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is required for the differentiation of multiple organ systems during development\nIn this study, we have generated a null mutation in the phosphatidylserine receptor (Ptdsr) gene in C57BL/6J mice. We show that ablation of Ptdsr results in profound differentiation defects in multiple organs and tissues during embryogenesis, although with variable penetrance. While this work was in progress, two other groups reported the generation of Ptdsr-deficient mice [31,32]. In all three knockout mouse lines, the first two exons ([31] and this study) or exons one to three [32] were deleted by replacement with a neomycin-selection cassette. The Ptdsr-knockout mouse lines differ in the genetic background in which the mutation was generated and maintained, however. In our case, the Ptdsr-null allele was generated in an isogenic C57BL/6J background, whereas Li et al. [31] and Kunisaki et al. [32] investigated the phenotype of their Ptdsr-knockout mice in a mixed 129 × C57BL/6 background. The ablation of Ptdsr function results in perinatal lethality in all cases, but there are interesting differences in severity or expressivities of phenotypes among the different Ptdsr-deficient mouse lines. This might be due either to differences in genetic background or because the phenotypes that have been investigated in this study have not been analyzed in such detail before.\nIn the Ptdsr-knockout mouse line reported here, growth retardation started from E12.5 onwards and was associated with delayed differentiation in several organs in which Ptdsr is expressed either during embryogenesis or later in adulthood. At E16.5 almost no branching morphogenesis of the lung epithelium was observed in Ptdsr -/- lungs. Similarly, epithelial structures were only partially developed in mutant kidneys, without terminal differentiation of Bowman's capsule and with a severe reduction in the number of differentiated collecting tubules. Likewise, the differentiation of the intestine was also severely delayed at this developmental stage. When compared with wild-type controls, intestinal tissues of Ptdsr knockout mice appeared unstructured, with an absence of enteric ganglia and of differentiated smooth muscle tissue. Interestingly, defects in kidney and intestine differentiation were not described in the Ptdsr-knockouts generated by Li et al. [31] and Kunisaki et al. [32]. Surprisingly, when we examined Ptdsr-/- embryos shortly before birth (E18.5) or neonatally, we found only mild differentiation delays in organs that appeared severely affected at mid-gestation. This 'recovery' was most visible in Ptdsr -/- lungs: at P0 we found expanded lungs in the knockout mice that showed normal branching patterns, with differentiated alveoli and bronchioles.\nWe investigated the occurrence of programmed cell death during lung development in wild-type and Ptdsr-knockout mice throughout embryogenesis (E16.5 to P0). Comparative immunohistochemistry for aCasp3 revealed that apoptosis is a rare event during lung morphogenesis. Furthermore, we failed to detect any differences in the number of apoptotic cells in Ptdsr-knockout and wild-type animals in the rare cases where we could detect apoptotic cells within lung tissues. These findings are contrary to the results reported by Li et al. [31], who suggested that impaired clearance of apoptotic mesenchymal and epithelial cells causes a failure in lung morphogenesis in Ptdsr-deficient mice. In contrast, our findings are in line with the current view on lung development during embryogenesis. Accordingly, formation of the epithelial lung via branching morphogenesis can be subdivided into a series of sequential steps that involve: first, formation of the organ anlage in the form of a placode; second, primary bud formation by placode invagination; third, branch initiation and branch outgrowth; fourth, further reiteration of the branching process; and fifth, terminal differentiation of organ-specific proximal and distal structures [34,35]. In contrast to other invagination processes during embryogenesis, such as mammary gland formation, the lumen of the lungs is expanded by successive branching events, branch outgrowth and elongation, rather than by apoptosis [34,36]. Finally, because the lungs of Ptdsr -/-neonates were almost fully expanded and appeared normal in structure in comparison to wild-type littermates, it is highly unlikely that Ptdsr mutants die of respiratory lung failure. In addition, Li and colleagues [31] demonstrated that surfactant expression is normal in Ptdsr-deficient animals, supporting the idea of normal maturation of surfactant-producing type II alveolar epithelial cells and lung function. Other defects must therefore be responsible for the death of Ptdsr-mutant mice. The frequently observed subcutaneous edema of various extents in Ptdsr-deficient homozygotes gave us a hint that Ptdsr-deficiency and lethality might be associated with cardiovascular problems. Indeed, very recently we have obtained strong evidence that Ptdsr-knockout mice die as a result of defects in heart development that are associated with specific cardiopulmonary malformations; (J.E. Schneider, J.B., S.D. Bamfort, A.D.G., C. Broadbent, K. Clarke, S. Neubauer, A.L. and S. Battacharya, unpublished observations).