Global genetic analysis in mice unveils central role for cilia in congenital heart disease
A forward genetic screen in fetal mice to identify genes involved in congenital heart disease (CHD) reveals that a large proportion of genes associated with CHD are related to cilia and cilia-transduced cell signalling, with potential implications for the human disease. Cilia defects in congenital h...
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| Published in | Nature (London) Vol. 521; no. 7553; pp. 520 - 524 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
28.05.2015
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | A forward genetic screen in fetal mice to identify genes involved in congenital heart disease (CHD) reveals that a large proportion of genes associated with CHD are related to cilia and cilia-transduced cell signalling, with potential implications for the human disease.
Cilia defects in congenital heart disease
The identification of genes causing congenital heart disease (CHD) has been challenging, in part because of the difficulty of distinguishing pathogenic mutations from random sequence genetic variability. Cecilia Lo and colleagues have therefore used a large-scale mouse forward genetic screen with chemical mutagenesis to recover mutations causing congenital heart disease. They identify 218 mouse models of the condition and, using whole-exome sequencing, 91 recessive mutations in 61 genes. A larger than expected proportion of these genes was found to be related to cilia and cilia-transduced cell signalling.
Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births
1
; the incidence of CHD is up to tenfold higher in human fetuses
2
,
3
. A genetic contribution is strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk
4
. Here we report findings from a recessive forward genetic screen in fetal mice, showing that cilia and cilia-transduced cell signalling have important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole-exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia-transduced cell signalling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signalling. Surprisingly, many CHD genes encoded interacting proteins, suggesting that an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note that the pathways identified show overlap with CHD candidate genes recovered in CHD patients
5
, suggesting that they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations have been sperm archived, creating a rich public resource for human disease modelling. |
|---|---|
| AbstractList | Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births
1
, but the incidence of CHD is up to ten fold higher in human fetuses
2
,
3
. A genetic contribution is strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk
4
. Here we report findings from a recessive forward genetic screen in fetal mice, showing the cilium and cilia transduced cell signaling play important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia transduced cell signaling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signaling. Surprisingly, many CHD genes encoded interacting proteins, suggesting an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note pathways identified show overlap with CHD candidate genes recovered in CHD patients
5
, suggesting they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations are sperm archived, creating a rich public resource for human disease modeling. Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births; the incidence of CHD is up to ten-fold higher in human fetuses. A genetic contributionis strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk. Here we report findings from a recessive forward genetic screen in fetal mice, showing that cilia and cilia-transduced cell signalling have important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole-exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia-transduced cell signalling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signalling. Surprisingly, many CHD genes encoded interacting proteins, suggesting that an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note that the pathways identified show overlap with CHD candidate genes recovered in CHD patients, suggesting that they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations have been sperm archived, creating a rich public resource for human disease modelling. Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births (1); the incidence of CHD is up to tenfold higher in human fetuses (2,3). A genetic contribution is strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk4. Here we report findings from a recessive forward genetic screen in fetal mice, showing that cilia and cilia-transduced cell signalling have important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole-exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia-transduced cell signalling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signalling. Surprisingly, many CHD genes encoded interacting proteins, suggesting that an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note that the pathways identified show overlap with CHD candidate genes recovered in CHD patients5, suggesting that they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations have been sperm archived, creating a rich public resource for human disease modelling. Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births; the incidence of CHD is up to tenfold higher in human fetuses. A genetic contribution is strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk. Here we report findings from a recessive forward genetic screen in fetal mice, showing that cilia and cilia-transduced cell signalling have important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole-exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia-transduced cell signalling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signalling. Surprisingly, many CHD genes encoded interacting proteins, suggesting that an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note that the pathways identified show overlap with CHD candidate genes recovered in CHD patients, suggesting that they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations have been sperm archived, creating a rich public resource for human disease modelling. A forward genetic screen in fetal mice to identify genes involved in congenital heart disease (CHD) reveals that a large proportion of genes associated with CHD are related to cilia and cilia-transduced cell signalling, with potential implications for the human disease. Cilia defects in congenital heart disease The identification of genes causing congenital heart disease (CHD) has been challenging, in part because of the difficulty of distinguishing pathogenic mutations from random sequence genetic variability. Cecilia Lo and colleagues have therefore used a large-scale mouse forward genetic screen with chemical mutagenesis to recover mutations causing congenital heart disease. They identify 218 mouse models of the condition and, using whole-exome sequencing, 91 recessive mutations in 61 genes. A larger than expected proportion of these genes was found to be related to cilia and cilia-transduced cell signalling. Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births 1 ; the incidence of CHD is up to tenfold higher in human fetuses 2 , 3 . A genetic contribution is strongly suggested by the association of CHD with chromosome abnormalities and high recurrence risk 4 . Here we report findings from a recessive forward genetic screen in fetal mice, showing that cilia and cilia-transduced cell signalling have important roles in the pathogenesis of CHD. The cilium is an evolutionarily conserved organelle projecting from the cell surface with essential roles in diverse cellular processes. Using echocardiography, we ultrasound scanned 87,355 chemically mutagenized C57BL/6J fetal mice and recovered 218 CHD mouse models. Whole-exome sequencing identified 91 recessive CHD mutations in 61 genes. This included 34 cilia-related genes, 16 genes involved in cilia-transduced cell signalling, and 10 genes regulating vesicular trafficking, a pathway important for ciliogenesis and cell signalling. Surprisingly, many CHD genes encoded interacting proteins, suggesting that an interactome protein network may provide a larger genomic context for CHD pathogenesis. These findings provide novel insights into the potential Mendelian genetic contribution to CHD in the fetal population, a segment of the human population not well studied. We note that the pathways identified show overlap with CHD candidate genes recovered in CHD patients 5 , suggesting that they may have relevance to the more complex genetics of CHD overall. These CHD mouse models and >8,000 incidental mutations have been sperm archived, creating a rich public resource for human disease modelling. |
| Audience | Academic |
| Author | Anderton, Shane Devine, William Morgan, Judy Leatherbury, Linda Li, You Ganapathiraju, Madhavi K. Chatterjee, Bishwanath Reinholdt, Laura Lo, Cecilia W. Lemke, Kristi Lawhead, Caroline Vescovi, Anita Kim, Andrew J. Smith, Cynthia L. Tobita, Kimimasa Liu, Xiaoqin Francis, Richard Gabriel, George C. Chen, Yu Pratt, Herbert Chang, Chienfu Eppig, Janan T. Haynes, Leslie Klena, Nikolai T. Yagi, Hisato Pazour, Gregory J. San Agustin, Jovenal T. Damerla, Rama Rao Thahir, Mohamed |
| AuthorAffiliation | 5 Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 4 Intelligent Systems Program, School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA 1 Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA 2 Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA 6 The Jackson Laboratory, Bar Harbor, ME 3 Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA 7 The Heart Center, Children's National Medical Center, Washington, D.C |
| AuthorAffiliation_xml | – name: 1 Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA – name: 4 Intelligent Systems Program, School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA – name: 2 Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA – name: 5 Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA – name: 7 The Heart Center, Children's National Medical Center, Washington, D.C – name: 3 Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA – name: 6 The Jackson Laboratory, Bar Harbor, ME |
