Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations

Gene linked to brain malformation The identification of genetic loci linked to abnormal cortical development is complicated by genetic heterogeneity, small family sizes and diagnostic classifications that do not reflect molecular pathogenesis. These obstacles have been overcome in a study using whol...

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Published in:Nature (London) Vol. 467; no. 7312; pp. 207 - 210
Main Authors: Bilgüvar, Kaya, Öztürk, Ali Kemal, Louvi, Angeliki, Kwan, Kenneth Y., Choi, Murim, Tatlı, Burak, Yalnızoğlu, Dilek, Tüysüz, Beyhan, Çağlayan, Ahmet Okay, Gökben, Sarenur, Kaymakçalan, Hande, Barak, Tanyeri, Bakırcıoğlu, Mehmet, Yasuno, Katsuhito, Ho, Winson, Sanders, Stephan, Zhu, Ying, Yılmaz, Sanem, Dinçer, Alp, Johnson, Michele H., Bronen, Richard A., Koçer, Naci, Per, Hüseyin, Mane, Shrikant, Pamir, Mehmet Necmettin, Yalçınkaya, Cengiz, Kumandaş, Sefer, Topçu, Meral, Özmen, Meral, Šestan, Nenad, Lifton, Richard P., State, Matthew W., Günel, Murat
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 09.09.2010
Nature Publishing Group
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ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract Gene linked to brain malformation The identification of genetic loci linked to abnormal cortical development is complicated by genetic heterogeneity, small family sizes and diagnostic classifications that do not reflect molecular pathogenesis. These obstacles have been overcome in a study using whole-exome sequencing. Recessive mutations in the WD repeat domain 62 ( WDR62 ) gene are shown to cause a wide spectrum of seemingly disparate brain abnormalities, including microcephaly, pachygyria and, in one instance, cerebellar hypoplasia. Unlike other known microcephaly genes, WDR62 does not associate with centrosomes; it is predominantly nuclear in localization and is expressed transiently in the neocortex during embryonic neurogenesis. Mapping disease loci that underlie putative Mendelian forms of malformations of cortical development is complicated by genetic heterogeneity, small family sizes and diagnostic classifications that may not reflect molecular pathogenesis. These authors use whole-exome sequencing to identify recessive mutations in WDR62 as the cause of a wide spectrum of severe cerebral cortical malformations. WDR62 's nuclear localization to germinal neuroepithelia indicates that cortical malformations can be caused by events during progenitor proliferation and neurogenesis. The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers 1 , 2 . An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development 3 , 4 , 5 , 6 . Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 ( WDR62 ) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
AbstractList The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers (1,2). An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development (3-6). Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 (WDR62)as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers. An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development. Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 (WDR62) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers. An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development. Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 (WDR62) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers. An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development. Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 (WDR62) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
Gene linked to brain malformation The identification of genetic loci linked to abnormal cortical development is complicated by genetic heterogeneity, small family sizes and diagnostic classifications that do not reflect molecular pathogenesis. These obstacles have been overcome in a study using whole-exome sequencing. Recessive mutations in the WD repeat domain 62 ( WDR62 ) gene are shown to cause a wide spectrum of seemingly disparate brain abnormalities, including microcephaly, pachygyria and, in one instance, cerebellar hypoplasia. Unlike other known microcephaly genes, WDR62 does not associate with centrosomes; it is predominantly nuclear in localization and is expressed transiently in the neocortex during embryonic neurogenesis. Mapping disease loci that underlie putative Mendelian forms of malformations of cortical development is complicated by genetic heterogeneity, small family sizes and diagnostic classifications that may not reflect molecular pathogenesis. These authors use whole-exome sequencing to identify recessive mutations in WDR62 as the cause of a wide spectrum of severe cerebral cortical malformations. WDR62 's nuclear localization to germinal neuroepithelia indicates that cortical malformations can be caused by events during progenitor proliferation and neurogenesis. The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers 1 , 2 . An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development 3 , 4 , 5 , 6 . Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 ( WDR62 ) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones, cell proliferation characterized by symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in six highly ordered, functionally specialized layers1,2. An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development3-6. Mapping of disease loci in putative Mendelian forms of malformations of cortical development has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WD repeat domain 62 (WDR62) as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygyria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with mutations in WDR62 had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mice and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. Expression of WDR62 in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the use of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging. [PUBLICATION ABSTRACT]
The development of the human cerebral cortex is an orchestrated process involving the birth of neural progenitors in the peri-ventricular germinal zones, cell proliferation characterized by both symmetric and asymmetric mitoses, followed by migration of post-mitotic neurons to their final destinations in 6 highly ordered, functionally-specialized layers1,2. An understanding of the molecular mechanisms guiding these intricate processes is in its infancy, substantially driven by the discovery of rare mutations that cause malformations of cortical development (MCD)3-6. Mapping of disease loci in putative Mendelian forms of MCD has been hindered by marked locus heterogeneity, small kindred sizes and diagnostic classifications that may not reflect molecular pathogenesis. Here we demonstrate the use of whole-exome sequencing to overcome these obstacles by identifying recessive mutations in WDR62 as the cause of a wide spectrum of severe cerebral cortical malformations including microcephaly, pachygria with cortical thickening as well as hypoplasia of the corpus callosum. Some patients with WDR62 mutations had evidence of additional abnormalities including lissencephaly, schizencephaly, polymicrogyria and, in one instance, cerebellar hypoplasia, all traits traditionally regarded as distinct entities. In mouse and humans, WDR62 transcripts and protein are enriched in neural progenitors within the ventricular and subventricular zones. WDR62 expression in the neocortex is transient, spanning the period of embryonic neurogenesis. Unlike other known microcephaly genes, WDR62 does not apparently associate with centrosomes and is predominantly nuclear in localization. These findings unify previously disparate aspects of cerebral cortical development and highlight the utility of whole-exome sequencing to identify disease loci in settings in which traditional methods have proved challenging.