\nIn addition, we demonstrate that eye development requires a functional Ptdsr gene. Ptdsr-deficient embryos can be roughly divided into two categories. The first, severely affected group develops anophthalmia that correlates with formation of ectopic retinal-pigmented epithelium and induction of proliferation of underlying mesenchyme in the nasal cavity. This phenotype represents a completely novel lesion that to our knowledge has not been described before in any other mouse mutant. The second group shows normal external eye structures, although in this case retinal development is temporally delayed during mid-gestation, with persistent, abnormal morphogenesis of the inner granular retinal layer at later stages of embryogenesis. A possible explanation for these two phenotypes can be found in the expression pattern of the Ptdsr gene. Initially, Ptdsr is expressed throughout the whole developing nervous system, with exceptionally high levels in the anterior part of the forebrain. Later expression becomes more restricted to the developing retina and lens. Thus, Ptdsr might play an important role in early events of ocular morphogenesis, such as establishment and bisection of eye fields and formation of optic cups. These early eye-formation steps are closely interconnected with development of the forebrain [37,38] and the nose [39-41].\nInterestingly, we occasionally observed serious malformations of forebrain and nasal structures in Ptdsr-knockout embryos that were associated with bilateral anophthalmia (see for example the mutant embryo in Figure 1g). This suggests that Ptdsr is involved in the regulation of differentiation processes within forebrain regions, and that ablation of Ptdsr function might secondarily affect early eye formation. Li et al. [31] found smaller lenses in Ptdsr-knockout mice and described the formation of retinal protrusions, although anophthalmia and specific differentiation defects of retinal cell layers were not reported in their study. Li et al. proposed [31] that the eye phenotype they observed could be explained by failed removal of apoptotic cells during eye development, but we think that the observed defects are unrelated to a failure of apoptotic cell clearance. A recent comprehensive kinetic analysis of apoptosis induction during mouse retinal development described four major peaks of apoptotic cell death [42]. This study demonstrated that there is an initial phase of cell death during the invagination of the optic cup (E10.5), followed by subsequent waves of apoptosis induction immediately before and after birth (E18.5 to postnatal day P2), and from postnatal days P9 to P10 and P14 to P16 [42]. Thus, besides the formation of the inner and outer layers of the optic cup in early eye development, other major phases of retinal cell apoptosis take place only postnatally and correspond to important periods in the establishment of neuronal connections. Furthermore, cell death during normal retinal development occurs in retinal layers distinct from the inner granular layer where we observed the most pronounced differentiation defects in the Ptdsr -/- mutants described here. Other studies that connect the postnatal elimination of apoptotic photoreceptor cells to Ptdsr-mediated macrophage engulfment [43] should be interpreted with extreme caution as these studies were based on the monoclonal anti-Ptdsr antibody mAb 217G8E9 [26,43] (see below).\nConsistent with the results of Li et al. [31], we found particular brain malformations in our Ptdsr -/- mice. Exencephaly and hyperplastic brain phenotypes were observed at a low penetrance in Ptdsr-mutant mice (less then 4.5% of homozygotes), but these do not resemble to any extent the brain-overgrowth phenotypes of caspase- or Apaf1-knockout mice ([44], and references therein) in that we failed to identify any differences in the number or distribution of apoptotic cells or pyknotic cell clusters in the neuroepithelium of Ptdsr -/- and Ptdsr+/+ mice. Thus, reduced cell death or diminished clearance of apoptotic neural progenitor cells is unlikely to be the cause of the brain hyperplasia.\nIn summary, our studies demonstrate that Ptdsr is required for normal tissue differentiation, especially during the mid-gestation period when we observed the most severe differentiation delays in several organs of Ptdsr-knockout mice. The multiple defects in tissue differentiation cannot be explained by failure of apoptotic cell clearance, as this process is normal in our Ptdsr-knockout line. This result therefore indicates that Ptdsr has a novel, hitherto unexpected, role in promoting tissue maturation and terminal differentiation. Additional studies with conditionally targeted Ptdsr-deficient mice are required to investigate the role of spatial and temporal Ptdsr expression and function during tissue differentiation."}

