Convergence of genes and cellular pathways dysregulated in autism spectrum disorders

American Journal of Human Genetics

Volumn 94, Issue 5, 2014, Pages 677-694

  Pinto, Dalila ^a   Delaby, Elsa ^b,c   Merico, Daniele ^d   Barbosa, Mafalda ^a   Merikangas, Alison ^e   Klei, Lambertus ^f   Thiruvahindrapuram, Bhooma ^d   Xu, Xiao ^a   Ziman, Robert ^d   Wang, Zhuozhi ^d   Vorstman, Jacob A S ^g   Thompson, Ann ^h   Regan, Regina ^i,j   Pilorge, Marion ^b,c   Pellecchia, Giovanna ^d   Pagnamenta, Alistair T ^k   Oliveira, Bárbara ^l,m   Marshall, Christian R ^d,n   Magalhaes, Tiago R ^i,j   Lowe, Jennifer K ^o   Howe, Jennifer L ^d   Griswold, Anthony J ^p   Gilbert, John ^p   Duketis, Eftichia ^q   Dombroski, Beth A ^r   De Jonge, Maretha V ^g   Cuccaro, Michael ^p   Crawford, Emily L ^s   Correia, Catarina T ^l,m   Conroy, Judith ^j,t   Conceição, Inês C ^l,m   Chiocchetti, Andreas G ^q   Casey, Jillian P ^i,j   Cai, Guiqing ^a   Cabrol, Christelle ^b,c   Bolshakova, Nadia ^e   Bacchelli, Elena ^u   Anney, Richard ^e   Gallinger, Steven ^v   Cotterchio, Michelle ^w   Casey, Graham ^x   Zwaigenbaum, Lonnie ^y   Wittemeyer, Kerstin ^z   Wing, Kirsty ^k   Wallace, Simon ^aa   Van Engeland, Herman ^g   Tryfon, Ana ^a,bl   Thomson, Susanne ^s   Soorya, Latha ^a,bm   Rogé, Bernadette ^ab   Roberts, Wendy ^ac   Poustka, Fritz ^q   Mouga, Susana ^ad,ae   Minshew, Nancy ^f   McInnes, L Alison ^a,bn   McGrew, Susan G ^s   Lord, Catherine ^af   Leboyer, Marion ^ag,ah,ai,aj   Le Couteur, Ann S ^ak   Kolevzon, Alexander ^a   Jiménez González, Patricia ^al   Jacob, Suma ^am,an   Holt, Richard ^k   Guter, Stephen ^am   Green, Jonathan ^ao,ap   Green, Andrew ^i,j   Gillberg, Christopher ^aq   Fernandez, Bridget A ^ar   Duque, Frederico ^ad,ae   Delorme, Richard ^ag,as,at,au   Dawson, Geraldine ^av   Chaste, Pauline ^f,ag   Café, Cátia ^ad   Brennan, Sean ^e   Bourgeron, Thomas ^ag,as,at,aw   Bolton, Patrick F ^ax,ay   Bölte, Sven ^q,bo   Bernier, Raphael ^az   Baird, Gillian ^ba   Bailey, Anthony J ^aa,bp   Anagnostou, Evdokia ^bb   Almeida, Joana ^ad   Wijsman, Ellen M ^az,bc   Vieland, Veronica J ^bd   Vicente, Astrid M ^l,m   Schellenberg, Gerard D ^r   Pericak Vance, Margaret ^p   Paterson, Andrew D ^d,n   Parr, Jeremy R ^ak   Oliveira, Guiomar ^ad,ae   Nurnberger, John I ^be   Monaco, Anthony P ^k,bf   Maestrini, Elena ^u   Klauck, Sabine M ^bg   Hakonarson, Hakon ^r,bh   Haines, Jonathan L ^s   Geschwind, Daniel H ^o   Freitag, Christine M ^q   Folstein, Susan E ^p   Ennis, Sean ^i,j   Coon, Hilary ^bi   Battaglia, Agatino ^bj   Szatmari, Peter ^h   Sutcliffe, James S ^s   Hallmayer, Joachim ^bk   Gill, Michael ^e   Cook, Edwin H ^am   Buxbaum, Joseph D ^a   Devlin, Bernie ^f   Gallagher, Louise ^e   Betancur, Catalina ^b,c   Scherer, Stephen W ^d,n   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b INSERM   (France)

