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of the little lung Mutation in Fog2\nWe screened third-generation progeny of ENU-mutagenized mice at embryonic day 18.5 (E18.5) for abnormal developmental phenotypes [14]. One line of mice was found to have multiple embryos in independent litters that displayed pulmonary hypoplasia and a thin diaphragm. The mutation, which we called little lung (lil), was mapped to Chromosome 15 by utilizing a strategy of interval haplotype analysis (data not shown) [15]. For high-resolution mapping, F2 progeny from two crosses were analyzed. In 450 progeny of an intercross of F1 (A/J × FVB/N) lil/+ mice, the interval containing the mutation was defined by 19 recombinants between D15Mit220 and D15Mit154. Because of the lack of informative markers within this interval, an additional 39 F2 progeny from an A/J × C57BL/6J cross were tested. The identification of two recombinants established D15Mit85 as the proximal and D15Mit5 as the distal flanking markers.\nThe lil phenotype was identified at E18.5 to have bilateral pulmonary hypoplasia and an abnormal diaphragm. Pulmonary hypoplasia was apparent in all mutant mice that survived to birth. In a comparison between wild-type and mutant mice found dead on day one of life, body weights were not different; however, the lung weights were significantly lower in the mutant mice. The average mutant lung weight was 9.6 ± 2.5 mg while the average wild-type lung weight was 26.4 ± 4.6 mg (p \u003c 0.001). All lungs from mutant mice were lacking an accessory lobe on the right side and had underdevelopment of the anterior right middle lobe (Figure 1A). Diaphragms from mutant lil mice were intact, but muscularization was absent in the dorsal regions. Myotubules were present in a limited and abnormal distribution. More specifically, myotubules normally radiate in a mediolateral fashion to meet the lateral body walls, with a normal paucity of muscle fibers in the central tendonous region. In the mutant diaphragm, myotubules radiated in a dorsal–ventral orientation, and muscle tissue did not meet the entire surface of the body walls (Figure 1B).\nFigure 1 Abnormal Pulmonary and Diaphragmatic Development in the lil Mouse\n(A) The mutant hypoplastic lung (right) lacks the development of the accessory lobe and the anterior portion of the right middle lobe (marked with arrows on the control sample on the left).\n(B) Whole diaphragms show a lack of normal muscularization in the posterolateral regions and the peripheral regions of the mutant diaphragm (control on left and lil diaphragm on the right). The number of lil mutant mice that survived to birth was less than 5% of total progeny, rather than the 25% expected for a recessive mutation. We evaluated litters at different embryonic time points to determine whether the reduced number was due to intra-uterine demise. Litters were collected at E12.5, 13.5, 15.5, 17.5, and 18.5, and embryos were genotyped and evaluated for evidence of intra-uterine demise, including growth retardation, pallor, and tissue friability. lil embryos had a progressively higher rate of demise between E13.5 and E15.5. At E12.5, 20 out of 87 (23%) were homozygous for the mutation, and all of these appeared viable. At E13.5, 13 of 49 (27%) were mutant and two had died. At E15.5, 22 out of 91 (24%) were mutant and the majority of mutant embryos (17 out of the 22) had died. By E18.5, nine of 29 embryos (31%) were homozygous for the mutation, of which only one embryo was viable. Diaphragmatic muscularization was abnormal in all mutant mice examined (n \u003e 25). Pulmonary hypoplasia was observed in 100% of mutants evaluated for that phenotype between E11.5 and birth (n \u003e 50).\nExamination of cardiac morphology showed that hearts from E15.5 lil mutant mice had a variety of developmental defects, including enlarged and abnormally developed endocardial cushions, a double-outlet right ventricle, and a complete atrioventricular canal. The myocardium was also poorly developed, with thinning of the outer compact layer and decreased vascularity. The cohort of mutant mice that survived to birth also had cardiac malformations including atrioventricular-canal-type ventricular septal defects, ostium primum atrial septal defects, and enlarged atria (data not shown). All mutants specifically evaluated for a cardiac phenotype (n = 10) had abnormal cardiac development.\nExamination of the 3-Mb region between D15Mit85 and D15Mit5 in DNA sequence databases revealed three predicted genes and four known genes, including Fog2. Targeted mutations of Fog2 have cardiac defects strikingly similar to those we identified in lil mutant mice, including atrioventricular canal defects, thinned myocardium, and absent coronary vasculature [16]. RT-PCR amplification of the proximal portion of Fog2 revealed longer transcripts in the lil mutant than in the wild-type embryos (Figure 2A). Sequencing of the mutant transcript revealed a point mutation (from thymine to cytosine) 2 bp after position 301, which is in the splice donor site at the end of the third exon. This mutation causes a splicing defect that results in the insertion of 85 bp of intronic sequence into the mutant transcript, and introduces a stop codon that generates a severely truncated protein product (Figure 2B). Heterozygous lil mutant mice were crossed with a Fog2 +/− (null allele) mutant generated by gene targeting [16]. Doubly heterozygous mice had an embryonic lethal phenotype; this failure to complement proves that lil is a mutation in Fog2. The variable phenotype of lil mice (relative to that found for the Fog2 null mutant) is likely due to the generation of a low level of normal transcript despite the presence of the splice site mutation.\nFigure 2 The ENU-Induced lil Mutation in Fog2 is a Splice Site Mutation\n(A) RT-PCR revealed a lengthened transcript in mice with the lil phenotype: the first band is a lil mouse, and the second band is a control mouse.\n(B) Sequencing Fog2 revealed a splice site mutation that causes the insertion of 85 bp of intronic sequence in the mutant mouse. This results in a premature stop codon prior to zinc finger transcription.\n\nLung and Diaphragm Development in the Fog2 Mutant Mouse\nExperiments were conducted to evaluate the role of Fog2 in pulmonary and diaphragmatic development. The pulmonary phenotype is characterized by diffuse hypoplasia and specific loss of the accessory lobe and a portion of the right middle lobe.\nIt is well established that abnormalities in either diaphragmatic development or fetal breathing can result in a secondary pulmonary hypoplasia, although loss of normal structure has never been documented in this context [17,18]. Fog2 is expressed diffusely in the pulmonary mesenchyme during the period of branching morphogenesis, while later expression is restricted to the smooth muscles of airways and pulmonary vessels (Figure 3). This, and the observation that lungs appeared small on transverse sections evaluated prior to diaphragmatic muscularization or function, suggests that the pulmonary hypoplasia occurs independently of the diaphragmatic defect. To test this hypothesis, lungs were dissected from Fog2 −/− mice and littermate controls before the onset of fetal diaphragmatic motion. Fog2 −/− mice were used for this experiment, as we wanted to avoid potential phenotypic variance from the lil hypomorphic mutation. Lungs dissected at E12 from Fog2 −/− embryos were smaller in size and lacked the development of an accessory lobe. In 11 viable Fog2− /− lung culture explants, there was never development of an accessory lobe, and the weights of mutant lungs cultured for 5 d were significantly lower than those of littermate controls (Figure 4). These data demonstrate that the pulmonary hypoplasia in Fog2 mutant mice is a primary defect.