20], we found a family of mice that urinated and drank excessively. Serum and urine analysis showed that plasma glucose levels were normal and there was no glucose in the urine (unpublished data). Hence, this was an example of diabetes insipidus.\nThe disorder in these mice segregated in a monogenic, autosomal recessive manner, making Aqp2 a candidate gene. Sequencing of Aqp2 coding region of affected mice identified a thymine to guanine (T to G) transversion (Figure 1A), which is predicted to lead to a valine for phenylalanine substitution at amino acid 204 of the protein (F204V).\nFigure 1 Analysis of Aqp2 Sequence and Phenotype in Mutant Mice\n(A) Chromatographic traces of Aqp2 F204V mutation. The box shows the mutated codon, TTC (Phe) to GTC (Val) at position 204.\nWT, wild type; Mut, mutant.\n(B) Amino acid conservation of mouse AQP2 (residues 194–214). The boxed residue indicates phenylalanine at position 204.\nhAQP2, human AQP2; mAQP1, mouse AQP1; mAQP2, mouse AQP2; rAQP2, rat AQP2; xAQP2, Xenopus AQP2.\n(C) Urine production (ml) and water consumption (ml) of 58 F2 mice over a 24-h period (both sexes, aged 10–22 wk). Mutant mice (black squares) exhibit overt polyuria and polydipsia compared to littermate wild-type (white triangles) and heterozygous (grey circles) mice.\n(D) Urine osmolality and concentrating ability in Aqp2 mutant and their littermates (10–22 wk, both sexes), before (white bars) and after (black bars) dDAVP treatment. Wild type (WT; n = 12); heterozygote (Het; n = 20); mutant (Mut; n = 9). Data represent averages ± standard error of the mean, **p \u003c 0.01; ***p \u003c 0.001. AQP2 is a six-transmembrane water channel, and F204 lies near the extracellular face of the sixth membrane spanning domain, a region rich in hydrophobic amino acids. This and the other membrane-spanning domains are conserved among vertebrate species. The phenylalanine at position 204 is particularly well conserved (Figure 1B), not only among vertebrate AQP2 proteins, but also among others members of this family.\nAqp2F204V/F204V mice have dramatically increased urine production, in some cases producing an amount of urine in 24 h that exceeds their body weight, compared to their heterozygous or wild-type littermates. Such loss of water would rapidly lead to dehydration were it not compensated by increased water intake. Indeed, mutant mice also dramatically increase their water intake (Figure 1C) compared to their heterozygous or wild-type littermates. This phenotype—increased urinary output and water intake—showed complete concordance with homozygosity of the F204V mutation in the 58 animals tested.\nDiabetes insipidus can be defined as an inability to concentrate urine where appropriate. Compared to wild-type or heterozygous littermates, Aqp2F204V/F204V mice produce very dilute urine (Figure 1D). Basal urine concentration in mutant mice is about 161 mOsm, compared to about 1,293 mOsm in wild-type mice (p \u003c 0.001). Normally, urine concentration is under the control of the hypothalamus, which, in response to hypovolemia or hypernatremia [21], secretes AVP. The synthetic AVP analog, 1-deamino-8-D-arginine vasopressin (dDAVP; also called desmopressin), is a potent agonist of AVPR2. When administered to wild-type mice, dDAVP leads to a dramatic increase in urine concentration, from 1,293 to 5,885 mOsm (4.6-fold; Figure 1D). With similar treatment, mutant mice concentrate their urine to a lesser but still significant extent, from 161 to 470 mOsm (2.9-fold), indicating that these animals are not only unable to concentrate their urine properly but are also defective in their response to dDAVP. The smaller response to dDAVP indicates some residual activity of the mutant AQP2 channel, which must be sufficient to allow survival of the individual, in contrast to the T126M knock-in mouse [18].\nMultiple heterozygous matings yielded 101 animals, which appeared at a ratio of 26:49:26, near the expected Mendelian wild type, heterozygote, and mutant frequencies, respectively, indicating that there is no reduced viability associated with this mutation. Other than the increased urine production and water intake, there was no overt phenotype in mutant mice, save distended kidneys, which appeared variably in adult animals (Figure 2A). Although not specifically measured, mutant mice seem to have a normal lifespan. The one animal that was followed lived to 18 mo, typical for animals in our colony.\nFigure 2 Anatomy and Histology of Mouse Kidneys\n(A) Gross anatomy of an affected mouse (8-mo-old male). This shows the enlargement and cystic dilatation of the renal pelvis. There is thinning of the overlying renal parenchyma imparting a translucent appearance to portions of the kidney and collecting system. The bladder is also dilated.\n(B) Left kidney from mutant mouse (right) shown in (A) compared to a kidney from an age-sex matched unaffected littermate (left).\n(C) Hematoxylin and eosin stained section of ureter from a mutant mouse, showing normal histology despite bloating of the kidney.