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is required for the differentiation of multiple organ systems during development\nIn this study, we have generated a null mutation in the phosphatidylserine receptor (Ptdsr) gene in C57BL/6J mice. We show that ablation of Ptdsr results in profound differentiation defects in multiple organs and tissues during embryogenesis, although with variable penetrance. While this work was in progress, two other groups reported the generation of Ptdsr-deficient mice [31,32]. In all three knockout mouse lines, the first two exons ([31] and this study) or exons one to three [32] were deleted by replacement with a neomycin-selection cassette. The Ptdsr-knockout mouse lines differ in the genetic background in which the mutation was generated and maintained, however. In our case, the Ptdsr-null allele was generated in an isogenic C57BL/6J background, whereas Li et al. [31] and Kunisaki et al. [32] investigated the phenotype of their Ptdsr-knockout mice in a mixed 129 × C57BL/6 background. The ablation of Ptdsr function results in perinatal lethality in all cases, but there are interesting differences in severity or expressivities of phenotypes among the different Ptdsr-deficient mouse lines. This might be due either to differences in genetic background or because the phenotypes that have been investigated in this study have not been analyzed in such detail before.\nIn the Ptdsr-knockout mouse line reported here, growth retardation started from E12.5 onwards and was associated with delayed differentiation in several organs in which Ptdsr is expressed either during embryogenesis or later in adulthood. At E16.5 almost no branching morphogenesis of the lung epithelium was observed in Ptdsr -/- lungs. Similarly, epithelial structures were only partially developed in mutant kidneys, without terminal differentiation of Bowman's capsule and with a severe reduction in the number of differentiated collecting tubules. Likewise, the differentiation of the intestine was also severely delayed at this developmental stage. When compared with wild-type controls, intestinal tissues of Ptdsr knockout mice appeared unstructured, with an absence of enteric ganglia and of differentiated smooth muscle tissue. Interestingly, defects in kidney and intestine differentiation were not described in the Ptdsr-knockouts generated by Li et al. [31] and Kunisaki et al. [32]. Surprisingly, when we examined Ptdsr-/- embryos shortly before birth (E18.5) or neonatally, we found only mild differentiation delays in organs that appeared severely affected at mid-gestation. This 'recovery' was most visible in Ptdsr -/- lungs: at P0 we found expanded lungs in the knockout mice that showed normal branching patterns, with differentiated alveoli and bronchioles.\nWe investigated the occurrence of programmed cell death during lung development in wild-type and Ptdsr-knockout mice throughout embryogenesis (E16.5 to P0). Comparative immunohistochemistry for aCasp3 revealed that apoptosis is a rare event during lung morphogenesis. Furthermore, we failed to detect any differences in the number of apoptotic cells in Ptdsr-knockout and wild-type animals in the rare cases where we could detect apoptotic cells within lung tissues. These findings are contrary to the results reported by Li et al. [31], who suggested that impaired clearance of apoptotic mesenchymal and epithelial cells causes a failure in lung morphogenesis in Ptdsr-deficient mice. In contrast, our findings are in line with the current view on lung development during embryogenesis. Accordingly, formation of the epithelial lung via branching morphogenesis can be subdivided into a series of sequential steps that involve: first, formation of the organ anlage in the form of a placode; second, primary bud formation by placode invagination; third, branch initiation and branch outgrowth; fourth, further reiteration of the branching process; and fifth, terminal differentiation of organ-specific proximal and distal structures [34,35]. In contrast to other invagination processes during embryogenesis, such as mammary gland formation, the lumen of the lungs is expanded by successive branching events, branch outgrowth and elongation, rather than by apoptosis [34,36]. Finally, because the lungs of Ptdsr -/-neonates were almost fully expanded and appeared normal in structure in comparison to wild-type littermates, it is highly unlikely that Ptdsr mutants die of respiratory lung failure. In addition, Li and colleagues [31] demonstrated that surfactant expression is normal in Ptdsr-deficient animals, supporting the idea of normal maturation of surfactant-producing type II alveolar epithelial cells and lung function. Other defects must therefore be responsible for the death of Ptdsr-mutant mice. The frequently observed subcutaneous edema of various extents in Ptdsr-deficient homozygotes gave us a hint that Ptdsr-deficiency and lethality might be associated with cardiovascular problems. Indeed, very recently we have obtained strong evidence that Ptdsr-knockout mice die as a result of defects in heart development that are associated with specific cardiopulmonary malformations; (J.E. Schneider, J.B., S.D. Bamfort, A.D.G., C. Broadbent, K. Clarke, S. Neubauer, A.L. and S. Battacharya, unpublished observations).