\nFigure 3 Fog2 Is Expressed in the Developing Lung and Diaphragm\nFog2 is expressed in the diffuse pulmonary mesenchyme at E13.5 (A) (arrow shows mesenchyme) and is restricted to the bronchial and vascular smooth muscle (sm) at E16.5 (B). Fog2 is expressed diffusely in the developing diaphragm (Dia) both prior to (E11.5) (C) and after muscularization (E13.5) (D).\nFigure 4 Fog2 Is Necessary for Primary Lung Development\nFog2 null lungs removed prior to diaphragmatic muscularization and grown in vitro show no accessory lobe development. Accessory lobe is labeled with black arrow in control littermate lungs. Branching in the unaffected lobes appeared to be delayed by 6–12 h, but all mutants developed an intricate branching pattern in the unaffected lobes after culture for 5 d.\nBecause the Fog2 phenotype is striking for specific lobar loss, the spatial pattern of Fog2 expression was evaluated in normal embryos during the period of early lobar establishment to determine whether Fog2 expression is specifically different at these lobar buds. Expression was evaluated in mice carrying a lacZ gene incorporated into the Fog2 locus (S. Tevosian, unpublished data). In nine mice examined at E11.5, all lungs showed a specific enhancement of Fog2 expression in the mesenchyme surrounding the accessory bud and the right middle lobe bud, which are the lobes that do not develop normally in Fog2 mutant mice (Figure 5). By E12.5, expression was diffuse in the pulmonary mesenchyme, as was seen previously with in situ hybridization on tissue sections.\nFigure 5 Fog2 Expression in Embryonic Non-Mutant Lungs\nIn embryonic non-mutant lungs, Fog2 is most highly expressed at the tips of the accessory (single arrows) and right middle lobes (double arrows) at E11.25 (A) and E11.75 (B), while expression is diffuse by E12.75 (C). Diaphragms from Fog2 lil mice show an intact membrane with a defect in muscular patterning (see Figure 1B). The membranous portion of the diaphragm is populated by a migratory population of muscle precursor cells, much like the limbs [19,20]. Mice with defects in genes known to be important for the control of this process have intact but amuscular diaphragms [17,21,22]. Hepatocyte growth factor/Scatter factor (HGF) is one potential candidate responsible for the guidance of muscle precursors to the membranous diaphragm. It has been shown that HGF is expressed along this anatomic pathway [23], and mice with absence of the HGF receptor c-Met fail to form muscularized pleuroperitoneal folds (PPFs), and thus have amuscular diaphragms [24,25]. Fog2 is expressed diffusely in the early amuscular diaphragm at E11.5 as well as in the later muscularized diaphragm (see Figure 3C and 3D). Pax3 and MyoD, transcription factors required for appropriate migration and determination of myogenic precursors, were detected in the PPFs of Fog2 lil mice (data not shown). However, in situ expression analysis demonstrated that the expression of HGF in the region where this structure meets the membranous diaphragm was markedly reduced in Fog2 mutant mice (Figure 6). We hypothesize that Fog2 is required (either directly or indirectly) for the induction of HGF in the developing diaphragm, and dysregulation of HGF patterning along the path of muscle precursor cell migration between the PPF and the diaphragm accounts for the abnormal phenotype in these mice.\nFigure 6 HGF Patterning Is Abnormal in Fog2 Null Mice\nIn situ hybridization of HGF in E12.5 wild-type (A) and Fog2 −/− (B) embryos demonstrates decreased expression in the region where the PPF meets the membranous diaphragm. Li, liver; Lu, lung.\n\nFOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nFOG2 sequence analysis was performed on autopsy tissue from 30 of 32 deceased children with an anatomic diagnosis of diaphragmatic defect evaluated at the Children's Hospital in Boston, Massachusetts, between 1993 and 2003. Autopsy reports were reviewed to determine the specific diagnoses. Of these 30 cases, 17 (57%) had Bochdalek CDH, two (7%) had diaphragmatic agenesis, seven (23%) had diaphragmatic eventration/muscularization defects (without Bochdalek CDH), and four (13%) had Bochdalek hernia of one hemidiaphragm and eventration of the other. Pulmonary hypoplasia was assessed using lung/body weight ratio and radial alveolar counts [26]. The material available for review included written reports and histologic slides in all cases and gross kodachromes in a subset of cases.\nOne child carried a highly significant FOG2 sequence change. The patient was a full-term 3,500-g baby girl who developed severe respiratory failure at birth and died after 5 h of resuscitation. Antemortem radiographs showed opacified lung fields and possible bowel in the chest. The patient's clinical diagnosis was CDH.\nReview of autopsy material revealed severe bilateral pulmonary hypoplasia (combined lung weight, 11.1 g; expected for body length/weight, 46.8 ± 26.2 g; [27]), most markedly involving the left lung. The lung/body weight ratio was 0.0037 (expected \u003e 0.010) [28]. There were a reduced number of bronchial generations, and the radial alveolar count was 2–3 (expected = 5) [29]. There were incomplete lung fissures bilaterally. A deep posterior diaphragmatic eventration was present on the left side. Additionally, two muscularized ligamentous bands resembling diaphragmatic remnants encircled the left lobe of the liver, creating an abnormal fissured liver contour. Away from the eventration, the diaphragm appeared well muscularized, measuring 0.3 cm in thickness. A complete autopsy revealed no other malformations; the heart was determined to be grossly normal and was donated for valve harvest.\nSequence analysis revealed a cytosine to thymine heterozygous change in exon 4 that changes the 112th amino acid from arginine to a stop codon. This mutation produces a severely truncated peptide that does not contain zinc finger domains (Figure 7). This base change was not present in the analysis of DNA from 400 normal adults. To assess the likelihood that the mutation was causal for the developmental phenotype, we examined both parents. Paternity was confirmed, and sequence analysis revealed that the neither parent carried this mutation, proving that the patient had a de novo mutation in FOG2 (Figure 7).\nFigure 7 FOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nSequencing revealed a de novo heterozygote nonsense mutation in a patient who died at birth with severe pulmonary hypoplasia and a posterior deep diaphragmatic eventration. She was clinically diagnosed with CDH. This nonsense mutation occurs prior to the functional zinc finger domains."}