\n(D) Hematoxylin and eosin stained histologic section of a kidney from a 4-wk-old female mutant mouse. The mutant kidney shows marked dilatation of the renal pelvis with blunting of the papilla. There is preservation of the cortex and medulla. Aqp2F204V/F204V mice suffer from severe hydronephrosis (Figure 2A and 2B), presumably as a consequence of an inability to cope with the extreme polyuria. We found distended kidneys in all Aqp2F204V/F204V mice; however, the degree of inflation was variable in affected mice and worsened with age. Severe hydronephrosis has previously been observed in double Aqp1/Aqp3 knock-out mice [17], and appears at 6 wk. Even at 4 wk, Aqp2F204V/F204V mice had hydronephrosis. Histologic sections from Aqp2F204V/F204V mice demonstrated marked dilatation of the renal pelvis yet normal morphology of the ureter (Figure 2C and 2D). In particular, the muscularis propria was neither hypertrophied nor thinned. There was the normal festooned appearance of the urothelium, and this transitional epithelium was of normal thickness. There was thinning of the kidney as measured from renal capsule to renal pelvis. However, the morphologic features of the glomeruli and proximal/distal tubules were unremarkable (Figure 2D).\nAs shown previously [18,22], immunoblotting revealed three different forms of AQP2, due to different degrees and forms of glycosylation (Figure 3A). Previous reports have demonstrated that nonglycosylated protein appears as a 29 kDa band, while complex glycosylated protein runs as a smear between 35 and 45 kDa. A short-lived intermediate form of 31 kDa representing core, high-mannose glycosylation of AQP2 is apparent from pulse-chase labeling experiments [22]. Compared to that from the kidneys of wild-type animals, AQP2 from mutant animals was reduced in both the high molecular weight, diffuse form and the lowest molecular weight form, but enriched in the intermediate molecular weight form (Figure 3A). Heterozygous animals showed intermediate amounts of all three forms. The nature of these glycosylated forms was revealed by digestion with endoglycosidase H, which specifically cleaves mannose-rich carbohydrate from the protein backbone. Treatment of endogenous AQP2 from kidneys of wild-type, heterozygous, and mutant animals specifically affected the intermediate molecular weight form (Figure 3B). The presence of some mature glycosylated proteins (35–45 kDa) in Aqp2F204V/F204V mice presumably permits their survival compared to Aqp2T126M/T126M mice, and is consistent with a diminished response to dDAVP.\nFigure 3 Immunoblot Analyses of AQP2 from Mouse Kidneys\n(A) Western blot analyses of total kidney membranes from littermate mice. An intermediate form of AQP2 at 31 kDa was identified in kidney membranes from a mutant mouse (Mut) and partially in a heterozygous mouse (Het).\n(B) Total kidney membranes were subjected to endoglycosidase H treatment (Endo H) prior to Western blotting. High-mannose (h.m.) glycosylated proteins that have not exited the ER are sensitive to endoglycosidase H digestion. In humans, recessive alleles of Aqp2 are postulated to cause NDI because they do not properly translocate to the apical cell surface in response to AVP. This postulate comes solely from in vitro studies in which mutant Aqp2 cDNAs corresponding to human disease mutations are transfected into kidney cell lines. In general, such recessive alleles, when visualized immunocytochemically, fail to localize to AVP-responsive vesicles. Rather, they get trapped in the endoplasmic reticulum (ER). Our mouse model of NDI affords the first opportunity to test this hypothesis in a mature animal. As shown in Figure 4A (top row of photomicrographs), AQP2 (stained red) normally localized to the subapical region of collecting duct cells in kidneys of wild-type mice. Upon stimulation with dDAVP, AQP2 translocated to or near the cell surface (Figure 4A, second row). In kidneys taken from mutant animals, however, AQP2 was distributed randomly throughout the cell in the basal state (Figure 4A, third row), while AQP3 (green) appropriately localized to the basolateral surface [23]. Furthermore, upon dDAVP stimulation, AQP2-F204V failed to translocate to the cell surface (Figure 4A, bottom row). To confirm these findings, the staining was repeated in kidneys taken from two further mice for each class, wild-type or mutant, with or without dDAVP treatment, with identical results.\nFigure 4 AQP2 Subcellular Localization and Translocation in Mouse Kidney Collecting Ducts and MDCK Cell Lines\n(A) Immunohistochemistry on collecting ducts in kidney sections from an AQP2-F204V mutant (Mut) mouse and an age-sex matched wild-type (WT) littermate. Mice were injected intraperitoneally with PBS (NT) or dDAVP before sacrificing and fixation of the kidneys. Kidneys sections were immunostained for AQP2 (red) and the basolateral marker AQP3 (green). The images were merged and an area of the cytoplasm was magnified (zoom). Note that mutant AQP2 is not properly localized to the subapical compartment, nor does it respond to dDAVP.