\nIn addition, we demonstrate that eye development requires a functional Ptdsr gene. Ptdsr-deficient embryos can be roughly divided into two categories. The first, severely affected group develops anophthalmia that correlates with formation of ectopic retinal-pigmented epithelium and induction of proliferation of underlying mesenchyme in the nasal cavity. This phenotype represents a completely novel lesion that to our knowledge has not been described before in any other mouse mutant. The second group shows normal external eye structures, although in this case retinal development is temporally delayed during mid-gestation, with persistent, abnormal morphogenesis of the inner granular retinal layer at later stages of embryogenesis. A possible explanation for these two phenotypes can be found in the expression pattern of the Ptdsr gene. Initially, Ptdsr is expressed throughout the whole developing nervous system, with exceptionally high levels in the anterior part of the forebrain. Later expression becomes more restricted to the developing retina and lens. Thus, Ptdsr might play an important role in early events of ocular morphogenesis, such as establishment and bisection of eye fields and formation of optic cups. These early eye-formation steps are closely interconnected with development of the forebrain [37,38] and the nose [39-41].\nInterestingly, we occasionally observed serious malformations of forebrain and nasal structures in Ptdsr-knockout embryos that were associated with bilateral anophthalmia (see for example the mutant embryo in Figure 1g). This suggests that Ptdsr is involved in the regulation of differentiation processes within forebrain regions, and that ablation of Ptdsr function might secondarily affect early eye formation. Li et al. [31] found smaller lenses in Ptdsr-knockout mice and described the formation of retinal protrusions, although anophthalmia and specific differentiation defects of retinal cell layers were not reported in their study. Li et al. proposed [31] that the eye phenotype they observed could be explained by failed removal of apoptotic cells during eye development, but we think that the observed defects are unrelated to a failure of apoptotic cell clearance. A recent comprehensive kinetic analysis of apoptosis induction during mouse retinal development described four major peaks of apoptotic cell death [42]. This study demonstrated that there is an initial phase of cell death during the invagination of the optic cup (E10.5), followed by subsequent waves of apoptosis induction immediately before and after birth (E18.5 to postnatal day P2), and from postnatal days P9 to P10 and P14 to P16 [42]. Thus, besides the formation of the inner and outer layers of the optic cup in early eye development, other major phases of retinal cell apoptosis take place only postnatally and correspond to important periods in the establishment of neuronal connections. Furthermore, cell death during normal retinal development occurs in retinal layers distinct from the inner granular layer where we observed the most pronounced differentiation defects in the Ptdsr -/- mutants described here. Other studies that connect the postnatal elimination of apoptotic photoreceptor cells to Ptdsr-mediated macrophage engulfment [43] should be interpreted with extreme caution as these studies were based on the monoclonal anti-Ptdsr antibody mAb 217G8E9 [26,43] (see below).\nConsistent with the results of Li et al. [31], we found particular brain malformations in our Ptdsr -/- mice. Exencephaly and hyperplastic brain phenotypes were observed at a low penetrance in Ptdsr-mutant mice (less then 4.5% of homozygotes), but these do not resemble to any extent the brain-overgrowth phenotypes of caspase- or Apaf1-knockout mice ([44], and references therein) in that we failed to identify any differences in the number or distribution of apoptotic cells or pyknotic cell clusters in the neuroepithelium of Ptdsr -/- and Ptdsr+/+ mice. Thus, reduced cell death or diminished clearance of apoptotic neural progenitor cells is unlikely to be the cause of the brain hyperplasia.\nIn summary, our studies demonstrate that Ptdsr is required for normal tissue differentiation, especially during the mid-gestation period when we observed the most severe differentiation delays in several organs of Ptdsr-knockout mice. The multiple defects in tissue differentiation cannot be explained by failure of apoptotic cell clearance, as this process is normal in our Ptdsr-knockout line. This result therefore indicates that Ptdsr has a novel, hitherto unexpected, role in promoting tissue maturation and terminal differentiation. Additional studies with conditionally targeted Ptdsr-deficient mice are required to investigate the role of spatial and temporal Ptdsr expression and function during tissue differentiation."}

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is required for the differentiation of multiple organ systems during development\nIn this study, we have generated a null mutation in the phosphatidylserine receptor (Ptdsr) gene in C57BL/6J mice. We show that ablation of Ptdsr results in profound differentiation defects in multiple organs and tissues during embryogenesis, although with variable penetrance. While this work was in progress, two other groups reported the generation of Ptdsr-deficient mice [31,32]. In all three knockout mouse lines, the first two exons ([31] and this study) or exons one to three [32] were deleted by replacement with a neomycin-selection cassette. The Ptdsr-knockout mouse lines differ in the genetic background in which the mutation was generated and maintained, however. In our case, the Ptdsr-null allele was generated in an isogenic C57BL/6J background, whereas Li et al. [31] and Kunisaki et al. [32] investigated the phenotype of their Ptdsr-knockout mice in a mixed 129 × C57BL/6 background. The ablation of Ptdsr function results in perinatal lethality in all cases, but there are interesting differences in severity or expressivities of phenotypes among the different Ptdsr-deficient mouse lines. This might be due either to differences in genetic background or because the phenotypes that have been investigated in this study have not been analyzed in such detail before.