{"project":"2_test","denotations":[{"id":"16103912-11818962-85559735","span":{"begin":190,"end":192},"obj":"11818962"},{"id":"16103912-9457677-85559736","span":{"begin":478,"end":480},"obj":"9457677"},{"id":"16103912-10892744-85559737","span":{"begin":4729,"end":4731},"obj":"10892744"},{"id":"16103912-10892744-85559738","span":{"begin":5382,"end":5384},"obj":"10892744"},{"id":"16103912-10696067-85559739","span":{"begin":6662,"end":6664},"obj":"10696067"},{"id":"16103912-9355800-85559740","span":{"begin":6665,"end":6667},"obj":"9355800"},{"id":"16103912-11063939-85559741","span":{"begin":9857,"end":9859},"obj":"11063939"},{"id":"16103912-10066685-85559742","span":{"begin":9860,"end":9862},"obj":"10066685"},{"id":"16103912-10696067-85559743","span":{"begin":9984,"end":9986},"obj":"10696067"},{"id":"16103912-12388344-85559744","span":{"begin":9987,"end":9989},"obj":"12388344"},{"id":"16103912-10226008-85559745","span":{"begin":9990,"end":9992},"obj":"10226008"},{"id":"16103912-10079225-85559746","span":{"begin":10216,"end":10218},"obj":"10079225"},{"id":"16103912-7651534-85559747","span":{"begin":10362,"end":10364},"obj":"7651534"},{"id":"16103912-8681797-85559748","span":{"begin":10365,"end":10367},"obj":"8681797"},{"id":"16103912-13726619-85559749","span":{"begin":12133,"end":12135},"obj":"13726619"},{"id":"16103912-7065526-85559750","span":{"begin":12854,"end":12856},"obj":"7065526"},{"id":"16103912-7179186-85559751","span":{"begin":12967,"end":12969},"obj":"7179186"},{"id":"T20943","span":{"begin":190,"end":192},"obj":"11818962"},{"id":"T62259","span":{"begin":478,"end":480},"obj":"9457677"},{"id":"T65342","span":{"begin":4729,"end":4731},"obj":"10892744"},{"id":"T5817","span":{"begin":5382,"end":5384},"obj":"10892744"},{"id":"T66232","span":{"begin":6662,"end":6664},"obj":"10696067"},{"id":"T74273","span":{"begin":6665,"end":6667},"obj":"9355800"},{"id":"T90741","span":{"begin":9857,"end":9859},"obj":"11063939"},{"id":"T7030","span":{"begin":9860,"end":9862},"obj":"10066685"},{"id":"T63606","span":{"begin":9984,"end":9986},"obj":"10696067"},{"id":"T80598","span":{"begin":9987,"end":9989},"obj":"12388344"},{"id":"T49937","span":{"begin":9990,"end":9992},"obj":"10226008"},{"id":"T83298","span":{"begin":10216,"end":10218},"obj":"10079225"},{"id":"T51026","span":{"begin":10362,"end":10364},"obj":"7651534"},{"id":"T15263","span":{"begin":10365,"end":10367},"obj":"8681797"},{"id":"T38411","span":{"begin":12133,"end":12135},"obj":"13726619"},{"id":"T80890","span":{"begin":12854,"end":12856},"obj":"7065526"},{"id":"T67813","span":{"begin":12967,"end":12969},"obj":"7179186"}],"text":"Results\n\nIdentification of the little lung Mutation in Fog2\nWe screened third-generation progeny of ENU-mutagenized mice at embryonic day 18.5 (E18.5) for abnormal developmental phenotypes [14]. One line of mice was found to have multiple embryos in independent litters that displayed pulmonary hypoplasia and a thin diaphragm. The mutation, which we called little lung (lil), was mapped to Chromosome 15 by utilizing a strategy of interval haplotype analysis (data not shown) [15]. For high-resolution mapping, F2 progeny from two crosses were analyzed. In 450 progeny of an intercross of F1 (A/J × FVB/N) lil/+ mice, the interval containing the mutation was defined by 19 recombinants between D15Mit220 and D15Mit154. Because of the lack of informative markers within this interval, an additional 39 F2 progeny from an A/J × C57BL/6J cross were tested. The identification of two recombinants established D15Mit85 as the proximal and D15Mit5 as the distal flanking markers.\nThe lil phenotype was identified at E18.5 to have bilateral pulmonary hypoplasia and an abnormal diaphragm. Pulmonary hypoplasia was apparent in all mutant mice that survived to birth. In a comparison between wild-type and mutant mice found dead on day one of life, body weights were not different; however, the lung weights were significantly lower in the mutant mice. The average mutant lung weight was 9.6 ± 2.5 mg while the average wild-type lung weight was 26.4 ± 4.6 mg (p \u003c 0.001). All lungs from mutant mice were lacking an accessory lobe on the right side and had underdevelopment of the anterior right middle lobe (Figure 1A). Diaphragms from mutant lil mice were intact, but muscularization was absent in the dorsal regions. Myotubules were present in a limited and abnormal distribution. More specifically, myotubules normally radiate in a mediolateral fashion to meet the lateral body walls, with a normal paucity of muscle fibers in the central tendonous region. In the mutant diaphragm, myotubules radiated in a dorsal–ventral orientation, and muscle tissue did not meet the entire surface of the body walls (Figure 1B).\nFigure 1 Abnormal Pulmonary and Diaphragmatic Development in the lil Mouse\n(A) The mutant hypoplastic lung (right) lacks the development of the accessory lobe and the anterior portion of the right middle lobe (marked with arrows on the control sample on the left).\n(B) Whole diaphragms show a lack of normal muscularization in the posterolateral regions and the peripheral regions of the mutant diaphragm (control on left and lil diaphragm on the right). The number of lil mutant mice that survived to birth was less than 5% of total progeny, rather than the 25% expected for a recessive mutation. We evaluated litters at different embryonic time points to determine whether the reduced number was due to intra-uterine demise. Litters were collected at E12.5, 13.5, 15.5, 17.5, and 18.5, and embryos were genotyped and evaluated for evidence of intra-uterine demise, including growth retardation, pallor, and tissue friability. lil embryos had a progressively higher rate of demise between E13.5 and E15.5. At E12.5, 20 out of 87 (23%) were homozygous for the mutation, and all of these appeared viable. At E13.5, 13 of 49 (27%) were mutant and two had died. At E15.5, 22 out of 91 (24%) were mutant and the majority of mutant embryos (17 out of the 22) had died. By E18.5, nine of 29 embryos (31%) were homozygous for the mutation, of which only one embryo was viable. Diaphragmatic muscularization was abnormal in all mutant mice examined (n \u003e 25). Pulmonary hypoplasia was observed in 100% of mutants evaluated for that phenotype between E11.5 and birth (n \u003e 50).\nExamination of cardiac morphology showed that hearts from E15.5 lil mutant mice had a variety of developmental defects, including enlarged and abnormally developed endocardial cushions, a double-outlet right ventricle, and a complete atrioventricular canal. The myocardium was also poorly developed, with thinning of the outer compact layer and decreased vascularity. The cohort of mutant mice that survived to birth also had cardiac malformations including atrioventricular-canal-type ventricular septal defects, ostium primum atrial septal defects, and enlarged atria (data not shown). All mutants specifically evaluated for a cardiac phenotype (n = 10) had abnormal cardiac development.\nExamination of the 3-Mb region between D15Mit85 and D15Mit5 in DNA sequence databases revealed three predicted genes and four known genes, including Fog2. Targeted mutations of Fog2 have cardiac defects strikingly similar to those we identified in lil mutant mice, including atrioventricular canal defects, thinned myocardium, and absent coronary vasculature [16]. RT-PCR amplification of the proximal portion of Fog2 revealed longer transcripts in the lil mutant than in the wild-type embryos (Figure 2A). Sequencing of the mutant transcript revealed a point mutation (from thymine to cytosine) 2 bp after position 301, which is in the splice donor site at the end of the third exon. This mutation causes a splicing defect that results in the insertion of 85 bp of intronic sequence into the mutant transcript, and introduces a stop codon that generates a severely truncated protein product (Figure 2B). Heterozygous lil mutant mice were crossed with a Fog2 +/− (null allele) mutant generated by gene targeting [16]. Doubly heterozygous mice had an embryonic lethal phenotype; this failure to complement proves that lil is a mutation in Fog2. The variable phenotype of lil mice (relative to that found for the Fog2 null mutant) is likely due to the generation of a low level of normal transcript despite the presence of the splice site mutation.