Evidence for contribution of common genetic variants within chromosome 8p21.2-8p21.1 to restricted and repetitive behaviors in autism spectrum disorders

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Tao, Yu ^a   Gao, Hui ^a   Ackerman, Benjamin ^b,c   Guo, Wei ^c   Saffen, David ^a   Shugart, Yin Yao ^c  

^a FUDAN UNIVERSITY   (China)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Autism Diagnostic Interview Revised (ADI R); Autism Spectrum Disorders (ASD); Genome Wide Association Study; Restricted and Repetitive Behaviors (RRB)

Indexed keywords

MESSENGER RNA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 2 BETA; STATHMIN; STATHMIN LIKE 4; UNCLASSIFIED DRUG;

ADULT; ANCESTRY GROUP; ARTICLE; AUTISM; AUTISM ASSESSMENT; AUTISM DIAGNOSTIC INTERVIEW REVISED; AUTISM GENETIC RESOURCE EXCHANGE; BEHAVIOR; CHROMOSOME; CHROMOSOME 8P21; COHORT ANALYSIS; COMPARATIVE STUDY; COMPULSION; CONTROLLED STUDY; CORRELATIONAL STUDY; EUROPEAN; FEMALE; GENE; GENE EXPRESSION; GENE REPLICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; HUMAN; INSISTENCE ON SAMENESS; MALE; NERVE CELL DIFFERENTIATION; PHENOTYPE; PREFRONTAL CORTEX; PTK2B GENE; REPETITIVE SENSORY MOTOR; RESTRICTED BEHAVIOR; SENSORIMOTOR FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STMN4 GENE; CAUCASIAN; CHROMOSOME 8; GENETICS; GENOTYPE; QUANTITATIVE TRAIT LOCUS;

AUTISM SPECTRUM DISORDER; CHROMOSOMES, HUMAN, PAIR 8; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84978648845     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2475-y     Document Type: Article

References (83)