\nIn the Ptdsr-knockout mouse line reported here, growth retardation started from E12.5 onwards and was associated with delayed differentiation in several organs in which Ptdsr is expressed either during embryogenesis or later in adulthood. At E16.5 almost no branching morphogenesis of the lung epithelium was observed in Ptdsr -/- lungs. Similarly, epithelial structures were only partially developed in mutant kidneys, without terminal differentiation of Bowman's capsule and with a severe reduction in the number of differentiated collecting tubules. Likewise, the differentiation of the intestine was also severely delayed at this developmental stage. When compared with wild-type controls, intestinal tissues of Ptdsr knockout mice appeared unstructured, with an absence of enteric ganglia and of differentiated smooth muscle tissue. Interestingly, defects in kidney and intestine differentiation were not described in the Ptdsr-knockouts generated by Li et al. [31] and Kunisaki et al. [32]. Surprisingly, when we examined Ptdsr-/- embryos shortly before birth (E18.5) or neonatally, we found only mild differentiation delays in organs that appeared severely affected at mid-gestation. This 'recovery' was most visible in Ptdsr -/- lungs: at P0 we found expanded lungs in the knockout mice that showed normal branching patterns, with differentiated alveoli and bronchioles.\nWe investigated the occurrence of programmed cell death during lung development in wild-type and Ptdsr-knockout mice throughout embryogenesis (E16.5 to P0). Comparative immunohistochemistry for aCasp3 revealed that apoptosis is a rare event during lung morphogenesis. Furthermore, we failed to detect any differences in the number of apoptotic cells in Ptdsr-knockout and wild-type animals in the rare cases where we could detect apoptotic cells within lung tissues. These findings are contrary to the results reported by Li et al. [31], who suggested that impaired clearance of apoptotic mesenchymal and epithelial cells causes a failure in lung morphogenesis in Ptdsr-deficient mice. In contrast, our findings are in line with the current view on lung development during embryogenesis. Accordingly, formation of the epithelial lung via branching morphogenesis can be subdivided into a series of sequential steps that involve: first, formation of the organ anlage in the form of a placode; second, primary bud formation by placode invagination; third, branch initiation and branch outgrowth; fourth, further reiteration of the branching process; and fifth, terminal differentiation of organ-specific proximal and distal structures [34,35]. In contrast to other invagination processes during embryogenesis, such as mammary gland formation, the lumen of the lungs is expanded by successive branching events, branch outgrowth and elongation, rather than by apoptosis [34,36]. Finally, because the lungs of Ptdsr -/-neonates were almost fully expanded and appeared normal in structure in comparison to wild-type littermates, it is highly unlikely that Ptdsr mutants die of respiratory lung failure. In addition, Li and colleagues [31] demonstrated that surfactant expression is normal in Ptdsr-deficient animals, supporting the idea of normal maturation of surfactant-producing type II alveolar epithelial cells and lung function. Other defects must therefore be responsible for the death of Ptdsr-mutant mice. The frequently observed subcutaneous edema of various extents in Ptdsr-deficient homozygotes gave us a hint that Ptdsr-deficiency and lethality might be associated with cardiovascular problems. Indeed, very recently we have obtained strong evidence that Ptdsr-knockout mice die as a result of defects in heart development that are associated with specific cardiopulmonary malformations; (J.E. Schneider, J.B., S.D. Bamfort, A.D.G., C. Broadbent, K. Clarke, S. Neubauer, A.L. and S. Battacharya, unpublished observations).\nIn addition, we demonstrate that eye development requires a functional Ptdsr gene. Ptdsr-deficient embryos can be roughly divided into two categories. The first, severely affected group develops anophthalmia that correlates with formation of ectopic retinal-pigmented epithelium and induction of proliferation of underlying mesenchyme in the nasal cavity. This phenotype represents a completely novel lesion that to our knowledge has not been described before in any other mouse mutant. The second group shows normal external eye structures, although in this case retinal development is temporally delayed during mid-gestation, with persistent, abnormal morphogenesis of the inner granular retinal layer at later stages of embryogenesis. A possible explanation for these two phenotypes can be found in the expression pattern of the Ptdsr gene. Initially, Ptdsr is expressed throughout the whole developing nervous system, with exceptionally high levels in the anterior part of the forebrain. Later expression becomes more restricted to the developing retina and lens. Thus, Ptdsr might play an important role in early events of ocular morphogenesis, such as establishment and bisection of eye fields and formation of optic cups. These early eye-formation steps are closely interconnected with development of the forebrain [37,38] and the nose [39-41].