\n(B) MDCK cell lines, stably transfected with constructs encoding mouse WT or AQP2-F204V, were treated with and without 150 μM forskolin for 90 min, after which cells were fixed, permeabilized, and subjected to immunocytochemistry. AQP2 is shown in green, and the basolateral marker Na+/K+-ATPase is shown in red, alongside the nuclear stain DAPI. The z-profile images were reconstructed from multiple z-sections, along the dotted line. Mutant AQP2 fails to localize to the cell surface upon forskolin stimulation. Rather, the perinuclear staining is consistent with an ER localization of mutant AQP2.\n(C) The MDCK cell line expressing AQP2-F204V was grown on fibronectin-coated coverslips until tight junctions formed, at which point the cells were treated with 150 μM forskolin for 90 min. Cells were fixed, permeabilized, and sequentially immunoblotted for AQP2 (green) and calnexin (red), an ER marker. The merged image shows that AQP2-F204V colocalizes with the endoplasmic reticulum marker. Scale bar refers to 10 μm. To investigate the mechanism of defective translocation of AQP2-F204V, we turned to transfection of MDCK cells. Stable cell lines expressing mouse wild-type AQP2 and AQP2-F204V were established. Immunoblots of protein extracts from stable cell lines showed that MDCK cells recapitulate the glycosylation defect seen in mutant mice (unpublished data). The wild-type protein was again present in three different forms. Cells expressing AQP2-F204V lacked the 35–45 kDa form and were enriched in the core-glycosylated 31 kDa form.\nIn transfected, unstimulated MDCK cells, wild-type AQP2 (stained green) appeared in a punctate pattern distributed throughout the subapical region (Figure 4B, left column photomicrographs), consistent with vesicular compartmentalization. AQP2-F204V, on the other hand, appeared in a punctate but perinuclear pattern (Figure 4B, third column). Upon stimulation with forskolin, a cAMP-dependent protein kinase activator, wild-type AQP2 translocated to the apical surface of polarized MDCK cells (Figure 4B, second column). Along the z-axis, the perinuclear distribution of AQP2-F204V was clearly seen, and this distribution is not altered by forskolin (Figure 4B, bottom row, two right columns). The perinuclear distribution of AQP2-F204V is consistent with an ER compartmentalization. To test the idea that AQP2-F204V localizes to the ER, we co-stained cells transfected with Aqp2F204V (cDNA) for AQP2 and an ER marker, calnexin (Figure 4C). Colocalization of calnexin with AQP2 was investigated directly, and it was found that 80% of all AQP2-F204V protein colocalized with calnexin. The remaining 20% appeared at the periphery of the ER, representing AQP2-F204V that had potentially progressed beyond the ER. This “ER escape” was consistent with the small proportion of mature, complex glycosylated, AQP2-F204V in mutant kidneys (see Figure 3A).\nAnimals heterozygous for the Aqp2F204V mutation were not affected in their urine production or urine osmolality (see Figure 1C and 1D). It has also been shown that a recessive NDI allele, AQP2-R187C, does not interact with wild-type protein in oocytes [24], nor does it homo-oligomerize in MDCK cells [22]. Therefore, kidneys from heterozygous animals were examined for evidence of two populations of AQP2 protein. Surprisingly, immunohistochemical staining of kidney collecting ducts from Aqp2F204V/+ mice revealed a pattern remarkably similar to wild type (Figure 5A). AQP2 translocated completely to the apical cell surface upon dDAVP stimulation. This wild-type staining pattern may simply reflect the fact that decreasing the amount of mutant protein by half makes it undetectable by immunocytochemistry. Alternatively, the presence of wild-type protein may alter the localization of the mutant protein. Indeed, Hendriks et al. proposed a “piggy-back” mechanism to explain the transport of nonglycosylated subunits of AQP2 to the cell surface by glycosylated subunits [22]. It has also been shown that wild-type AQP2 protein can rescue a translocation-defective mutant protein, AQP2-P262L, when the two are coexpressed in MDCK cells [25].\nFigure 5 AQP2-F204V Rescue in Heterozygous Mouse Collecting Ducts and in Cotransfected MDCK Cells\n(A) In heterozygous animals, AQP2 localizes and responds to dDAVP normally. Immunohistochemistry was carried out on kidney sections from an Aqp2F204V/+ mouse, after injection with dDAVP. Kidney sections were sequentially immunostained for AQP2 (red) and the basolateral marker AQP3 (green).\n(B) Mutant and wild-type AQP2 physically interact. MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP tagged wild-type AQP2, AQP2-F204V, or GFP alone. Solubilized membranes were immunoprecipitated with a GFP antibody. Total membranes and immunoprecipitates (GFP-IP) were Western blotted using an antibody against AQP2 (arrow) or AQP2-GFP fusions (arrowhead).