Home LiteratureArticle Details
PMID: 24896178 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genome sequencing identifies major causes of severe intellectual disability.

Nature ·Vol. 511 ·No. 7509 ·2014-07-17 ·Pages 344-7

Gilissen C, Hehir-Kwa JY, Thung DT, van de Vorst M, van Bon BW, Willemsen MH, Kwint M, Janssen IM, Hoischen A, Schenck A, Leach R, Klein R, Tearle R, Bo T, Pfundt R, Yntema HG, de Vries BB, Kleefstra T, Brunner HG, Vissers LE, Veltman JA

Abstract

Severe intellectual disability (ID) occurs in 0.5% of newborns and is thought to be largely genetic in origin. The extensive genetic heterogeneity of this disorder requires a genome-wide detection of all types of genetic variation. Microarray studies and, more recently, exome sequencing have demonstrated the importance of de novo copy number variations (CNVs) and single-nucleotide variations (SNVs) in ID, but the majority of cases remain undiagnosed. Here we applied whole-genome sequencing to 50 patients with severe ID and their unaffected parents. All patients included had not received a molecular diagnosis after extensive genetic prescreening, including microarray-based CNV studies and exome sequencing. Notwithstanding this prescreening, 84 de novo SNVs affecting the coding region were identified, which showed a statistically significant enrichment of loss-of-function mutations as well as an enrichment for genes previously implicated in ID-related disorders. In addition, we identified eight de novo CNVs, including single-exon and intra-exonic deletions, as well as interchromosomal duplications. These CNVs affected known ID genes more frequently than expected. On the basis of diagnostic interpretation of all de novo variants, a conclusive genetic diagnosis was reached in 20 patients. Together with one compound heterozygous CNV causing disease in a recessive mode, this results in a diagnostic yield of 42% in this extensively studied cohort, and 62% as a cumulative estimate in an unselected cohort. These results suggest that de novo SNVs and CNVs affecting the coding region are a major cause of severe ID. Genome sequencing can be applied as a single genetic test to reliably identify and characterize the comprehensive spectrum of genetic variation, providing a genetic diagnosis in the majority of patients with severe ID.