\nInterestingly, we occasionally observed serious malformations of forebrain and nasal structures in Ptdsr-knockout embryos that were associated with bilateral anophthalmia (see for example the mutant embryo in Figure 1g). This suggests that Ptdsr is involved in the regulation of differentiation processes within forebrain regions, and that ablation of Ptdsr function might secondarily affect early eye formation. Li et al. [31] found smaller lenses in Ptdsr-knockout mice and described the formation of retinal protrusions, although anophthalmia and specific differentiation defects of retinal cell layers were not reported in their study. Li et al. proposed [31] that the eye phenotype they observed could be explained by failed removal of apoptotic cells during eye development, but we think that the observed defects are unrelated to a failure of apoptotic cell clearance. A recent comprehensive kinetic analysis of apoptosis induction during mouse retinal development described four major peaks of apoptotic cell death [42]. This study demonstrated that there is an initial phase of cell death during the invagination of the optic cup (E10.5), followed by subsequent waves of apoptosis induction immediately before and after birth (E18.5 to postnatal day P2), and from postnatal days P9 to P10 and P14 to P16 [42]. Thus, besides the formation of the inner and outer layers of the optic cup in early eye development, other major phases of retinal cell apoptosis take place only postnatally and correspond to important periods in the establishment of neuronal connections. Furthermore, cell death during normal retinal development occurs in retinal layers distinct from the inner granular layer where we observed the most pronounced differentiation defects in the Ptdsr -/- mutants described here. Other studies that connect the postnatal elimination of apoptotic photoreceptor cells to Ptdsr-mediated macrophage engulfment [43] should be interpreted with extreme caution as these studies were based on the monoclonal anti-Ptdsr antibody mAb 217G8E9 [26,43] (see below).\nConsistent with the results of Li et al. [31], we found particular brain malformations in our Ptdsr -/- mice. Exencephaly and hyperplastic brain phenotypes were observed at a low penetrance in Ptdsr-mutant mice (less then 4.5% of homozygotes), but these do not resemble to any extent the brain-overgrowth phenotypes of caspase- or Apaf1-knockout mice ([44], and references therein) in that we failed to identify any differences in the number or distribution of apoptotic cells or pyknotic cell clusters in the neuroepithelium of Ptdsr -/- and Ptdsr+/+ mice. Thus, reduced cell death or diminished clearance of apoptotic neural progenitor cells is unlikely to be the cause of the brain hyperplasia.\nIn summary, our studies demonstrate that Ptdsr is required for normal tissue differentiation, especially during the mid-gestation period when we observed the most severe differentiation delays in several organs of Ptdsr-knockout mice. The multiple defects in tissue differentiation cannot be explained by failure of apoptotic cell clearance, as this process is normal in our Ptdsr-knockout line. This result therefore indicates that Ptdsr has a novel, hitherto unexpected, role in promoting tissue maturation and terminal differentiation. Additional studies with conditionally targeted Ptdsr-deficient mice are required to investigate the role of spatial and temporal Ptdsr expression and function during tissue differentiation."}

{"project":"2_test","denotations":[{"id":"15345036-14645847-55938512","span":{"begin":464,"end":466},"obj":"14645847"},{"id":"15345036-14715629-55938513","span":{"begin":467,"end":469},"obj":"14715629"},{"id":"15345036-14645847-55938514","span":{"begin":529,"end":531},"obj":"14645847"},{"id":"15345036-14715629-55938515","span":{"begin":572,"end":574},"obj":"14715629"},{"id":"15345036-14645847-55938516","span":{"begin":869,"end":871},"obj":"14645847"},{"id":"15345036-14715629-55938517","span":{"begin":894,"end":896},"obj":"14715629"},{"id":"15345036-14645847-55938518","span":{"begin":2341,"end":2343},"obj":"14645847"},{"id":"15345036-14715629-55938519","span":{"begin":2366,"end":2368},"obj":"14715629"},{"id":"15345036-14645847-55938520","span":{"begin":3286,"end":3288},"obj":"14645847"},{"id":"15345036-12530959-55938521","span":{"begin":3986,"end":3988},"obj":"12530959"},{"id":"15345036-12559759-55938522","span":{"begin":3989,"end":3991},"obj":"12559759"},{"id":"15345036-12530959-55938523","span":{"begin":4219,"end":4221},"obj":"12530959"},{"id":"15345036-12372298-55938524","span":{"begin":4222,"end":4224},"obj":"12372298"},{"id":"15345036-14645847-55938525","span":{"begin":4481,"end":4483},"obj":"14645847"},{"id":"15345036-11687490-55938526","span":{"begin":6606,"end":6608},"obj":"11687490"},{"id":"15345036-14634635-55938527","span":{"begin":6609,"end":6611},"obj":"14634635"},{"id":"15345036-12569128-55938528","span":{"begin":6627,"end":6629},"obj":"12569128"},{"id":"15345036-7789273-55938528","span":{"begin":6627,"end":6629},"obj":"7789273"},{"id":"15345036-11105055-55938528","span":{"begin":6627,"end":6629},"obj":"11105055"},{"id":"15345036-14645847-55938529","span":{"begin":7059,"end":7061},"obj":"14645847"},{"id":"15345036-14645847-55938530","span":{"begin":7295,"end":7297},"obj":"14645847"},{"id":"15345036-14517994-55938531","span":{"begin":7659,"end":7661},"obj":"14517994"},{"id":"15345036-14517994-55938532","span":{"begin":7949,"end":7951},"obj":"14517994"},{"id":"15345036-12759244-55938533","span":{"begin":8562,"end":8564},"obj":"12759244"},{"id":"15345036-10811223-55938534","span":{"begin":8688,"end":8690},"obj":"10811223"},{"id":"15345036-12759244-55938535","span":{"begin":8691,"end":8693},"obj":"12759244"},{"id":"15345036-14645847-55938536","span":{"begin":8750,"end":8752},"obj":"14645847"},{"id":"15345036-10578172-55938537","span":{"begin":9061,"end":9063},"obj":"10578172"}],"text":"Ptdsr