\n(C) Wild-type AQP2 rescues the localization defect of mutant AQP2. GFP fusions of either wild-type AQP2 (WT-GFP, top photomicrographs) or F204V AQP2 (F204V-GFP, bottom photomicrographs) were expressed in polarized MDCK stable cell lines expressing vector alone (vector, left photomicrographs) or AQP2-WT (right photomicrographs). Cells were stimulated with forskolin, processed for immunocytochemistry, and used to generate z-sectional images.\n(D) Mutant AQP2 is present at the cell surface in cells coexpressing wild-type AQP2 (AQP2-WT). GFP fused to AQP2-F204V was expressed in MDCK cells expressing wild-type AQP2 or vector alone. Cells were stimulated with forskolin, and cell surface biotinylated proteins were precipitated then analyzed for the presence of wild-type AQP2 (arrow) and AQP2-F204V (arrowhead) by Western blot. In the collecting ducts from Aqp2F204V/+ mice, the wild type may rescue the mutant protein as suggested by the subcellular distribution of AQP2 protein. To test this idea, we first looked for an interaction between mutant and wild-type proteins in transfected MDCK cells (Figure 5B). MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP expression constructs encoding GFP-tagged wild-type AQP2, AQP2-F204V, or GFP alone. Antibodies against GFP coimmunoprecipitated wild-type AQP2 when AQP2-GFP or AQP2-F204V-GFP was transiently transfected, but not when GFP by itself was transiently transfected into MDCK cells stably expressing wild-type AQP2 (Figure 5B, upper blots). Western blot of total membranes showed that wild-type AQP2 is equivalently expressed in all three cases (Figure 5B, lower blots).\nIf wild-type and mutant proteins are indeed interacting in the cell, is this interaction sufficient to rescue the localization of mutant protein? To answer this question, we used MDCK cells stably transfected with wild-type AQP2 expressing vector or with empty vector. On top of these, we transiently transfected AQP2-GFP or AQP2-F204V-GFP expression constructs. AQP2-GFP localized to the apical surface upon forskolin stimulation whether it was transiently transfected into vector-only cells (Figure 5C, upper left images) or into wild-type AQP2 cells (Figure 5C, upper right). AQP2-F204V-GFP, when expressed by transient transfection into vector only cells, showed a diffuse cytoplasmic distribution pattern (Figure 5C, lower left). When expressed in wild-type AQP2 cells, however, AQP2-F204V-GFP localized to the apical surface to varying degrees (Figure 5C, lower right images [i–iii]). The lower right images of Figure 5C shows three cells from a single transfection. The first is a nontransfected cell that shows the localization of the stably expressing wild-type AQP2, which is apical upon forskolin stimulation. The next two show expression of both the stable wild-type AQP2 and the transient AQP2-F204V-GFP. In cell (ii), localization of wild-type AQP2 was indistinguishable from AQP2-F204V-GFP; both were apical upon forskolin stimulation. Although the effect was subtle in cell (iii), AQP2-F204V-GFP was partly localized to the apical surface. Generally, the localization of AQP2-F204V-GFP was clearly more apical when wild-type AQP2 was also expressed.\nTo confirm these results biochemically, we transfected the same cell lines (wild-type AQP2 or vector) with F204V-GFP, biotinylated surface proteins after forskolin stimulation, and precipitated the biotinylated proteins (Figure 5D). AQP2-F204V-GFP is expressed approximately equally in both cell lines (Figure 5D, total cells), but is biotinylated only when wild-type AQP2 is also expressed (Figure 5D, surface biotinylated). Since only cell surface proteins are accessible to biotin, these results indicate that AQP2-F204V is transported to the cell surface when wild-type AQP2 is present, but not on its own."}

{"project":"2_test","denotations":[{"id":"16121255-15064401-85587788","span":{"begin":180,"end":182},"obj":"15064401"},{"id":"16121255-11567631-85587789","span":{"begin":183,"end":185},"obj":"11567631"},{"id":"16121255-11793119-85587790","span":{"begin":3253,"end":3255},"obj":"11793119"},{"id":"16121255-11035038-85587791","span":{"begin":4008,"end":4010},"obj":"11035038"},{"id":"16121255-9916798-85587792","span":{"begin":5845,"end":5847},"obj":"9916798"},{"id":"16121255-11035038-85587793","span":{"begin":6487,"end":6489},"obj":"11035038"},{"id":"16121255-14593099-85587794","span":{"begin":6490,"end":6492},"obj":"14593099"},{"id":"16121255-14593099-85587795","span":{"begin":6926,"end":6928},"obj":"14593099"},{"id":"16121255-7517548-85587796","span":{"begin":9357,"end":9359},"obj":"7517548"},{"id":"16121255-11929850-85587797","span":{"begin":13458,"end":13460},"obj":"11929850"},{"id":"16121255-14593099-85587798","span":{"begin":13507,"end":13509},"obj":"14593099"},{"id":"16121255-14593099-85587799","span":{"begin":14279,"end":14281},"obj":"14593099"},{"id":"16121255-15509592-85587800","span":{"begin