^c and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^h MCMASTER UNIVERSITY   (Canada)

ⁱ OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^j UNIVERSITY COLLEGE DUBLIN   (Ireland)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^m UNIVERSITY OF LISBON   (Portugal)

ⁿ UNIVERSITY OF TORONTO   (Canada)

^o UNIVERSITY OF CALIFORNIA   (United States)

^p UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^q GOETHE UNIVERSITY   (Germany)

^r UNIVERSITY OF PENNSYLVANIA   (United States)

^s VANDERBILT UNIVERSITY   (United States)

^t CHILDREN S UNIVERSITY HOSPITAL   (Ireland)

^u UNIVERSITY OF BOLOGNA   (Italy)

^v MOUNT SINAI HOSPITAL   (Canada)

^w CANCER CARE ONTARIO   (Canada)

^x UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^y UNIVERSITY OF ALBERTA   (Canada)

^z UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^aa UNIVERSITY OF OXFORD   (United Kingdom)

^ab Université de Toulouse II Le Mirail   (France)

^ac HOSPITAL FOR SICK CHILDREN   (Canada)

^ad CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

^ae UNIVERSITY OF COIMBRA   (Portugal)

^af WEILL CORNELL MEDICAL CENTER   (United States)

^ag FONDATION FONDAMENTAL   (France)

^ah INSERM U955   (France)

^ai FACULTÉ DE MÉDECINE   (France)

^aj HENRI MONDOR HOSPITAL   (France)

^ak NEWCASTLE UNIVERSITY   (United Kingdom)

^al HOSPITAL NACIONAL DE NIÑOS   (Costa Rica)

^am UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^an UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^ao UNIVERSITY OF MANCHESTER   (United Kingdom)

^ap UNIVERSITY OF MANCHESTER   (United Kingdom)

^aq UNIVERSITY OF GOTHENBURG   (Sweden)

^ar MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^as INSTITUT PASTEUR   (France)

^at CNRS   (France)

^au HÔPITAL ROBERT DEBRÉ   (France)

^av DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^aw UNIVERSITÉ PARIS DESCARTES   (France)

^ax KING'S COLLEGE LONDON   (United Kingdom)

^ay King s College London   (United Kingdom)

^az UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^ba KING'S COLLEGE LONDON   (United Kingdom)

^bb University of Toronto   (Canada)

^bc UNIVERSITY OF WASHINGTON   (United States)

^bd THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^be INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^bf TUFTS UNIVERSITY   (United States)

^bg GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^bh CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^bi UNIVERSITY OF UTAH   (United States)

^bj DEPARTMENT OF DEVELOPMENTAL NEUROSCIENCE   (Italy)

^bk STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^bl UNIVERSITÉ DE MONTRÉAL   (Canada)

^bm RUSH UNIVERSITY MEDICAL CENTER   (United States)

^bn Battelle Center for Mathematical Medicine Research Institute at Nationwide Children's Hospital ^*  (United States)

^bo KAROLINSKA INSTITUTE   (Sweden)

^bp UNIVERSITY OF BRITISH COLUMBIA   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTISM; CHD2 GENE; CHROMATIN; CONTROLLED STUDY; CONVERGENT EVOLUTION; COPY NUMBER VARIATION; DEVELOPMENTAL GENE; FEMALE; FRAGILE X SYNDROME; GDI1 GENE; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; HDAC4 GENE; HDAC9 GENE; HUMAN; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MALE; MIR137 GENE; PRIORITY JOURNAL; SETD5 GENE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SYNAPTIC TRANSMISSION; X CHROMOSOME LINKED DISORDER; AUTOSOMAL DOMINANT INHERITANCE; BRACHYDACTYLY; CHROMOSOME ABERRATION; GENE INTERACTION; GENETIC RISK; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; OVERLAPPING GENE; SEGMENTAL DUPLICATION; SEX RATIO; SMITH MAGENIS SYNDROME;