\nFigure 2 The ENU-Induced lil Mutation in Fog2 is a Splice Site Mutation\n(A) RT-PCR revealed a lengthened transcript in mice with the lil phenotype: the first band is a lil mouse, and the second band is a control mouse.\n(B) Sequencing Fog2 revealed a splice site mutation that causes the insertion of 85 bp of intronic sequence in the mutant mouse. This results in a premature stop codon prior to zinc finger transcription.\n\nLung and Diaphragm Development in the Fog2 Mutant Mouse\nExperiments were conducted to evaluate the role of Fog2 in pulmonary and diaphragmatic development. The pulmonary phenotype is characterized by diffuse hypoplasia and specific loss of the accessory lobe and a portion of the right middle lobe.\nIt is well established that abnormalities in either diaphragmatic development or fetal breathing can result in a secondary pulmonary hypoplasia, although loss of normal structure has never been documented in this context [17,18]. Fog2 is expressed diffusely in the pulmonary mesenchyme during the period of branching morphogenesis, while later expression is restricted to the smooth muscles of airways and pulmonary vessels (Figure 3). This, and the observation that lungs appeared small on transverse sections evaluated prior to diaphragmatic muscularization or function, suggests that the pulmonary hypoplasia occurs independently of the diaphragmatic defect. To test this hypothesis, lungs were dissected from Fog2 −/− mice and littermate controls before the onset of fetal diaphragmatic motion. Fog2 −/− mice were used for this experiment, as we wanted to avoid potential phenotypic variance from the lil hypomorphic mutation. Lungs dissected at E12 from Fog2 −/− embryos were smaller in size and lacked the development of an accessory lobe. In 11 viable Fog2− /− lung culture explants, there was never development of an accessory lobe, and the weights of mutant lungs cultured for 5 d were significantly lower than those of littermate controls (Figure 4). These data demonstrate that the pulmonary hypoplasia in Fog2 mutant mice is a primary defect.\nFigure 3 Fog2 Is Expressed in the Developing Lung and Diaphragm\nFog2 is expressed in the diffuse pulmonary mesenchyme at E13.5 (A) (arrow shows mesenchyme) and is restricted to the bronchial and vascular smooth muscle (sm) at E16.5 (B). Fog2 is expressed diffusely in the developing diaphragm (Dia) both prior to (E11.5) (C) and after muscularization (E13.5) (D).\nFigure 4 Fog2 Is Necessary for Primary Lung Development\nFog2 null lungs removed prior to diaphragmatic muscularization and grown in vitro show no accessory lobe development. Accessory lobe is labeled with black arrow in control littermate lungs. Branching in the unaffected lobes appeared to be delayed by 6–12 h, but all mutants developed an intricate branching pattern in the unaffected lobes after culture for 5 d.\nBecause the Fog2 phenotype is striking for specific lobar loss, the spatial pattern of Fog2 expression was evaluated in normal embryos during the period of early lobar establishment to determine whether Fog2 expression is specifically different at these lobar buds. Expression was evaluated in mice carrying a lacZ gene incorporated into the Fog2 locus (S. Tevosian, unpublished data). In nine mice examined at E11.5, all lungs showed a specific enhancement of Fog2 expression in the mesenchyme surrounding the accessory bud and the right middle lobe bud, which are the lobes that do not develop normally in Fog2 mutant mice (Figure 5). By E12.5, expression was diffuse in the pulmonary mesenchyme, as was seen previously with in situ hybridization on tissue sections.\nFigure 5 Fog2 Expression in Embryonic Non-Mutant Lungs\nIn embryonic non-mutant lungs, Fog2 is most highly expressed at the tips of the accessory (single arrows) and right middle lobes (double arrows) at E11.25 (A) and E11.75 (B), while expression is diffuse by E12.75 (C). Diaphragms from Fog2 lil mice show an intact membrane with a defect in muscular patterning (see Figure 1B). The membranous portion of the diaphragm is populated by a migratory population of muscle precursor cells, much like the limbs [19,20]. Mice with defects in genes known to be important for the control of this process have intact but amuscular diaphragms [17,21,22]. Hepatocyte growth factor/Scatter factor (HGF) is one potential candidate responsible for the guidance of muscle precursors to the membranous diaphragm. It has been shown that HGF is expressed along this anatomic pathway [23], and mice with absence of the HGF receptor c-Met fail to form muscularized pleuroperitoneal folds (PPFs), and thus have amuscular diaphragms [24,25]. Fog2 is expressed diffusely in the early amuscular diaphragm at E11.5 as well as in the later muscularized diaphragm (see Figure 3C and 3D). Pax3 and MyoD, transcription factors required for appropriate migration and determination of myogenic precursors, were detected in the PPFs of Fog2 lil mice (data not shown). However, in situ expression analysis demonstrated that the expression of HGF in the region where this structure meets the membranous diaphragm was markedly reduced in Fog2 mutant mice (Figure 6). We hypothesize that Fog2 is required (either directly or indirectly) for the induction of HGF in the developing diaphragm, and dysregulation of HGF patterning along the path of muscle precursor cell migration between the PPF and the diaphragm accounts for the abnormal phenotype in these mice.\nFigure 6 HGF Patterning Is Abnormal in Fog2 Null Mice\nIn situ hybridization of HGF in E12.5 wild-type (A) and Fog2 −/− (B) embryos demonstrates decreased expression in the region where the PPF meets the membranous diaphragm. Li, liver; Lu, lung.\n\nFOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nFOG2 sequence analysis was performed on autopsy tissue from 30 of 32 deceased children with an anatomic diagnosis of diaphragmatic defect evaluated at the Children's Hospital in Boston, Massachusetts, between 1993 and 2003. Autopsy reports were reviewed to determine the specific diagnoses. Of these 30 cases, 17 (57%) had Bochdalek CDH, two (7%) had diaphragmatic agenesis, seven (23%) had diaphragmatic eventration/muscularization defects (without Bochdalek CDH), and four (13%) had Bochdalek hernia of one hemidiaphragm and eventration of the other. Pulmonary hypoplasia was assessed using lung/body weight ratio and radial alveolar counts [26]. The material available for review included written reports and histologic slides in all cases and gross kodachromes in a subset of cases.\nOne child carried a highly significant FOG2 sequence change. The patient was a full-term 3,500-g baby girl who developed severe respiratory failure at birth and died after 5 h of resuscitation. Antemortem radiographs showed opacified lung fields and possible bowel in the chest. The patient's clinical diagnosis was CDH.\nReview of autopsy material revealed severe bilateral pulmonary hypoplasia (combined lung weight, 11.1 g; expected for body length/weight, 46.8 ± 26.2 g; [27]), most markedly involving the left lung. The lung/body weight ratio was 0.0037 (expected \u003e 0.010) [28]. There were a reduced number of bronchial generations, and the radial alveolar count was 2–3 (expected = 5) [29]. There were incomplete lung fissures bilaterally. A deep posterior diaphragmatic eventration was present on the left side. Additionally, two muscularized ligamentous bands resembling diaphragmatic remnants encircled the left lobe of the liver, creating an abnormal fissured liver contour. Away from the eventration, the diaphragm appeared well muscularized, measuring 0.3 cm in thickness. A complete autopsy revealed no other malformations; the heart was determined to be grossly normal and was donated for valve harvest.