":14444,"end":14446},"obj":"15509592"},{"id":"T47462","span":{"begin":180,"end":182},"obj":"15064401"},{"id":"T2172","span":{"begin":183,"end":185},"obj":"11567631"},{"id":"T493","span":{"begin":3253,"end":3255},"obj":"11793119"},{"id":"T51608","span":{"begin":4008,"end":4010},"obj":"11035038"},{"id":"T17076","span":{"begin":5845,"end":5847},"obj":"9916798"},{"id":"T44574","span":{"begin":6487,"end":6489},"obj":"11035038"},{"id":"T91505","span":{"begin":6490,"end":6492},"obj":"14593099"},{"id":"T46479","span":{"begin":6926,"end":6928},"obj":"14593099"},{"id":"T63600","span":{"begin":9357,"end":9359},"obj":"7517548"},{"id":"T18045","span":{"begin":13458,"end":13460},"obj":"11929850"},{"id":"T35488","span":{"begin":13507,"end":13509},"obj":"14593099"},{"id":"T95687","span":{"begin":14279,"end":14281},"obj":"14593099"},{"id":"T49378","span":{"begin":14444,"end":14446},"obj":"15509592"}],"text":"Results\nIn a forward genetic screen that used ethylnitrosourea (ENU) to induce mutations in a founder animal whose offspring were then screened for abnormal whole body metabolism [19,20], we found a family of mice that urinated and drank excessively. Serum and urine analysis showed that plasma glucose levels were normal and there was no glucose in the urine (unpublished data). Hence, this was an example of diabetes insipidus.\nThe disorder in these mice segregated in a monogenic, autosomal recessive manner, making Aqp2 a candidate gene. Sequencing of Aqp2 coding region of affected mice identified a thymine to guanine (T to G) transversion (Figure 1A), which is predicted to lead to a valine for phenylalanine substitution at amino acid 204 of the protein (F204V).\nFigure 1 Analysis of Aqp2 Sequence and Phenotype in Mutant Mice\n(A) Chromatographic traces of Aqp2 F204V mutation. The box shows the mutated codon, TTC (Phe) to GTC (Val) at position 204.\nWT, wild type; Mut, mutant.\n(B) Amino acid conservation of mouse AQP2 (residues 194–214). The boxed residue indicates phenylalanine at position 204.\nhAQP2, human AQP2; mAQP1, mouse AQP1; mAQP2, mouse AQP2; rAQP2, rat AQP2; xAQP2, Xenopus AQP2.\n(C) Urine production (ml) and water consumption (ml) of 58 F2 mice over a 24-h period (both sexes, aged 10–22 wk). Mutant mice (black squares) exhibit overt polyuria and polydipsia compared to littermate wild-type (white triangles) and heterozygous (grey circles) mice.\n(D) Urine osmolality and concentrating ability in Aqp2 mutant and their littermates (10–22 wk, both sexes), before (white bars) and after (black bars) dDAVP treatment. Wild type (WT; n = 12); heterozygote (Het; n = 20); mutant (Mut; n = 9). Data represent averages ± standard error of the mean, **p \u003c 0.01; ***p \u003c 0.001. AQP2 is a six-transmembrane water channel, and F204 lies near the extracellular face of the sixth membrane spanning domain, a region rich in hydrophobic amino acids. This and the other membrane-spanning domains are conserved among vertebrate species. The phenylalanine at position 204 is particularly well conserved (Figure 1B), not only among vertebrate AQP2 proteins, but also among others members of this family.\nAqp2F204V/F204V mice have dramatically increased urine production, in some cases producing an amount of urine in 24 h that exceeds their body weight, compared to their heterozygous or wild-type littermates. Such loss of water would rapidly lead to dehydration were it not compensated by increased water intake. Indeed, mutant mice also dramatically increase their water intake (Figure 1C) compared to their heterozygous or wild-type littermates. This phenotype—increased urinary output and water intake—showed complete concordance with homozygosity of the F204V mutation in the 58 animals tested.\nDiabetes insipidus can be defined as an inability to concentrate urine where appropriate. Compared to wild-type or heterozygous littermates, Aqp2F204V/F204V mice produce very dilute urine (Figure 1D). Basal urine concentration in mutant mice is about 161 mOsm, compared to about 1,293 mOsm in wild-type mice (p \u003c 0.001). Normally, urine concentration is under the control of the hypothalamus, which, in response to hypovolemia or hypernatremia [21], secretes AVP. The synthetic AVP analog, 1-deamino-8-D-arginine vasopressin (dDAVP; also called desmopressin), is a potent agonist of AVPR2. When administered to wild-type mice, dDAVP leads to a dramatic increase in urine concentration, from 1,293 to 5,885 mOsm (4.6-fold; Figure 1D). With similar treatment, mutant mice concentrate their urine to a lesser but still significant extent, from 161 to 470 mOsm (2.9-fold), indicating that these animals are not only unable to concentrate their urine properly but are also defective in their response to dDAVP. The smaller response to dDAVP indicates some residual activity of the mutant AQP2 channel, which must be sufficient to allow survival of the individual, in contrast to the T126M knock-in mouse [18].