| Author_xml | – sequence: 1 givenname: You surname: Li fullname: Li, You organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 2 givenname: Nikolai T. surname: Klena fullname: Klena, Nikolai T. organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 3 givenname: George C. surname: Gabriel fullname: Gabriel, George C. organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 4 givenname: Xiaoqin surname: Liu fullname: Liu, Xiaoqin organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 5 givenname: Andrew J. surname: Kim fullname: Kim, Andrew J. organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 6 givenname: Kristi surname: Lemke fullname: Lemke, Kristi organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 7 givenname: Yu surname: Chen fullname: Chen, Yu organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 8 givenname: Bishwanath surname: Chatterjee fullname: Chatterjee, Bishwanath organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 9 givenname: William surname: Devine fullname: Devine, William organization: Department of Pathology, University of Pittsburgh School of Medicine – sequence: 10 givenname: Rama Rao surname: Damerla fullname: Damerla, Rama Rao organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 11 givenname: Chienfu surname: Chang fullname: Chang, Chienfu organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 12 givenname: Hisato surname: Yagi fullname: Yagi, Hisato organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 13 givenname: Jovenal T. surname: San Agustin fullname: San Agustin, Jovenal T. organization: Program in Molecular Medicine, University of Massachusetts Medical School – sequence: 14 givenname: Mohamed surname: Thahir fullname: Thahir, Mohamed organization: Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Intelligent Systems Program, School of Arts and Sciences, University of Pittsburgh – sequence: 15 givenname: Shane surname: Anderton fullname: Anderton, Shane organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 16 givenname: Caroline surname: Lawhead fullname: Lawhead, Caroline organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 17 givenname: Anita surname: Vescovi fullname: Vescovi, Anita organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 18 givenname: Herbert surname: Pratt fullname: Pratt, Herbert organization: The Jackson Laboratory – sequence: 19 givenname: Judy surname: Morgan fullname: Morgan, Judy organization: The Jackson Laboratory – sequence: 20 givenname: Leslie surname: Haynes fullname: Haynes, Leslie organization: The Jackson Laboratory – sequence: 21 givenname: Cynthia L. surname: Smith fullname: Smith, Cynthia L. organization: The Jackson Laboratory – sequence: 22 givenname: Janan T. surname: Eppig fullname: Eppig, Janan T. organization: The Jackson Laboratory – sequence: 23 givenname: Laura surname: Reinholdt fullname: Reinholdt, Laura organization: The Jackson Laboratory – sequence: 24 givenname: Richard surname: Francis fullname: Francis, Richard organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 25 givenname: Linda surname: Leatherbury fullname: Leatherbury, Linda organization: The Heart Center, Children’s National Medical Center – sequence: 26 givenname: Madhavi K. surname: Ganapathiraju fullname: Ganapathiraju, Madhavi K. organization: Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Intelligent Systems Program, School of Arts and Sciences, University of Pittsburgh – sequence: 27 givenname: Kimimasa surname: Tobita fullname: Tobita, Kimimasa organization: Department of Developmental Biology, University of Pittsburgh School of Medicine – sequence: 28 givenname: Gregory J. surname: Pazour fullname: Pazour, Gregory J. organization: Program in Molecular Medicine, University of Massachusetts Medical School – sequence: 29 givenname: Cecilia W. surname: Lo fullname: Lo, Cecilia W. email: cel36@pitt.edu organization: Department of Developmental Biology, University of Pittsburgh School of Medicine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25807483$$D View this record in MEDLINE/PubMed |
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| Snippet | A forward genetic screen in fetal mice to identify genes involved in congenital heart disease (CHD) reveals that a large proportion of genes associated with... Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births; the incidence of CHD is up to tenfold higher in human... Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births (1); the incidence of CHD is up to tenfold higher in... Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births; the incidence of CHD is up to ten-fold higher in human... Congenital heart disease (CHD) is the most prevalent birth defect, affecting nearly 1% of live births 1 , but the incidence of CHD is up to ten fold higher in... |
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| SubjectTerms | 14/19 14/63 45 45/23 45/70 631/208 64/60 Animals Birth defects Cardiovascular disease Cardiovascular diseases Cilia - diagnostic imaging Cilia - genetics Cilia - pathology Cilia - physiology Cilia and ciliary motion Congenital diseases Congenital heart disease Defects DNA Mutational Analysis Electrocardiography Embryos Exome - genetics Fetuses Genes, Recessive Genetic aspects Genetic Testing Genetics Genotype & phenotype Heart Defects, Congenital - diagnostic imaging Heart Defects, Congenital - genetics Heart Defects, Congenital - pathology Human populations Humanities and Social Sciences Humans letter Male Mice Mice, Inbred C57BL multidisciplinary Mutation Mutation - genetics Pathogenesis Proteins Rodents Science Signal Transduction Ultrasonography |
| Title | Global genetic analysis in mice unveils central role for cilia in congenital heart disease |
| URI | https://link.springer.com/article/10.1038/nature14269 https://www.ncbi.nlm.nih.gov/pubmed/25807483 https://www.proquest.com/docview/1684954960 https://pubmed.ncbi.nlm.nih.gov/PMC4617540 |
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