BINDING PROTEIN; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 9; MICRORNA; RAB PROTEIN;

CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DNA COPY NUMBER VARIATIONS; FEMALE; GENE REGULATORY NETWORKS; HUMANS; MALE; METABOLIC NETWORKS AND PATHWAYS; MULTIGENE FAMILY; PEDIGREE; SEQUENCE DELETION;

EID: 84899918742     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.03.018     Document Type: Article

References (64)

1. J.N. Constantino, A. Todorov, C. Hilton, P. Law, Y. Zhang, E. Molloy, R. Fitzgerald, and D. Geschwind Autism recurrence in half siblings: strong support for genetic mechanisms of transmission in ASD Mol. Psychiatry 18 2013 137 138
2. D. Levy, M. Ronemus, B. Yamrom, Y.H. Lee, A. Leotta, J. Kendall, S. Marks, B. Lakshmi, D. Pai, and K. Ye et al. Rare de novo and transmitted copy-number variation in autistic spectrum disorders Neuron 70 2011 886 897
3. C.R. Marshall, A. Noor, J.B. Vincent, A.C. Lionel, L. Feuk, J. Skaug, M. Shago, R. Moessner, D. Pinto, and Y. Ren et al. Structural variation of chromosomes in autism spectrum disorder Am. J. Hum. Genet. 82 2008 477 488
4. S.J. Sanders, A.G. Ercan-Sencicek, V. Hus, R. Luo, M.T. Murtha, D. Moreno-De-Luca, S.H. Chu, M.P. Moreau, A.R. Gupta, and S.A. Thomson et al. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism Neuron 70 2011 863 885
5. P. Szatmari, A.D. Paterson, L. Zwaigenbaum, W. Roberts, J. Brian, X.Q. Liu, J.B. Vincent, J.L. Skaug, A.P. Thompson, L. Senman Autism Genome Project Consortium Mapping autism risk loci using genetic linkage and chromosomal rearrangements Nat. Genet. 39 2007 319 328
6. D. Pinto, A.T. Pagnamenta, L. Klei, R. Anney, D. Merico, R. Regan, J. Conroy, T.R. Magalhaes, C. Correia, and B.S. Abrahams et al. Functional impact of global rare copy number variation in autism spectrum disorders Nature 466 2010 368 372
7. I. Iossifov, M. Ronemus, D. Levy, Z. Wang, I. Hakker, J. Rosenbaum, B. Yamrom, Y.H. Lee, G. Narzisi, and A. Leotta et al. De novo gene disruptions in children on the autistic spectrum Neuron 74 2012 285 299
8. B.M. Neale, Y. Kou, L. Liu, A. Ma'ayan, K.E. Samocha, A. Sabo, C.F. Lin, C. Stevens, L.S. Wang, and V. Makarov et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders Nature 485 2012 242 245
9. S.J. Sanders, M.T. Murtha, A.R. Gupta, J.D. Murdoch, M.J. Raubeson, A.J. Willsey, A.G. Ercan-Sencicek, N.M. DiLullo, N.N. Parikshak, and J.L. Stein et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism Nature 485 2012 237 241
10. B.J. O'Roak, L. Vives, S. Girirajan, E. Karakoc, N. Krumm, B.P. Coe, R. Levy, A. Ko, C. Lee, and J.D. Smith et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations Nature 485 2012 246 250
11. T.W. Yu, M.H. Chahrour, M.E. Coulter, S. Jiralerspong, K. Okamura-Ikeda, B. Ataman, K. Schmitz-Abe, D.A. Harmin, M. Adli, and A.N. Malik et al. Using whole-exome sequencing to identify inherited causes of autism Neuron 77 2013 259 273