\nMultiple heterozygous matings yielded 101 animals, which appeared at a ratio of 26:49:26, near the expected Mendelian wild type, heterozygote, and mutant frequencies, respectively, indicating that there is no reduced viability associated with this mutation. Other than the increased urine production and water intake, there was no overt phenotype in mutant mice, save distended kidneys, which appeared variably in adult animals (Figure 2A). Although not specifically measured, mutant mice seem to have a normal lifespan. The one animal that was followed lived to 18 mo, typical for animals in our colony.\nFigure 2 Anatomy and Histology of Mouse Kidneys\n(A) Gross anatomy of an affected mouse (8-mo-old male). This shows the enlargement and cystic dilatation of the renal pelvis. There is thinning of the overlying renal parenchyma imparting a translucent appearance to portions of the kidney and collecting system. The bladder is also dilated.\n(B) Left kidney from mutant mouse (right) shown in (A) compared to a kidney from an age-sex matched unaffected littermate (left).\n(C) Hematoxylin and eosin stained section of ureter from a mutant mouse, showing normal histology despite bloating of the kidney.\n(D) Hematoxylin and eosin stained histologic section of a kidney from a 4-wk-old female mutant mouse. The mutant kidney shows marked dilatation of the renal pelvis with blunting of the papilla. There is preservation of the cortex and medulla. Aqp2F204V/F204V mice suffer from severe hydronephrosis (Figure 2A and 2B), presumably as a consequence of an inability to cope with the extreme polyuria. We found distended kidneys in all Aqp2F204V/F204V mice; however, the degree of inflation was variable in affected mice and worsened with age. Severe hydronephrosis has previously been observed in double Aqp1/Aqp3 knock-out mice [17], and appears at 6 wk. Even at 4 wk, Aqp2F204V/F204V mice had hydronephrosis. Histologic sections from Aqp2F204V/F204V mice demonstrated marked dilatation of the renal pelvis yet normal morphology of the ureter (Figure 2C and 2D). In particular, the muscularis propria was neither hypertrophied nor thinned. There was the normal festooned appearance of the urothelium, and this transitional epithelium was of normal thickness. There was thinning of the kidney as measured from renal capsule to renal pelvis. However, the morphologic features of the glomeruli and proximal/distal tubules were unremarkable (Figure 2D).\nAs shown previously [18,22], immunoblotting revealed three different forms of AQP2, due to different degrees and forms of glycosylation (Figure 3A). Previous reports have demonstrated that nonglycosylated protein appears as a 29 kDa band, while complex glycosylated protein runs as a smear between 35 and 45 kDa. A short-lived intermediate form of 31 kDa representing core, high-mannose glycosylation of AQP2 is apparent from pulse-chase labeling experiments [22]. Compared to that from the kidneys of wild-type animals, AQP2 from mutant animals was reduced in both the high molecular weight, diffuse form and the lowest molecular weight form, but enriched in the intermediate molecular weight form (Figure 3A). Heterozygous animals showed intermediate amounts of all three forms. The nature of these glycosylated forms was revealed by digestion with endoglycosidase H, which specifically cleaves mannose-rich carbohydrate from the protein backbone. Treatment of endogenous AQP2 from kidneys of wild-type, heterozygous, and mutant animals specifically affected the intermediate molecular weight form (Figure 3B). The presence of some mature glycosylated proteins (35–45 kDa) in Aqp2F204V/F204V mice presumably permits their survival compared to Aqp2T126M/T126M mice, and is consistent with a diminished response to dDAVP.\nFigure 3 Immunoblot Analyses of AQP2 from Mouse Kidneys\n(A) Western blot analyses of total kidney membranes from littermate mice. An intermediate form of AQP2 at 31 kDa was identified in kidney membranes from a mutant mouse (Mut) and partially in a heterozygous mouse (Het).\n(B) Total kidney membranes were subjected to endoglycosidase H treatment (Endo H) prior to Western blotting. High-mannose (h.m.) glycosylated proteins that have not exited the ER are sensitive to endoglycosidase H digestion. In humans, recessive alleles of Aqp2 are postulated to cause NDI because they do not properly translocate to the apical cell surface in response to AVP. This postulate comes solely from in vitro studies in which mutant Aqp2 cDNAs corresponding to human disease mutations are transfected into kidney cell lines. In general, such recessive alleles, when visualized immunocytochemically, fail to localize to AVP-responsive vesicles. Rather, they get trapped in the endoplasmic reticulum (ER). Our mouse model of NDI affords the first opportunity to test this hypothesis in a mature animal. As shown in Figure 4A (top row of photomicrographs), AQP2 (stained red) normally localized to the subapical region of collecting duct cells in kidneys of wild-type mice. Upon stimulation with dDAVP, AQP2 translocated to or near the cell surface (Figure 4A, second row). In kidneys taken from mutant animals, however, AQP2 was distributed randomly throughout the cell in the basal state (Figure 4A, third row), while AQP3 (green) appropriately localized to the basolateral surface [23]. Furthermore, upon dDAVP stimulation, AQP2-F204V failed to translocate to the cell surface (Figure 4A, bottom row). To confirm these findings, the staining was repeated in kidneys taken from two further mice for each class, wild-type or mutant, with or without dDAVP treatment, with identical results.