\nSequence analysis revealed a cytosine to thymine heterozygous change in exon 4 that changes the 112th amino acid from arginine to a stop codon. This mutation produces a severely truncated peptide that does not contain zinc finger domains (Figure 7). This base change was not present in the analysis of DNA from 400 normal adults. To assess the likelihood that the mutation was causal for the developmental phenotype, we examined both parents. Paternity was confirmed, and sequence analysis revealed that the neither parent carried this mutation, proving that the patient had a de novo mutation in FOG2 (Figure 7).\nFigure 7 FOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nSequencing revealed a de novo heterozygote nonsense mutation in a patient who died at birth with severe pulmonary hypoplasia and a posterior deep diaphragmatic eventration. She was clinically diagnosed with CDH. This nonsense mutation occurs prior to the functional zinc finger domains."}

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of the little lung Mutation in Fog2\nWe screened third-generation progeny of ENU-mutagenized mice at embryonic day 18.5 (E18.5) for abnormal developmental phenotypes [14]. One line of mice was found to have multiple embryos in independent litters that displayed pulmonary hypoplasia and a thin diaphragm. The mutation, which we called little lung (lil), was mapped to Chromosome 15 by utilizing a strategy of interval haplotype analysis (data not shown) [15]. For high-resolution mapping, F2 progeny from two crosses were analyzed. In 450 progeny of an intercross of F1 (A/J × FVB/N) lil/+ mice, the interval containing the mutation was defined by 19 recombinants between D15Mit220 and D15Mit154. Because of the lack of informative markers within this interval, an additional 39 F2 progeny from an A/J × C57BL/6J cross were tested. The identification of two recombinants established D15Mit85 as the proximal and D15Mit5 as the distal flanking markers.\nThe lil phenotype was identified at E18.5 to have bilateral pulmonary hypoplasia and an abnormal diaphragm. Pulmonary hypoplasia was apparent in all mutant mice that survived to birth. In a comparison between wild-type and mutant mice found dead on day one of life, body weights were not different; however, the lung weights were significantly lower in the mutant mice. The average mutant lung weight was 9.6 ± 2.5 mg while the average wild-type lung weight was 26.4 ± 4.6 mg (p \u003c 0.001). All lungs from mutant mice were lacking an accessory lobe on the right side and had underdevelopment of the anterior right middle lobe (Figure 1A). Diaphragms from mutant lil mice were intact, but muscularization was absent in the dorsal regions. Myotubules were present in a limited and abnormal distribution. More specifically, myotubules normally radiate in a mediolateral fashion to meet the lateral body walls, with a normal paucity of muscle fibers in the central tendonous region. In the mutant diaphragm, myotubules radiated in a dorsal–ventral orientation, and muscle tissue did not meet the entire surface of the body walls (Figure 1B).\nFigure 1 Abnormal Pulmonary and Diaphragmatic Development in the lil Mouse\n(A) The mutant hypoplastic lung (right) lacks the development of the accessory lobe and the anterior portion of the right middle lobe (marked with arrows on the control sample on the left).\n(B) Whole diaphragms show a lack of normal muscularization in the posterolateral regions and the peripheral regions of the mutant diaphragm (control on left and lil diaphragm on the right). The number of lil mutant mice that survived to birth was less than 5% of total progeny, rather than the 25% expected for a recessive mutation. We evaluated litters at different embryonic time points to determine whether the reduced number was due to intra-uterine demise. Litters were collected at E12.5, 13.5, 15.5, 17.5, and 18.5, and embryos were genotyped and evaluated for evidence of intra-uterine demise, including growth retardation, pallor, and tissue friability. lil embryos had a progressively higher rate of demise between E13.5 and E15.5. At E12.5, 20 out of 87 (23%) were homozygous for the mutation, and all of these appeared viable. At E13.5, 13 of 49 (27%) were mutant and two had died. At E15.5, 22 out of 91 (24%) were mutant and the majority of mutant embryos (17 out of the 22) had died. By E18.5, nine of 29 embryos (31%) were homozygous for the mutation, of which only one embryo was viable. Diaphragmatic muscularization was abnormal in all mutant mice examined (n \u003e 25). Pulmonary hypoplasia was observed in 100% of mutants evaluated for that phenotype between E11.5 and birth (n \u003e 50).\nExamination of cardiac morphology showed that hearts from E15.5 lil mutant mice had a variety of developmental defects, including enlarged and abnormally developed endocardial cushions, a double-outlet right ventricle, and a complete atrioventricular canal. The myocardium was also poorly developed, with thinning of the outer compact layer and decreased vascularity. The cohort of mutant mice that survived to birth also had cardiac malformations including atrioventricular-canal-type ventricular septal defects, ostium primum atrial septal defects, and enlarged atria (data not shown). All mutants specifically evaluated for a cardiac phenotype (n = 10) had abnormal cardiac development.\nExamination of the 3-Mb region between D15Mit85 and D15Mit5 in DNA sequence databases revealed three predicted genes and four known genes, including Fog2. Targeted mutations of Fog2 have cardiac defects strikingly similar to those we identified in lil mutant mice, including atrioventricular canal defects, thinned myocardium, and absent coronary vasculature [16]. RT-PCR amplification of the proximal portion of Fog2 revealed longer transcripts in the lil mutant than in the wild-type embryos (Figure 2A). Sequencing of the mutant transcript revealed a point mutation (from thymine to cytosine) 2 bp after position 301, which is in the splice donor site at the end of the third exon. This mutation causes a splicing defect that results in the insertion of 85 bp of intronic sequence into the mutant transcript, and introduces a stop codon that generates a severely truncated protein product (Figure 2B). Heterozygous lil mutant mice were crossed with a Fog2 +/− (null allele) mutant generated by gene targeting [16]. Doubly heterozygous mice had an embryonic lethal phenotype; this failure to complement proves that lil is a mutation in Fog2. The variable phenotype of lil mice (relative to that found for the Fog2 null mutant) is likely due to the generation of a low level of normal transcript despite the presence of the splice site mutation.\nFigure 2 The ENU-Induced lil Mutation in Fog2 is a Splice Site Mutation\n(A) RT-PCR revealed a lengthened transcript in mice with the lil phenotype: the first band is a lil mouse, and the second band is a control mouse.\n(B) Sequencing Fog2 revealed a splice site mutation that causes the insertion of 85 bp of intronic sequence in the mutant mouse. This results in a premature stop codon prior to zinc finger transcription.