is required for the differentiation of multiple organ systems during development\nIn this study, we have generated a null mutation in the phosphatidylserine receptor (Ptdsr) gene in C57BL/6J mice. We show that ablation of Ptdsr results in profound differentiation defects in multiple organs and tissues during embryogenesis, although with variable penetrance. While this work was in progress, two other groups reported the generation of Ptdsr-deficient mice [31,32]. In all three knockout mouse lines, the first two exons ([31] and this study) or exons one to three [32] were deleted by replacement with a neomycin-selection cassette. The Ptdsr-knockout mouse lines differ in the genetic background in which the mutation was generated and maintained, however. In our case, the Ptdsr-null allele was generated in an isogenic C57BL/6J background, whereas Li et al. [31] and Kunisaki et al. [32] investigated the phenotype of their Ptdsr-knockout mice in a mixed 129 × C57BL/6 background. The ablation of Ptdsr function results in perinatal lethality in all cases, but there are interesting differences in severity or expressivities of phenotypes among the different Ptdsr-deficient mouse lines. This might be due either to differences in genetic background or because the phenotypes that have been investigated in this study have not been analyzed in such detail before.\nIn the Ptdsr-knockout mouse line reported here, growth retardation started from E12.5 onwards and was associated with delayed differentiation in several organs in which Ptdsr is expressed either during embryogenesis or later in adulthood. At E16.5 almost no branching morphogenesis of the lung epithelium was observed in Ptdsr -/- lungs. Similarly, epithelial structures were only partially developed in mutant kidneys, without terminal differentiation of Bowman's capsule and with a severe reduction in the number of differentiated collecting tubules. Likewise, the differentiation of the intestine was also severely delayed at this developmental stage. When compared with wild-type controls, intestinal tissues of Ptdsr knockout mice appeared unstructured, with an absence of enteric ganglia and of differentiated smooth muscle tissue. Interestingly, defects in kidney and intestine differentiation were not described in the Ptdsr-knockouts generated by Li et al. [31] and Kunisaki et al. [32]. Surprisingly, when we examined Ptdsr-/- embryos shortly before birth (E18.5) or neonatally, we found only mild differentiation delays in organs that appeared severely affected at mid-gestation. This 'recovery' was most visible in Ptdsr -/- lungs: at P0 we found expanded lungs in the knockout mice that showed normal branching patterns, with differentiated alveoli and bronchioles.\nWe investigated the occurrence of programmed cell death during lung development in wild-type and Ptdsr-knockout mice throughout embryogenesis (E16.5 to P0). Comparative immunohistochemistry for aCasp3 revealed that apoptosis is a rare event during lung morphogenesis. Furthermore, we failed to detect any differences in the number of apoptotic cells in Ptdsr-knockout and wild-type animals in the rare cases where we could detect apoptotic cells within lung tissues. These findings are contrary to the results reported by Li et al. [31], who suggested that impaired clearance of apoptotic mesenchymal and epithelial cells causes a failure in lung morphogenesis in Ptdsr-deficient mice. In contrast, our findings are in line with the current view on lung development during embryogenesis. Accordingly, formation of the epithelial lung via branching morphogenesis can be subdivided into a series of sequential steps that involve: first, formation of the organ anlage in the form of a placode; second, primary bud formation by placode invagination; third, branch initiation and branch outgrowth; fourth, further reiteration of the branching process; and fifth, terminal differentiation of organ-specific proximal and distal structures [34,35]. In contrast to other invagination processes during embryogenesis, such as mammary gland formation, the lumen of the lungs is expanded by successive branching events, branch outgrowth and elongation, rather than by apoptosis [34,36]. Finally, because the lungs of Ptdsr -/-neonates were almost fully expanded and appeared normal in structure in comparison to wild-type littermates, it is highly unlikely that Ptdsr mutants die of respiratory lung failure. In addition, Li and colleagues [31] demonstrated that surfactant expression is normal in Ptdsr-deficient animals, supporting the idea of normal maturation of surfactant-producing type II alveolar epithelial cells and lung function. Other defects must therefore be responsible for the death of Ptdsr-mutant mice. The frequently observed subcutaneous edema of various extents in Ptdsr-deficient homozygotes gave us a hint that Ptdsr-deficiency and lethality might be associated with cardiovascular problems. Indeed, very recently we have obtained strong evidence that Ptdsr-knockout mice die as a result of defects in heart development that are associated with specific cardiopulmonary malformations; (J.E. Schneider, J.B., S.D. Bamfort, A.D.G., C. Broadbent, K. Clarke, S. Neubauer, A.L. and S. Battacharya, unpublished observations).