\nFigure 4 AQP2 Subcellular Localization and Translocation in Mouse Kidney Collecting Ducts and MDCK Cell Lines\n(A) Immunohistochemistry on collecting ducts in kidney sections from an AQP2-F204V mutant (Mut) mouse and an age-sex matched wild-type (WT) littermate. Mice were injected intraperitoneally with PBS (NT) or dDAVP before sacrificing and fixation of the kidneys. Kidneys sections were immunostained for AQP2 (red) and the basolateral marker AQP3 (green). The images were merged and an area of the cytoplasm was magnified (zoom). Note that mutant AQP2 is not properly localized to the subapical compartment, nor does it respond to dDAVP.\n(B) MDCK cell lines, stably transfected with constructs encoding mouse WT or AQP2-F204V, were treated with and without 150 μM forskolin for 90 min, after which cells were fixed, permeabilized, and subjected to immunocytochemistry. AQP2 is shown in green, and the basolateral marker Na+/K+-ATPase is shown in red, alongside the nuclear stain DAPI. The z-profile images were reconstructed from multiple z-sections, along the dotted line. Mutant AQP2 fails to localize to the cell surface upon forskolin stimulation. Rather, the perinuclear staining is consistent with an ER localization of mutant AQP2.\n(C) The MDCK cell line expressing AQP2-F204V was grown on fibronectin-coated coverslips until tight junctions formed, at which point the cells were treated with 150 μM forskolin for 90 min. Cells were fixed, permeabilized, and sequentially immunoblotted for AQP2 (green) and calnexin (red), an ER marker. The merged image shows that AQP2-F204V colocalizes with the endoplasmic reticulum marker. Scale bar refers to 10 μm. To investigate the mechanism of defective translocation of AQP2-F204V, we turned to transfection of MDCK cells. Stable cell lines expressing mouse wild-type AQP2 and AQP2-F204V were established. Immunoblots of protein extracts from stable cell lines showed that MDCK cells recapitulate the glycosylation defect seen in mutant mice (unpublished data). The wild-type protein was again present in three different forms. Cells expressing AQP2-F204V lacked the 35–45 kDa form and were enriched in the core-glycosylated 31 kDa form.\nIn transfected, unstimulated MDCK cells, wild-type AQP2 (stained green) appeared in a punctate pattern distributed throughout the subapical region (Figure 4B, left column photomicrographs), consistent with vesicular compartmentalization. AQP2-F204V, on the other hand, appeared in a punctate but perinuclear pattern (Figure 4B, third column). Upon stimulation with forskolin, a cAMP-dependent protein kinase activator, wild-type AQP2 translocated to the apical surface of polarized MDCK cells (Figure 4B, second column). Along the z-axis, the perinuclear distribution of AQP2-F204V was clearly seen, and this distribution is not altered by forskolin (Figure 4B, bottom row, two right columns). The perinuclear distribution of AQP2-F204V is consistent with an ER compartmentalization. To test the idea that AQP2-F204V localizes to the ER, we co-stained cells transfected with Aqp2F204V (cDNA) for AQP2 and an ER marker, calnexin (Figure 4C). Colocalization of calnexin with AQP2 was investigated directly, and it was found that 80% of all AQP2-F204V protein colocalized with calnexin. The remaining 20% appeared at the periphery of the ER, representing AQP2-F204V that had potentially progressed beyond the ER. This “ER escape” was consistent with the small proportion of mature, complex glycosylated, AQP2-F204V in mutant kidneys (see Figure 3A).\nAnimals heterozygous for the Aqp2F204V mutation were not affected in their urine production or urine osmolality (see Figure 1C and 1D). It has also been shown that a recessive NDI allele, AQP2-R187C, does not interact with wild-type protein in oocytes [24], nor does it homo-oligomerize in MDCK cells [22]. Therefore, kidneys from heterozygous animals were examined for evidence of two populations of AQP2 protein. Surprisingly, immunohistochemical staining of kidney collecting ducts from Aqp2F204V/+ mice revealed a pattern remarkably similar to wild type (Figure 5A). AQP2 translocated completely to the apical cell surface upon dDAVP stimulation. This wild-type staining pattern may simply reflect the fact that decreasing the amount of mutant protein by half makes it undetectable by immunocytochemistry. Alternatively, the presence of wild-type protein may alter the localization of the mutant protein. Indeed, Hendriks et al. proposed a “piggy-back” mechanism to explain the transport of nonglycosylated subunits of AQP2 to the cell surface by glycosylated subunits [22]. It has also been shown that wild-type AQP2 protein can rescue a translocation-defective mutant protein, AQP2-P262L, when the two are coexpressed in MDCK cells [25].