\n\nLung and Diaphragm Development in the Fog2 Mutant Mouse\nExperiments were conducted to evaluate the role of Fog2 in pulmonary and diaphragmatic development. The pulmonary phenotype is characterized by diffuse hypoplasia and specific loss of the accessory lobe and a portion of the right middle lobe.\nIt is well established that abnormalities in either diaphragmatic development or fetal breathing can result in a secondary pulmonary hypoplasia, although loss of normal structure has never been documented in this context [17,18]. Fog2 is expressed diffusely in the pulmonary mesenchyme during the period of branching morphogenesis, while later expression is restricted to the smooth muscles of airways and pulmonary vessels (Figure 3). This, and the observation that lungs appeared small on transverse sections evaluated prior to diaphragmatic muscularization or function, suggests that the pulmonary hypoplasia occurs independently of the diaphragmatic defect. To test this hypothesis, lungs were dissected from Fog2 −/− mice and littermate controls before the onset of fetal diaphragmatic motion. Fog2 −/− mice were used for this experiment, as we wanted to avoid potential phenotypic variance from the lil hypomorphic mutation. Lungs dissected at E12 from Fog2 −/− embryos were smaller in size and lacked the development of an accessory lobe. In 11 viable Fog2− /− lung culture explants, there was never development of an accessory lobe, and the weights of mutant lungs cultured for 5 d were significantly lower than those of littermate controls (Figure 4). These data demonstrate that the pulmonary hypoplasia in Fog2 mutant mice is a primary defect.\nFigure 3 Fog2 Is Expressed in the Developing Lung and Diaphragm\nFog2 is expressed in the diffuse pulmonary mesenchyme at E13.5 (A) (arrow shows mesenchyme) and is restricted to the bronchial and vascular smooth muscle (sm) at E16.5 (B). Fog2 is expressed diffusely in the developing diaphragm (Dia) both prior to (E11.5) (C) and after muscularization (E13.5) (D).\nFigure 4 Fog2 Is Necessary for Primary Lung Development\nFog2 null lungs removed prior to diaphragmatic muscularization and grown in vitro show no accessory lobe development. Accessory lobe is labeled with black arrow in control littermate lungs. Branching in the unaffected lobes appeared to be delayed by 6–12 h, but all mutants developed an intricate branching pattern in the unaffected lobes after culture for 5 d.\nBecause the Fog2 phenotype is striking for specific lobar loss, the spatial pattern of Fog2 expression was evaluated in normal embryos during the period of early lobar establishment to determine whether Fog2 expression is specifically different at these lobar buds. Expression was evaluated in mice carrying a lacZ gene incorporated into the Fog2 locus (S. Tevosian, unpublished data). In nine mice examined at E11.5, all lungs showed a specific enhancement of Fog2 expression in the mesenchyme surrounding the accessory bud and the right middle lobe bud, which are the lobes that do not develop normally in Fog2 mutant mice (Figure 5). By E12.5, expression was diffuse in the pulmonary mesenchyme, as was seen previously with in situ hybridization on tissue sections.\nFigure 5 Fog2 Expression in Embryonic Non-Mutant Lungs\nIn embryonic non-mutant lungs, Fog2 is most highly expressed at the tips of the accessory (single arrows) and right middle lobes (double arrows) at E11.25 (A) and E11.75 (B), while expression is diffuse by E12.75 (C). Diaphragms from Fog2 lil mice show an intact membrane with a defect in muscular patterning (see Figure 1B). The membranous portion of the diaphragm is populated by a migratory population of muscle precursor cells, much like the limbs [19,20]. Mice with defects in genes known to be important for the control of this process have intact but amuscular diaphragms [17,21,22]. Hepatocyte growth factor/Scatter factor (HGF) is one potential candidate responsible for the guidance of muscle precursors to the membranous diaphragm. It has been shown that HGF is expressed along this anatomic pathway [23], and mice with absence of the HGF receptor c-Met fail to form muscularized pleuroperitoneal folds (PPFs), and thus have amuscular diaphragms [24,25]. Fog2 is expressed diffusely in the early amuscular diaphragm at E11.5 as well as in the later muscularized diaphragm (see Figure 3C and 3D). Pax3 and MyoD, transcription factors required for appropriate migration and determination of myogenic precursors, were detected in the PPFs of Fog2 lil mice (data not shown). However, in situ expression analysis demonstrated that the expression of HGF in the region where this structure meets the membranous diaphragm was markedly reduced in Fog2 mutant mice (Figure 6). We hypothesize that Fog2 is required (either directly or indirectly) for the induction of HGF in the developing diaphragm, and dysregulation of HGF patterning along the path of muscle precursor cell migration between the PPF and the diaphragm accounts for the abnormal phenotype in these mice.\nFigure 6 HGF Patterning Is Abnormal in Fog2 Null Mice\nIn situ hybridization of HGF in E12.5 wild-type (A) and Fog2 −/− (B) embryos demonstrates decreased expression in the region where the PPF meets the membranous diaphragm. Li, liver; Lu, lung.\n\nFOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nFOG2 sequence analysis was performed on autopsy tissue from 30 of 32 deceased children with an anatomic diagnosis of diaphragmatic defect evaluated at the Children's Hospital in Boston, Massachusetts, between 1993 and 2003. Autopsy reports were reviewed to determine the specific diagnoses. Of these 30 cases, 17 (57%) had Bochdalek CDH, two (7%) had diaphragmatic agenesis, seven (23%) had diaphragmatic eventration/muscularization defects (without Bochdalek CDH), and four (13%) had Bochdalek hernia of one hemidiaphragm and eventration of the other. Pulmonary hypoplasia was assessed using lung/body weight ratio and radial alveolar counts [26]. The material available for review included written reports and histologic slides in all cases and gross kodachromes in a subset of cases.\nOne child carried a highly significant FOG2 sequence change. The patient was a full-term 3,500-g baby girl who developed severe respiratory failure at birth and died after 5 h of resuscitation. Antemortem radiographs showed opacified lung fields and possible bowel in the chest. The patient's clinical diagnosis was CDH.\nReview of autopsy material revealed severe bilateral pulmonary hypoplasia (combined lung weight, 11.1 g; expected for body length/weight, 46.8 ± 26.2 g; [27]), most markedly involving the left lung. The lung/body weight ratio was 0.0037 (expected \u003e 0.010) [28]. There were a reduced number of bronchial generations, and the radial alveolar count was 2–3 (expected = 5) [29]. There were incomplete lung fissures bilaterally. A deep posterior diaphragmatic eventration was present on the left side. Additionally, two muscularized ligamentous bands resembling diaphragmatic remnants encircled the left lobe of the liver, creating an abnormal fissured liver contour. Away from the eventration, the diaphragm appeared well muscularized, measuring 0.3 cm in thickness. A complete autopsy revealed no other malformations; the heart was determined to be grossly normal and was donated for valve harvest.\nSequence analysis revealed a cytosine to thymine heterozygous change in exon 4 that changes the 112th amino acid from arginine to a stop codon. This mutation produces a severely truncated peptide that does not contain zinc finger domains (Figure 7). This base change was not present in the analysis of DNA from 400 normal adults. To assess the likelihood that the mutation was causal for the developmental phenotype, we examined both parents. Paternity was confirmed, and sequence analysis revealed that the neither parent carried this mutation, proving that the patient had a de novo mutation in FOG2 (Figure 7).\nFigure 7 FOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nSequencing revealed a de novo heterozygote nonsense mutation in a patient who died at birth with severe pulmonary hypoplasia and a posterior deep diaphragmatic eventration. She was clinically diagnosed with CDH. This nonsense mutation occurs prior to the functional zinc finger domains."}