12. F. Béna, D.L. Bruno, M. Eriksson, C. van Ravenswaaij-Arts, Z. Stark, T. Dijkhuizen, E. Gerkes, S. Gimelli, D. Ganesamoorthy, and A.C. Thuresson et al. Molecular and clinical characterization of 25 individuals with exonic deletions of NRXN1 and comprehensive review of the literature Am. J. Med. Genet. B. Neuropsychiatr. Genet. 162B 2013 388 403
13. D. Moreno-De-Luca, S.J. Sanders, A.J. Willsey, J.G. Mulle, J.K. Lowe, D.H. Geschwind, M.W. State, C.L. Martin, and D.H. Ledbetter Using large clinical data sets to infer pathogenicity for rare copy number variants in autism cohorts Mol. Psychiatry 18 2013 1090 1095
14. A. Noor, A. Whibley, C.R. Marshall, P.J. Gianakopoulos, A. Piton, A.R. Carson, M. Orlic-Milacic, A.C. Lionel, D. Sato, D. Pinto Autism Genome Project Consortium Disruption at the PTCHD1 Locus on Xp22.11 in Autism spectrum disorder and intellectual disability Sci. Transl. Med. 2 2010 49ra68
15. Y.H. Jiang, R.K. Yuen, X. Jin, M. Wang, N. Chen, X. Wu, J. Ju, J. Mei, Y. Shi, and M. He et al. Detection of clinically relevant genetic variants in autism spectrum disorder by whole-genome sequencing Am. J. Hum. Genet. 93 2013 249 263
16. E.T. Lim, S. Raychaudhuri, S.J. Sanders, C. Stevens, A. Sabo, D.G. MacArthur, B.M. Neale, A. Kirby, D.M. Ruderfer, M. Fromer NHLBI Exome Sequencing Project Rare complete knockouts in humans: population distribution and significant role in autism spectrum disorders Neuron 77 2013 235 242
17. B. Devlin, and S.W. Scherer Genetic architecture in autism spectrum disorder Curr. Opin. Genet. Dev. 22 2012 229 237
18. C. Betancur Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting Brain Res. 1380 2011 42 77
19. J.D. Buxbaum, M.J. Daly, B. Devlin, T. Lehner, K. Roeder, M.W. State Autism Sequencing Consortium The autism sequencing consortium: large-scale, high-throughput sequencing in autism spectrum disorders Neuron 76 2012 1052 1056
20. R. Anney, L. Klei, D. Pinto, R. Regan, J. Conroy, T.R. Magalhaes, C. Correia, B.S. Abrahams, N. Sykes, and A.T. Pagnamenta et al. A genome-wide scan for common alleles affecting risk for autism Hum. Mol. Genet. 19 2010 4072 4082
21. R. Anney, L. Klei, D. Pinto, J. Almeida, E. Bacchelli, G. Baird, N. Bolshakova, S. Bölte, P.F. Bolton, and T. Bourgeron et al. Individual common variants exert weak effects on the risk for autism spectrum disorders Hum. Mol. Genet. 21 2012 4781 4792
22. C. Lord, M. Rutter, S. Goode, J. Heemsbergen, H. Jordan, L. Mawhood, and E. Schopler Autism diagnostic observation schedule: a standardized observation of communicative and social behavior J. Autism Dev. Disord. 19 1989 185 212
23. C. Lord, M. Rutter, and A. Le Couteur Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders J. Autism Dev. Disord. 24 1994 659 685
24. S. Risi, C. Lord, K. Gotham, C. Corsello, C. Chrysler, P. Szatmari, E.H. Cook Jr., B.L. Leventhal, and A. Pickles Combining information from multiple sources in the diagnosis of autism spectrum disorders J. Am. Acad. Child Adolesc. Psychiatry 45 2006 1094 1103
25. S.S. Sparrow, D.V. Cicchetti, and D.A. Balla Vineland Adaptive Behavior Scales, Second edition (Vineland-II) 2005 Pearson San Antonio