\nFigure 5 AQP2-F204V Rescue in Heterozygous Mouse Collecting Ducts and in Cotransfected MDCK Cells\n(A) In heterozygous animals, AQP2 localizes and responds to dDAVP normally. Immunohistochemistry was carried out on kidney sections from an Aqp2F204V/+ mouse, after injection with dDAVP. Kidney sections were sequentially immunostained for AQP2 (red) and the basolateral marker AQP3 (green).\n(B) Mutant and wild-type AQP2 physically interact. MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP tagged wild-type AQP2, AQP2-F204V, or GFP alone. Solubilized membranes were immunoprecipitated with a GFP antibody. Total membranes and immunoprecipitates (GFP-IP) were Western blotted using an antibody against AQP2 (arrow) or AQP2-GFP fusions (arrowhead).\n(C) Wild-type AQP2 rescues the localization defect of mutant AQP2. GFP fusions of either wild-type AQP2 (WT-GFP, top photomicrographs) or F204V AQP2 (F204V-GFP, bottom photomicrographs) were expressed in polarized MDCK stable cell lines expressing vector alone (vector, left photomicrographs) or AQP2-WT (right photomicrographs). Cells were stimulated with forskolin, processed for immunocytochemistry, and used to generate z-sectional images.\n(D) Mutant AQP2 is present at the cell surface in cells coexpressing wild-type AQP2 (AQP2-WT). GFP fused to AQP2-F204V was expressed in MDCK cells expressing wild-type AQP2 or vector alone. Cells were stimulated with forskolin, and cell surface biotinylated proteins were precipitated then analyzed for the presence of wild-type AQP2 (arrow) and AQP2-F204V (arrowhead) by Western blot. In the collecting ducts from Aqp2F204V/+ mice, the wild type may rescue the mutant protein as suggested by the subcellular distribution of AQP2 protein. To test this idea, we first looked for an interaction between mutant and wild-type proteins in transfected MDCK cells (Figure 5B). MDCK cells stably expressing wild-type AQP2 were transiently transfected with GFP expression constructs encoding GFP-tagged wild-type AQP2, AQP2-F204V, or GFP alone. Antibodies against GFP coimmunoprecipitated wild-type AQP2 when AQP2-GFP or AQP2-F204V-GFP was transiently transfected, but not when GFP by itself was transiently transfected into MDCK cells stably expressing wild-type AQP2 (Figure 5B, upper blots). Western blot of total membranes showed that wild-type AQP2 is equivalently expressed in all three cases (Figure 5B, lower blots).\nIf wild-type and mutant proteins are indeed interacting in the cell, is this interaction sufficient to rescue the localization of mutant protein? To answer this question, we used MDCK cells stably transfected with wild-type AQP2 expressing vector or with empty vector. On top of these, we transiently transfected AQP2-GFP or AQP2-F204V-GFP expression constructs. AQP2-GFP localized to the apical surface upon forskolin stimulation whether it was transiently transfected into vector-only cells (Figure 5C, upper left images) or into wild-type AQP2 cells (Figure 5C, upper right). AQP2-F204V-GFP, when expressed by transient transfection into vector only cells, showed a diffuse cytoplasmic distribution pattern (Figure 5C, lower left). When expressed in wild-type AQP2 cells, however, AQP2-F204V-GFP localized to the apical surface to varying degrees (Figure 5C, lower right images [i–iii]). The lower right images of Figure 5C shows three cells from a single transfection. The first is a nontransfected cell that shows the localization of the stably expressing wild-type AQP2, which is apical upon forskolin stimulation. The next two show expression of both the stable wild-type AQP2 and the transient AQP2-F204V-GFP. In cell (ii), localization of wild-type AQP2 was indistinguishable from AQP2-F204V-GFP; both were apical upon forskolin stimulation. Although the effect was subtle in cell (iii), AQP2-F204V-GFP was partly localized to the apical surface. Generally, the localization of AQP2-F204V-GFP was clearly more apical when wild-type AQP2 was also expressed.\nTo confirm these results biochemically, we transfected the same cell lines (wild-type AQP2 or vector) with F204V-GFP, biotinylated surface proteins after forskolin stimulation, and precipitated the biotinylated proteins (Figure 5D). AQP2-F204V-GFP is expressed approximately equally in both cell lines (Figure 5D, total cells), but is biotinylated only when wild-type AQP2 is also expressed (Figure 5D, surface biotinylated). Since only cell surface proteins are accessible to biotin, these results indicate that AQP2-F204V is transported to the cell surface when wild-type AQP2 is present, but not on its own."}