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of the little lung Mutation in Fog2\nWe screened third-generation progeny of ENU-mutagenized mice at embryonic day 18.5 (E18.5) for abnormal developmental phenotypes [14]. One line of mice was found to have multiple embryos in independent litters that displayed pulmonary hypoplasia and a thin diaphragm. The mutation, which we called little lung (lil), was mapped to Chromosome 15 by utilizing a strategy of interval haplotype analysis (data not shown) [15]. For high-resolution mapping, F2 progeny from two crosses were analyzed. In 450 progeny of an intercross of F1 (A/J × FVB/N) lil/+ mice, the interval containing the mutation was defined by 19 recombinants between D15Mit220 and D15Mit154. Because of the lack of informative markers within this interval, an additional 39 F2 progeny from an A/J × C57BL/6J cross were tested. The identification of two recombinants established D15Mit85 as the proximal and D15Mit5 as the distal flanking markers.\nThe lil phenotype was identified at E18.5 to have bilateral pulmonary hypoplasia and an abnormal diaphragm. Pulmonary hypoplasia was apparent in all mutant mice that survived to birth. In a comparison between wild-type and mutant mice found dead on day one of life, body weights were not different; however, the lung weights were significantly lower in the mutant mice. The average mutant lung weight was 9.6 ± 2.5 mg while the average wild-type lung weight was 26.4 ± 4.6 mg (p \u003c 0.001). All lungs from mutant mice were lacking an accessory lobe on the right side and had underdevelopment of the anterior right middle lobe (Figure 1A). Diaphragms from mutant lil mice were intact, but muscularization was absent in the dorsal regions. Myotubules were present in a limited and abnormal distribution. More specifically, myotubules normally radiate in a mediolateral fashion to meet the lateral body walls, with a normal paucity of muscle fibers in the central tendonous region. In the mutant diaphragm, myotubules radiated in a dorsal–ventral orientation, and muscle tissue did not meet the entire surface of the body walls (Figure 1B).\nFigure 1 Abnormal Pulmonary and Diaphragmatic Development in the lil Mouse\n(A) The mutant hypoplastic lung (right) lacks the development of the accessory lobe and the anterior portion of the right middle lobe (marked with arrows on the control sample on the left).\n(B) Whole diaphragms show a lack of normal muscularization in the posterolateral regions and the peripheral regions of the mutant diaphragm (control on left and lil diaphragm on the right). The number of lil mutant mice that survived to birth was less than 5% of total progeny, rather than the 25% expected for a recessive mutation. We evaluated litters at different embryonic time points to determine whether the reduced number was due to intra-uterine demise. Litters were collected at E12.5, 13.5, 15.5, 17.5, and 18.5, and embryos were genotyped and evaluated for evidence of intra-uterine demise, including growth retardation, pallor, and tissue friability. lil embryos had a progressively higher rate of demise between E13.5 and E15.5. At E12.5, 20 out of 87 (23%) were homozygous for the mutation, and all of these appeared viable. At E13.5, 13 of 49 (27%) were mutant and two had died. At E15.5, 22 out of 91 (24%) were mutant and the majority of mutant embryos (17 out of the 22) had died. By E18.5, nine of 29 embryos (31%) were homozygous for the mutation, of which only one embryo was viable. Diaphragmatic muscularization was abnormal in all mutant mice examined (n \u003e 25). Pulmonary hypoplasia was observed in 100% of mutants evaluated for that phenotype between E11.5 and birth (n \u003e 50).\nExamination of cardiac morphology showed that hearts from E15.5 lil mutant mice had a variety of developmental defects, including enlarged and abnormally developed endocardial cushions, a double-outlet right ventricle, and a complete atrioventricular canal. The myocardium was also poorly developed, with thinning of the outer compact layer and decreased vascularity. The cohort of mutant mice that survived to birth also had cardiac malformations including atrioventricular-canal-type ventricular septal defects, ostium primum atrial septal defects, and enlarged atria (data not shown). All mutants specifically evaluated for a cardiac phenotype (n = 10) had abnormal cardiac development.\nExamination of the 3-Mb region between D15Mit85 and D15Mit5 in DNA sequence databases revealed three predicted genes and four known genes, including Fog2. Targeted mutations of Fog2 have cardiac defects strikingly similar to those we identified in lil mutant mice, including atrioventricular canal defects, thinned myocardium, and absent coronary vasculature [16]. RT-PCR amplification of the proximal portion of Fog2 revealed longer transcripts in the lil mutant than in the wild-type embryos (Figure 2A). Sequencing of the mutant transcript revealed a point mutation (from thymine to cytosine) 2 bp after position 301, which is in the splice donor site at the end of the third exon. This mutation causes a splicing defect that results in the insertion of 85 bp of intronic sequence into the mutant transcript, and introduces a stop codon that generates a severely truncated protein product (Figure 2B). Heterozygous lil mutant mice were crossed with a Fog2 +/− (null allele) mutant generated by gene targeting [16]. Doubly heterozygous mice had an embryonic lethal phenotype; this failure to complement proves that lil is a mutation in Fog2. The variable phenotype of lil mice (relative to that found for the Fog2 null mutant) is likely due to the generation of a low level of normal transcript despite the presence of the splice site mutation.\nFigure 2 The ENU-Induced lil Mutation in Fog2 is a Splice Site Mutation\n(A) RT-PCR revealed a lengthened transcript in mice with the lil phenotype: the first band is a lil mouse, and the second band is a control mouse.\n(B) Sequencing Fog2 revealed a splice site mutation that causes the insertion of 85 bp of intronic sequence in the mutant mouse. This results in a premature stop codon prior to zinc finger transcription.\n\nLung and Diaphragm Development in the Fog2 Mutant Mouse\nExperiments were conducted to evaluate the role of Fog2 in pulmonary and diaphragmatic development. The pulmonary phenotype is characterized by diffuse hypoplasia and specific loss of the accessory lobe and a portion of the right middle lobe.