26. L.J. Bierut, A. Agrawal, K.K. Bucholz, K.F. Doheny, C. Laurie, E. Pugh, S. Fisher, L. Fox, W. Howells, S. Bertelsen Gene, Environment Association Studies Consortium A genome-wide association study of alcohol dependence Proc. Natl. Acad. Sci. USA 107 2010 5082 5087
27. J.C. Figueiredo, J.P. Lewinger, C. Song, P.T. Campbell, D.V. Conti, C.K. Edlund, D.J. Duggan, J. Rangrej, M. Lemire, and T. Hudson et al. Genotype-environment interactions in microsatellite stable/microsatellite instability-low colorectal cancer: results from a genome-wide association study Cancer Epidemiol. Biomarkers Prev. 20 2011 758 766
28. P.A. Newcomb, J. Baron, M. Cotterchio, S. Gallinger, J. Grove, R. Haile, D. Hall, J.L. Hopper, J. Jass, L. Le Marchand Colon Cancer Family Registry Colon Cancer Family Registry: an international resource for studies of the genetic epidemiology of colon cancer Cancer Epidemiol. Biomarkers Prev. 16 2007 2331 2343
29. C.S. Fox, Y. Liu, C.C. White, M. Feitosa, A.V. Smith, N. Heard-Costa, K. Lohman, A.D. Johnson, M.C. Foster, D.M. Greenawalt GIANT Consortium MAGIC Consortium GLGC Consortium Genome-wide association for abdominal subcutaneous and visceral adipose reveals a novel locus for visceral fat in women PLoS Genet. 8 2012 e1002695
30. D. Pinto, K. Darvishi, X. Shi, D. Rajan, D. Rigler, T. Fitzgerald, A.C. Lionel, B. Thiruvahindrapuram, J.R. Macdonald, and R. Mills et al. Comprehensive assessment of array-based platforms and calling algorithms for detection of copy number variants Nat. Biotechnol. 29 2011 512 520
31. G. Kirov, A.J. Pocklington, P. Holmans, D. Ivanov, M. Ikeda, D. Ruderfer, J. Moran, K. Chambert, D. Toncheva, and L. Georgieva et al. De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia Mol. Psychiatry 17 2012 142 153
32. H.M. Kearney, E.C. Thorland, K.K. Brown, F. Quintero-Rivera, S.T. South Working Group of the American College of Medical Genetics Laboratory Quality Assurance Committee American College of Medical Genetics standards and guidelines for interpretation and reporting of postnatal constitutional copy number variants Genet. Med. 13 2011 680 685
33. A. Bayés, L.N. van de Lagemaat, M.O. Collins, M.D. Croning, I.R. Whittle, J.S. Choudhary, and S.G. Grant Characterization of the proteome, diseases and evolution of the human postsynaptic density Nat. Neurosci. 14 2011 19 21
34. J.C. Darnell, S.J. Van Driesche, C. Zhang, K.Y. Hung, A. Mele, C.E. Fraser, E.F. Stone, C. Chen, J.J. Fak, and S.W. Chi et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism Cell 146 2011 247 261
35. N. Huang, I. Lee, E.M. Marcotte, and M.E. Hurles Characterising and predicting haploinsufficiency in the human genome PLoS Genet. 6 2010 e1001154
36. S.R. Gilman, I. Iossifov, D. Levy, M. Ronemus, M. Wigler, and D. Vitkup Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses Neuron 70 2011 898 907
37. E.J. Rossin, K. Lage, S. Raychaudhuri, R.J. Xavier, D. Tatar, Y. Benita, C. Cotsapas, M.J. Daly International Inflammatory Bowel Disease Genetics Constortium Proteins encoded in genomic regions associated with immune-mediated disease physically interact and suggest underlying biology PLoS Genet. 7 2011 e1001273