MeSH Terms
Chromosomes, Human, Pair 4/genetics Chromosomes, Human, X/genetics Cohort Studies DNA Copy Number Variations/genetics Gene Duplication/genetics Genome, Human/genetics Guanine Nucleotide Exchange Factors/genetics Humans Intellectual Disability/genetics Male Mutation/genetics Polymorphism, Single Nucleotide/genetics Sequence Analysis, DNA
Chemicals
Guanine Nucleotide Exchange Factors IQSEC2 protein, human
Authors & Affiliations
21 authors, click to expand affiliations / ORCID
Gilissen Christian
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2].
Hehir-Kwa Jayne Y
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2].
Thung Djie Tjwan
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
van de Vorst Maartje
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
van Bon Bregje W M
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Willemsen Marjolein H
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Kwint Michael
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Janssen Irene M
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Hoischen Alexander
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Schenck Annette
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Leach Richard
Complete Genomics Inc. 2071 Stierlin Court, Mountain View, California 94043, USA.
Klein Robert
Complete Genomics Inc. 2071 Stierlin Court, Mountain View, California 94043, USA.
Tearle Rick
Complete Genomics Inc. 2071 Stierlin Court, Mountain View, California 94043, USA.
Bo Tan
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2] State Key Laboratory of Medical Genetics, Central South University. 110 Xiangya Road, Changsha, Hunan 410078, China.
Pfundt Rolph
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Yntema Helger G
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
de Vries Bert B A
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Kleefstra Tjitske
Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands.
Brunner Han G
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2] Department of Clinical Genetics, Maastricht University Medical Centre. Universiteitssingel 50, 6229 ER Maastricht, the Netherlands [3].
Vissers Lisenka E L M
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2].
Veltman Joris A
1] Department of Human Genetics, Radboud Institute for Molecular Life Sciences and Donders Centre for Neuroscience, Radboud University Medical Center, Geert Grooteplein 10, 6525 GA Nijmegen, the Netherlands [2] Department of Clinical Genetics, Maastricht University Medical Centre. Universiteitssingel 50, 6229 ER Maastricht, the Netherlands [3].
References (29)
29 references, click to expand
  1. Patterns and rates of exonic de novo mutations in autism spectrum disorders.
    Nature. 2012 Apr 04;485(7397):242-5 PMID: 22495311
  2. Diagnostic genome profiling in mental retardation.
    Am J Hum Genet. 2005 Oct;77(4):606-16 PMID: 16175506
  3. Genic intolerance to functional variation and the interpretation of personal genomes.
    PLoS Genet. 2013;9(8):e1003709 PMID: 23990802
  4. Deploying whole genome sequencing in clinical practice and public health: meeting the challenge one bin at a time.
    Genet Med. 2011 Jun;13(6):499-504 PMID: 21558861
  5. Whole-genome sequencing in a patient with Charcot-Marie-Tooth neuropathy.
    N Engl J Med. 2010 Apr 1;362(13):1181-91 PMID: 20220177
  6. Exome sequencing supports a de novo mutational paradigm for schizophrenia.
    Nat Genet. 2011 Aug 07;43(9):864-8 PMID: 21822266
  7. An integrated encyclopedia of DNA elements in the human genome.
    Nature. 2012 Sep 6;489(7414):57-74 PMID: 22955616
  8. Rate of de novo mutations and the importance of father's age to disease risk.
    Nature. 2012 Aug 23;488(7412):471-5 PMID: 22914163
  9. Formation of chimeric genes by copy-number variation as a mutational mechanism in schizophrenia.
    Am J Hum Genet. 2013 Oct 3;93(4):697-710 PMID: 24094746
  10. Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays.
    Science. 2010 Jan 1;327(5961):78-81 PMID: 19892942
  11. De novo gene disruptions in children on the autistic spectrum.
    Neuron. 2012 Apr 26;74(2):285-99 PMID: 22542183
  12. Increased exonic de novo mutation rate in individuals with schizophrenia.
    Nat Genet. 2011 Jul 10;43(9):860-3 PMID: 21743468
  13. Pathogenic or not? Assessing the clinical relevance of copy number variants.
    Clin Genet. 2013 Nov;84(5):415-21 PMID: 23895381
  14. Clinical significance of de novo and inherited copy-number variation.
    Hum Mutat. 2013 Dec;34(12):1679-87 PMID: 24038936
  15. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations.
    Nature. 2012 Apr 04;485(7397):246-50 PMID: 22495309
  16. De novo mutations in epileptic encephalopathies.
    Nature. 2013 Sep 12;501(7466):217-21 PMID: 23934111
  17. A de novo paradigm for mental retardation.
    Nat Genet. 2010 Dec;42(12):1109-12 PMID: 21076407
  18. Cohen syndrome is caused by mutations in a novel gene, COH1, encoding a transmembrane protein with a presumed role in vesicle-mediated sorting and intracellular protein transport.
    Am J Hum Genet. 2003 Jun;72(6):1359-69 PMID: 12730828
  19. Whole-genome sequencing in autism identifies hot spots for de novo germline mutation.
    Cell. 2012 Dec 21;151(7):1431-42 PMID: 23260136
  20. Computational techniques for human genome resequencing using mated gapped reads.
    J Comput Biol. 2012 Mar;19(3):279-92 PMID: 22175250
  21. A genomic view of mosaicism and human disease.
    Nat Rev Genet. 2013 May;14(5):307-20 PMID: 23594909
  22. Detection of clinically relevant genetic variants in autism spectrum disorder by whole-genome sequencing.
    Am J Hum Genet. 2013 Aug 8;93(2):249-63 PMID: 23849776
  23. Spatial and temporal mapping of de novo mutations in schizophrenia to a fetal prefrontal cortical network.
    Cell. 2013 Aug 1;154(3):518-29 PMID: 23911319
  24. Genetics of early onset cognitive impairment.
    Annu Rev Genomics Hum Genet. 2010;11:161-87 PMID: 20822471
  25. Diagnostic exome sequencing in persons with severe intellectual disability.
    N Engl J Med. 2012 Nov 15;367(20):1921-9 PMID: 23033978
  26. A systematic survey of loss-of-function variants in human protein-coding genes.
    Science. 2012 Feb 17;335(6070):823-8 PMID: 22344438
  27. Genomics, intellectual disability, and autism.
    N Engl J Med. 2012 Feb 23;366(8):733-43 PMID: 22356326
  28. De novo mutations revealed by whole-exome sequencing are strongly associated with autism.
    Nature. 2012 Apr 04;485(7397):237-41 PMID: 22495306
  29. Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study.
    Lancet. 2012 Nov 10;380(9854):1674-82 PMID: 23020937
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2014-07-17
Epub
2014-00-04
Pages
344-7
Language
English
Region
England
NLM ID
0410462
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]