\nIt is well established that abnormalities in either diaphragmatic development or fetal breathing can result in a secondary pulmonary hypoplasia, although loss of normal structure has never been documented in this context [17,18]. Fog2 is expressed diffusely in the pulmonary mesenchyme during the period of branching morphogenesis, while later expression is restricted to the smooth muscles of airways and pulmonary vessels (Figure 3). This, and the observation that lungs appeared small on transverse sections evaluated prior to diaphragmatic muscularization or function, suggests that the pulmonary hypoplasia occurs independently of the diaphragmatic defect. To test this hypothesis, lungs were dissected from Fog2 −/− mice and littermate controls before the onset of fetal diaphragmatic motion. Fog2 −/− mice were used for this experiment, as we wanted to avoid potential phenotypic variance from the lil hypomorphic mutation. Lungs dissected at E12 from Fog2 −/− embryos were smaller in size and lacked the development of an accessory lobe. In 11 viable Fog2− /− lung culture explants, there was never development of an accessory lobe, and the weights of mutant lungs cultured for 5 d were significantly lower than those of littermate controls (Figure 4). These data demonstrate that the pulmonary hypoplasia in Fog2 mutant mice is a primary defect.\nFigure 3 Fog2 Is Expressed in the Developing Lung and Diaphragm\nFog2 is expressed in the diffuse pulmonary mesenchyme at E13.5 (A) (arrow shows mesenchyme) and is restricted to the bronchial and vascular smooth muscle (sm) at E16.5 (B). Fog2 is expressed diffusely in the developing diaphragm (Dia) both prior to (E11.5) (C) and after muscularization (E13.5) (D).\nFigure 4 Fog2 Is Necessary for Primary Lung Development\nFog2 null lungs removed prior to diaphragmatic muscularization and grown in vitro show no accessory lobe development. Accessory lobe is labeled with black arrow in control littermate lungs. Branching in the unaffected lobes appeared to be delayed by 6–12 h, but all mutants developed an intricate branching pattern in the unaffected lobes after culture for 5 d.\nBecause the Fog2 phenotype is striking for specific lobar loss, the spatial pattern of Fog2 expression was evaluated in normal embryos during the period of early lobar establishment to determine whether Fog2 expression is specifically different at these lobar buds. Expression was evaluated in mice carrying a lacZ gene incorporated into the Fog2 locus (S. Tevosian, unpublished data). In nine mice examined at E11.5, all lungs showed a specific enhancement of Fog2 expression in the mesenchyme surrounding the accessory bud and the right middle lobe bud, which are the lobes that do not develop normally in Fog2 mutant mice (Figure 5). By E12.5, expression was diffuse in the pulmonary mesenchyme, as was seen previously with in situ hybridization on tissue sections.\nFigure 5 Fog2 Expression in Embryonic Non-Mutant Lungs\nIn embryonic non-mutant lungs, Fog2 is most highly expressed at the tips of the accessory (single arrows) and right middle lobes (double arrows) at E11.25 (A) and E11.75 (B), while expression is diffuse by E12.75 (C). Diaphragms from Fog2 lil mice show an intact membrane with a defect in muscular patterning (see Figure 1B). The membranous portion of the diaphragm is populated by a migratory population of muscle precursor cells, much like the limbs [19,20]. Mice with defects in genes known to be important for the control of this process have intact but amuscular diaphragms [17,21,22]. Hepatocyte growth factor/Scatter factor (HGF) is one potential candidate responsible for the guidance of muscle precursors to the membranous diaphragm. It has been shown that HGF is expressed along this anatomic pathway [23], and mice with absence of the HGF receptor c-Met fail to form muscularized pleuroperitoneal folds (PPFs), and thus have amuscular diaphragms [24,25]. Fog2 is expressed diffusely in the early amuscular diaphragm at E11.5 as well as in the later muscularized diaphragm (see Figure 3C and 3D). Pax3 and MyoD, transcription factors required for appropriate migration and determination of myogenic precursors, were detected in the PPFs of Fog2 lil mice (data not shown). However, in situ expression analysis demonstrated that the expression of HGF in the region where this structure meets the membranous diaphragm was markedly reduced in Fog2 mutant mice (Figure 6). We hypothesize that Fog2 is required (either directly or indirectly) for the induction of HGF in the developing diaphragm, and dysregulation of HGF patterning along the path of muscle precursor cell migration between the PPF and the diaphragm accounts for the abnormal phenotype in these mice.\nFigure 6 HGF Patterning Is Abnormal in Fog2 Null Mice\nIn situ hybridization of HGF in E12.5 wild-type (A) and Fog2 −/− (B) embryos demonstrates decreased expression in the region where the PPF meets the membranous diaphragm. Li, liver; Lu, lung.\n\nFOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nFOG2 sequence analysis was performed on autopsy tissue from 30 of 32 deceased children with an anatomic diagnosis of diaphragmatic defect evaluated at the Children's Hospital in Boston, Massachusetts, between 1993 and 2003. Autopsy reports were reviewed to determine the specific diagnoses. Of these 30 cases, 17 (57%) had Bochdalek CDH, two (7%) had diaphragmatic agenesis, seven (23%) had diaphragmatic eventration/muscularization defects (without Bochdalek CDH), and four (13%) had Bochdalek hernia of one hemidiaphragm and eventration of the other. Pulmonary hypoplasia was assessed using lung/body weight ratio and radial alveolar counts [26]. The material available for review included written reports and histologic slides in all cases and gross kodachromes in a subset of cases.\nOne child carried a highly significant FOG2 sequence change. The patient was a full-term 3,500-g baby girl who developed severe respiratory failure at birth and died after 5 h of resuscitation. Antemortem radiographs showed opacified lung fields and possible bowel in the chest. The patient's clinical diagnosis was CDH.\nReview of autopsy material revealed severe bilateral pulmonary hypoplasia (combined lung weight, 11.1 g; expected for body length/weight, 46.8 ± 26.2 g; [27]), most markedly involving the left lung. The lung/body weight ratio was 0.0037 (expected \u003e 0.010) [28]. There were a reduced number of bronchial generations, and the radial alveolar count was 2–3 (expected = 5) [29]. There were incomplete lung fissures bilaterally. A deep posterior diaphragmatic eventration was present on the left side. Additionally, two muscularized ligamentous bands resembling diaphragmatic remnants encircled the left lobe of the liver, creating an abnormal fissured liver contour. Away from the eventration, the diaphragm appeared well muscularized, measuring 0.3 cm in thickness. A complete autopsy revealed no other malformations; the heart was determined to be grossly normal and was donated for valve harvest.\nSequence analysis revealed a cytosine to thymine heterozygous change in exon 4 that changes the 112th amino acid from arginine to a stop codon. This mutation produces a severely truncated peptide that does not contain zinc finger domains (Figure 7). This base change was not present in the analysis of DNA from 400 normal adults. To assess the likelihood that the mutation was causal for the developmental phenotype, we examined both parents. Paternity was confirmed, and sequence analysis revealed that the neither parent carried this mutation, proving that the patient had a de novo mutation in FOG2 (Figure 7).\nFigure 7 FOG2 Mutation in a Patient with Diaphragm and Lung Abnormalities\nSequencing revealed a de novo heterozygote nonsense mutation in a patient who died at birth with severe pulmonary hypoplasia and a posterior deep diaphragmatic eventration. She was clinically diagnosed with CDH. This nonsense mutation occurs prior to the functional zinc finger domains."}