Audience Academic
Author Zhu, Ying
Bronen, Richard A.
Choi, Murim
Mane, Shrikant
Kwan, Kenneth Y.
Koçer, Naci
Lifton, Richard P.
Johnson, Michele H.
Öztürk, Ali Kemal
Bakırcıoğlu, Mehmet
Barak, Tanyeri
Pamir, Mehmet Necmettin
Günel, Murat
Yasuno, Katsuhito
Yılmaz, Sanem
Kaymakçalan, Hande
Per, Hüseyin
Özmen, Meral
Dinçer, Alp
Šestan, Nenad
State, Matthew W.
Sanders, Stephan
Tüysüz, Beyhan
Tatlı, Burak
Ho, Winson
Bilgüvar, Kaya
Louvi, Angeliki
Yalnızoğlu, Dilek
Gökben, Sarenur
Topçu, Meral
Kumandaş, Sefer
Çağlayan, Ahmet Okay
Yalçınkaya, Cengiz
AuthorAffiliation 8 Department of Medical Genetics, Kayseri Education and Research Hospital, Kayseri, Turkey
13 Department of Radiology, School of Medicine, Acibadem University, Istanbul, Turkey
15 Department of Otolaryngology, Yale University School of Medicine, New Haven CT, 06510, USA
17 Division of Neurology, Department of Pediatrics, Erciyes University School of Medicine, Kayseri, Turkey
7 Division of Genetics, Department of Pediatrics, Istanbul University Cerrahpasa Faculty of Medicine, Istanbul, Turkey
12 Child Study Center, Yale University School of Medicine, New Haven CT, 06510, USA
2 Department of Neurobiology, Program on Neurogenetics, Yale University School of Medicine, New Haven CT, 06510, USA
1 Department of Neurosurgery, Program on Neurogenetics, Yale University School of Medicine, New Haven CT, 06510, USA
16 Department of Radiology, Istanbul University Cerrahpasa Faculty of Medicine, Istanbul, Turkey
9 Division of Neurology, Department of Pediatrics, Faculty of Medicine, Ege University, Izmir, Tu
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/20729831$$D View this record in MEDLINE/PubMed
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COPYRIGHT 2010 Nature Publishing Group
Copyright Nature Publishing Group Sep 9, 2010
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These authors contributed equally to the study
Author contributions M.W.S., R.P.L. and M.G. designed the study and K.B., A.L., N.S., R.P.L., and M.G. designed the experiments. K.B., A.K.O., A.L., K.Y.K., T.B., M.B., S.S., W.H., and S.M. performed the experiments. B.T., D.Y., B.T., A.O.C., S.G., H.K., S.Y., H.P., C.Y., S.K., M.T. and M.O. identified, consented and recruited the study subjects and provided clinical information. A.D., M.H.J., R.A.B., N.K. and M.N.P. performed and evaluated magnetic resonance imaging. M.C. and R.P.L. developed the bioinformatics scripts for data analysis. K.B., A.K.O., K.Y., A.L. and M.G. analyzed the genetics data. A.L., K.Y.K, Y.Z., N.S. and M.G. analyzed the expression data. K.B., A.K.O, A.L., R.P.L., M.W.S., and M.G. wrote the paper.
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Snippet Gene linked to brain malformation The identification of genetic loci linked to abnormal cortical development is complicated by genetic heterogeneity, small...
The development of the human cerebral cortex is an orchestrated process involving the generation of neural progenitors in the periventricular germinal zones,...
The development of the human cerebral cortex is an orchestrated process involving the birth of neural progenitors in the peri-ventricular germinal zones, cell...
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StartPage 207
SubjectTerms 631/208/212
631/208/2489/144
631/378/1689/2608
Abnormalities
Amino acids
Animals
Artificial chromosomes
Base Sequence
Brain - abnormalities
Brain - growth & development
Brain - pathology
Brain diseases
Brain Diseases - genetics
Brain Diseases - pathology
Cell Cycle Proteins
Cerebral cortex
DNA Mutational Analysis - methods
DNA sequencing
Enrichment
Female
Genes
Genes, Recessive
Genetic aspects
Genetics
Heterogeneity
Human
Human subjects
Humanities and Social Sciences
Humans
Intellectual disabilities
letter
Loci
Male
Medical imaging
Mice
Microcephaly - genetics
Microcephaly - pathology
Molecular Sequence Data
multidisciplinary
Mutation
Mutations
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
Nucleotide sequencing
Obstacles
Pedigree
Position (location)
Proteins
Schizencephaly
Science
Science (multidisciplinary)
Sequencing
Studies
Technological change
Title Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations
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Volume 467
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