\nIn addition, we demonstrate that eye development requires a functional Ptdsr gene. Ptdsr-deficient embryos can be roughly divided into two categories. The first, severely affected group develops anophthalmia that correlates with formation of ectopic retinal-pigmented epithelium and induction of proliferation of underlying mesenchyme in the nasal cavity. This phenotype represents a completely novel lesion that to our knowledge has not been described before in any other mouse mutant. The second group shows normal external eye structures, although in this case retinal development is temporally delayed during mid-gestation, with persistent, abnormal morphogenesis of the inner granular retinal layer at later stages of embryogenesis. A possible explanation for these two phenotypes can be found in the expression pattern of the Ptdsr gene. Initially, Ptdsr is expressed throughout the whole developing nervous system, with exceptionally high levels in the anterior part of the forebrain. Later expression becomes more restricted to the developing retina and lens. Thus, Ptdsr might play an important role in early events of ocular morphogenesis, such as establishment and bisection of eye fields and formation of optic cups. These early eye-formation steps are closely interconnected with development of the forebrain [37,38] and the nose [39-41].\nInterestingly, we occasionally observed serious malformations of forebrain and nasal structures in Ptdsr-knockout embryos that were associated with bilateral anophthalmia (see for example the mutant embryo in Figure 1g). This suggests that Ptdsr is involved in the regulation of differentiation processes within forebrain regions, and that ablation of Ptdsr function might secondarily affect early eye formation. Li et al. [31] found smaller lenses in Ptdsr-knockout mice and described the formation of retinal protrusions, although anophthalmia and specific differentiation defects of retinal cell layers were not reported in their study. Li et al. proposed [31] that the eye phenotype they observed could be explained by failed removal of apoptotic cells during eye development, but we think that the observed defects are unrelated to a failure of apoptotic cell clearance. A recent comprehensive kinetic analysis of apoptosis induction during mouse retinal development described four major peaks of apoptotic cell death [42]. This study demonstrated that there is an initial phase of cell death during the invagination of the optic cup (E10.5), followed by subsequent waves of apoptosis induction immediately before and after birth (E18.5 to postnatal day P2), and from postnatal days P9 to P10 and P14 to P16 [42]. Thus, besides the formation of the inner and outer layers of the optic cup in early eye development, other major phases of retinal cell apoptosis take place only postnatally and correspond to important periods in the establishment of neuronal connections. Furthermore, cell death during normal retinal development occurs in retinal layers distinct from the inner granular layer where we observed the most pronounced differentiation defects in the Ptdsr -/- mutants described here. Other studies that connect the postnatal elimination of apoptotic photoreceptor cells to Ptdsr-mediated macrophage engulfment [43] should be interpreted with extreme caution as these studies were based on the monoclonal anti-Ptdsr antibody mAb 217G8E9 [26,43] (see below).\nConsistent with the results of Li et al. [31], we found particular brain malformations in our Ptdsr -/- mice. Exencephaly and hyperplastic brain phenotypes were observed at a low penetrance in Ptdsr-mutant mice (less then 4.5% of homozygotes), but these do not resemble to any extent the brain-overgrowth phenotypes of caspase- or Apaf1-knockout mice ([44], and references therein) in that we failed to identify any differences in the number or distribution of apoptotic cells or pyknotic cell clusters in the neuroepithelium of Ptdsr -/- and Ptdsr+/+ mice. Thus, reduced cell death or diminished clearance of apoptotic neural progenitor cells is unlikely to be the cause of the brain hyperplasia.\nIn summary, our studies demonstrate that Ptdsr is required for normal tissue differentiation, especially during the mid-gestation period when we observed the most severe differentiation delays in several organs of Ptdsr-knockout mice. The multiple defects in tissue differentiation cannot be explained by failure of apoptotic cell clearance, as this process is normal in our Ptdsr-knockout line. This result therefore indicates that Ptdsr has a novel, hitherto unexpected, role in promoting tissue maturation and terminal differentiation. Additional studies with conditionally targeted Ptdsr-deficient mice are required to investigate the role of spatial and temporal Ptdsr expression and function during tissue differentiation."}