38. D. Malhotra, S. McCarthy, J.J. Michaelson, V. Vacic, K.E. Burdick, S. Yoon, S. Cichon, A. Corvin, S. Gary, and E.S. Gershon et al. High frequencies of de novo CNVs in bipolar disorder and schizophrenia Neuron 72 2011 951 963
39. M.T. Carter, S.M. Nikkel, B.A. Fernandez, C.R. Marshall, A. Noor, A.C. Lionel, A. Prasad, D. Pinto, A.M. Joseph-George, and C. Noakes et al. Hemizygous deletions on chromosome 1p21.3 involving the DPYD gene in individuals with autism spectrum disorder Clin. Genet. 80 2011 435 443
40. M.H. Willemsen, A. Vallès, L.A. Kirkels, M. Mastebroek, N. Olde Loohuis, A. Kos, W.M. Wissink-Lindhout, A.P. de Brouwer, W.M. Nillesen, and R. Pfundt et al. Chromosome 1p21.3 microdeletions comprising DPYD and MIR137 are associated with intellectual disability J. Med. Genet. 48 2011 810 818
41. Schizophrenia Psychiatric Genome-Wide Association Study (GWAS) Consortium Genome-wide association study identifies five new schizophrenia loci Nat. Genet. 43 2011 969 976
42. J. Vandewalle, H. Van Esch, K. Govaerts, J. Verbeeck, C. Zweier, I. Madrigal, M. Mila, E. Pijkels, I. Fernandez, and J. Kohlhase et al. Dosage-dependent severity of the phenotype in patients with mental retardation due to a recurrent copy-number gain at Xq28 mediated by an unusual recombination Am. J. Hum. Genet. 85 2009 809 822
43. N. Urraca, J. Cleary, V. Brewer, E.K. Pivnick, K. McVicar, R.L. Thibert, N.C. Schanen, C. Esmer, D. Lamport, and L.T. Reiter The interstitial duplication 15q11.2-q13 syndrome includes autism, mild facial anomalies and a characteristic EEG signature Autism Res. 6 2013 268 279
44. P.N. Robinson, S. Köhler, S. Bauer, D. Seelow, D. Horn, and S. Mundlos The Human Phenotype Ontology: a tool for annotating and analyzing human hereditary disease Am. J. Hum. Genet. 83 2008 610 615
45. C.L. Smith, C.A. Goldsmith, and J.T. Eppig The Mammalian Phenotype Ontology as a tool for annotating, analyzing and comparing phenotypic information Genome Biol. 6 2005 R7
46. D.J. Turner, M. Miretti, D. Rajan, H. Fiegler, N.P. Carter, M.L. Blayney, S. Beck, and M.E. Hurles Germline rates of de novo meiotic deletions and duplications causing several genomic disorders Nat. Genet. 40 2008 90 95
47. X. Gai, H.M. Xie, J.C. Perin, N. Takahashi, K. Murphy, A.S. Wenocur, M. D'arcy, R.J. O'Hara, E. Goldmuntz, and D.E. Grice et al. Rare structural variation of synapse and neurotransmission genes in autism Mol. Psychiatry 17 2012 402 411
48. P. Stankiewicz, S. Kulkarni, A.V. Dharmadhikari, S. Sampath, S.S. Bhatt, T.H. Shaikh, Z. Xia, A.N. Pursley, M.L. Cooper, and M. Shinawi et al. Recurrent deletions and reciprocal duplications of 10q11.21q11.23 including CHAT and SLC18A3 are likely mediated by complex low-copy repeats Hum. Mutat. 33 2012 165 179
49. G.L. Carvill, S.B. Heavin, S.C. Yendle, J.M. McMahon, B.J. O'Roak, J. Cook, A. Khan, M.O. Dorschner, M. Weaver, and S. Calvert et al. Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1 Nat. Genet. 45 2013 825 830
50. A. Rauch, D. Wieczorek, E. Graf, T. Wieland, S. Endele, T. Schwarzmayr, B. Albrecht, D. Bartholdi, J. Beygo, and N. Di Donato et al. Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study Lancet 380 2012 1674 1682
51. S. Schoch, P.E. Castillo, T. Jo, K. Mukherjee, M. Geppert, Y. Wang, F. Schmitz, R.C. Malenka, and T.C. Südhof RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone Nature 415 2002 321 326
52. J. de Ligt, M.H. Willemsen, B.W. van Bon, T. Kleefstra, H.G. Yntema, T. Kroes, A.T. Vulto-van Silfhout, D.A. Koolen, P. de Vries, and C. Gilissen et al. Diagnostic exome sequencing in persons with severe intellectual disability N. Engl. J. Med. 367 2012 1921 1929
53. B. Xu, I. Ionita-Laza, J.L. Roos, B. Boone, S. Woodrick, Y. Sun, S. Levy, J.A. Gogos, and M. Karayiorgou De novo gene mutations highlight patterns of genetic and neural complexity in schizophrenia Nat. Genet. 44 2012 1365 1369
54. M.H. Berryer, F.F. Hamdan, L.L. Klitten, R.S. Møller, L. Carmant, J. Schwartzentruber, L. Patry, S. Dobrzeniecka, D. Rochefort, and M. Neugnot-Cerioli et al. Mutations in SYNGAP1 cause intellectual disability, autism, and a specific form of epilepsy by inducing haploinsufficiency Hum. Mutat. 34 2013 385 394
55. E. Khurana, Y. Fu, J. Chen, and M. Gerstein Interpretation of genomic variants using a unified biological network approach PLoS Comput. Biol. 9 2013 e1002886
56. E.B. Robinson, P. Lichtenstein, H. Anckarsäter, F. Happé, and A. Ronald Examining and interpreting the female protective effect against autistic behavior Proc. Natl. Acad. Sci. USA 110 2013 5258 5262
57. D. Sato, A.C. Lionel, C.S. Leblond, A. Prasad, D. Pinto, S. Walker, I. O'Connor, C. Russell, I.E. Drmic, and F.F. Hamdan et al. SHANK1 deletions in males with autism spectrum disorder Am. J. Hum. Genet. 90 2012 879 887
58. M. Tropeano, J.W. Ahn, R.J. Dobson, G. Breen, J. Rucker, A. Dixit, D.K. Pal, P. McGuffin, A. Farmer, and P.S. White et al. Male-biased autosomal effect of 16p13.11 copy number variation in neurodevelopmental disorders PLoS ONE 8 2013 e61365
59. M. Ascano Jr., N. Mukherjee, P. Bandaru, J.B. Miller, J.D. Nusbaum, D.L. Corcoran, C. Langlois, M. Munschauer, S. Dewell, and M. Hafner et al. FMRP targets distinct mRNA sequence elements to regulate protein expression Nature 492 2012 382 386
60. J.C. Darnell Defects in translational regulation contributing to human cognitive and behavioral disease Curr. Opin. Genet. Dev. 21 2011 465 473
61. J.J. Day, and J.D. Sweatt Epigenetic mechanisms in cognition Neuron 70 2011 813 829
62. C. Gross, M. Nakamoto, X. Yao, C.B. Chan, S.Y. Yim, K. Ye, S.T. Warren, and G.J. Bassell Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome J. Neurosci. 30 2010 10624 10638
63. A. Sharma, C.A. Hoeffer, Y. Takayasu, T. Miyawaki, S.M. McBride, E. Klann, and R.S. Zukin Dysregulation of mTOR signaling in fragile X syndrome J. Neurosci. 30 2010 694 702
64. C. Albertinazzi, D. Gilardelli, S. Paris, R. Longhi, and I. de Curtis Overexpression of a neural-specific rho family GTPase, cRac1B, selectively induces enhanced neuritogenesis and neurite branching in primary neurons J. Cell Biol. 142 1998 815 825