1. Abrahams BS, Geschwind DH. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet. 2008;9(5):341-55.
2. Fombonne E. Epidemiology of pervasive developmental disorders. Pediatr Res. 2009;65(6):591-8.
3. Gillberg C. Infantile autism and other childhood psychoses in a Swedish urban region. Epidemiological aspects. J Child Psychol Psychiatry. 1984;25(1):35-43.
4. Kim YS, Leventhal BL, Koh YJ, Fombonne E, Laska E, Lim EC, et al. Prevalence of autism spectrum disorders in a total population sample. Am J Psychiatry. 2011;168(9):904-12.
5. Elsabbagh M, Divan G, Koh YJ, Kim YS, Kauchali S, Marcin C, et al. Global prevalence of autism and other pervasive developmental disorders. Autism research: official journal of the International Society for Autism Research. 2012;5(3):160-79.
6. Geschwind DH. Advances in Autism. Annu Rev Med. 2009;60:367-80.
7. Berg JM, Geschwind DH. Autism genetics: searching for specificity and convergence. Genome Biol. 2012;13(7):247.
8. Geschwind DH, State MW. Gene hunting in autism spectrum disorder: on the path to precision medicine. The Lancet Neurology 2015;14(11):1109-20.
9. Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS, et al. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature. 2009;459(7246):528-33.
10. Ma D, Salyakina D, Jaworski JM, Konidari I, Whitehead PL, Andersen AN, et al. A genome-wide association study of autism reveals a common novel risk locus at 5p14.1. Ann Hum Genet. 2009;73(Pt 3):263-73.
11. Weiss LA, Arking DE, Daly MJ, Chakravarti A. A genome-wide linkage and association scan reveals novel loci for autism. Nature. 2009;461(7265):802-8.
12. Anney R, Klei L, Pinto D, Regan R, Conroy J, Magalhaes TR, et al. A genome-wide scan for common alleles affecting risk for autism. Hum Mol Genet. 2010;19(20):4072-82.
13. Anney R, Klei L, Pinto D, Almeida J, Bacchelli E, Baird G, et al. Individual common variants exert weak effects on the risk for autism spectrum disorderspi. Hum Mol Genet. 2012;21(21):4781-92.
14. Xia K, Guo H, Hu Z, Xun G, Zuo L, Peng Y, et al. Common genetic variants on 1p13.2 associate with risk of autism. Mol Psychiatry. 2014;19(11):1212-9.
15. Jeste SS, Geschwind DH. Disentangling the heterogeneity of autism spectrum disorder through genetic findings. Nat Rev Neurol. 2014;10(2):74-81.
16. Hu VW, Addington A, Hyman A. Novel autism subtype-dependent genetic variants are revealed by quantitative trait and subphenotype association analyses of published GWAS data. PLoS One. 2011;6(4):e19067.
17. O'Roak BJ, Stessman HA, Boyle EA, Witherspoon KT, Martin B, Lee C, Vives L, Baker C, Hiatt JB, Nickerson DA, et al. Recurrent de novo mutations implicate novel genes underlying simplex autism risk. Nat Commun. 2014;5:5595.
18. Coe BP, Witherspoon K, Rosenfeld JA. Refining analyses of copy number variation identifies specific genes associated with developmental delay. Nat Genet. 2014;46(10):1063-71.
19. Lowe JK, Werling DM, Constantino JN, Cantor RM, Geschwind DH. Social responsiveness, an autism endophenotype: genomewide significant linkage to two regions on chromosome 8. Am J Psychiatry. 2015;172(3):266-75.
20. Leekam SR, Prior MR, Uljarevic M. Restricted and repetitive behaviors in autism spectrum disorders: a review of research in the last decade. Psychol Bull. 2011;137(4):562-93.
21. Mandy WP, Skuse DH. Research review: What is the association between the social-communication element of autism and repetitive interests, behaviours and activities? J Child Psychol Psychiatry. 2008;49(8):795-808.
22. Silverman JM, Smith CJ, Schmeidler J, Hollander E, Lawlor BA, Fitzgerald M, et al. Symptom domains in autism and related conditions: evidence for familiality. Am J Med Genet. 2002;114(1):64-73.
23. Veatch OJ, Veenstra-Vanderweele J, Potter M, Pericak-Vance MA, Haines JL. Genetically meaningful phenotypic subgroups in autism spectrum disorders. Genes Brain Behav. 2014;13(3):276-85.
24. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659-85.
25. Cannon DS, Miller JS, Robison RJ, Villalobos ME, Wahmhoff NK, Allen-Brady K, et al. Genome-wide linkage analyses of two repetitive behavior phenotypes in Utah pedigrees with autism spectrum disorders. Molecular autism. 2010;1(1):3.
26. Liu XQ, Paterson AD, Szatmari P. Genome-wide linkage analyses of quantitative and categorical autism subphenotypes. Biol Psychiatry. 2008;64(7):561-70.
27. Bishop SL, Hus V, Duncan A, Huerta M, Gotham K, Pickles A, et al. Subcategories of restricted and repetitive behaviors in children with autism spectrum disorders. J Autism Dev Disord. 2013;43(6):1287-97.
28. Lewis M, Kim SJ. The pathophysiology of restricted repetitive behavior. J Neurodev Disord. 2009;1(2):114-32.
29. Bishop SL, Richler J, Lord C. Association between restricted and repetitive behaviors and nonverbal IQ in children with autism spectrum disorders. Child neuropsychology: a journal on normal and abnormal development in childhood and adolescence. 2006;12(4-5):247-67.
30. Cuccaro ML, Shao Y, Grubber J, Slifer M, Wolpert CM, Donnelly SL, et al. Factor analysis of restricted and repetitive behaviors in autism using the Autism Diagnostic Interview-R. Child Psychiatry Hum Dev. 2003;34(1):3-17.
31. Shao Y, Cuccaro ML, Hauser ER, Raiford KL, Menold MM, Wolpert CM, et al. Fine mapping of autistic disorder to chromosome 15q11-q13 by use of phenotypic subtypes. Am J Hum Genet. 2003;72(3):539-48.
32. Szatmari P, Georgiades S, Bryson S, Zwaigenbaum L, Roberts W, Mahoney W, et al. Investigating the structure of the restricted, repetitive behaviours and interests domain of autism. J Child Psychol Psychiatry. 2006;47(6):582-90.
33. Hus V, Pickles A, Cook Jr EH, Risi S, Lord C. Using the autism diagnostic interview--revised to increase phenotypic homogeneity in genetic studies of autism. Biol Psychiatry. 2007;61(4):438-48.
34. Lam KS, Bodfish JW, Piven J. Evidence for three subtypes of repetitive behavior in autism that differ in familiality and association with other symptoms. J Child Psychol Psychiatry. 2008;49(11):1193-200.
35. Geschwind DH, Sowinski J, Lord C, Iversen P, Shestack J, Jones P, et al. The autism genetic resource exchange: a resource for the study of autism and related neuropsychiatric conditions. Am J Hum Genet. 2001;69(2):463-6.
36. Lord C, Risi S, Lambrecht L, Cook Jr EH, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205-23.
37. Fischbach GD, Lord C. The Simons Simplex Collection: a resource for identification of autism genetic risk factors. Neuron. 2010;68(2):192-5.
38. Spiker D, Lotspeich LJ, Dimiceli S, Myers RM, Risch N. Behavioral phenotypic variation in autism multiplex families: evidence for a continuous severity gradient. Am J Med Genet. 2002;114(2):129-36.
39. Howie BN, Donnelly P, Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009;5(6):e1000529.
40. Howie B, Marchini J, Stephens M. Genotype imputation with thousands of genomes. G3 (Bethesda). 2011;1(6):457-70.
41. Delaneau O, Marchini J, Zagury JF. A linear complexity phasing method for thousands of genomes. Nat Methods. 2012;9(2):179-81.
42. Team RDC. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2010.
43. Dunteman GH. Principal Component Analysis, Quantitative Applications in the Social Sciences. Thousand Oaks: Sage; 1989.
44. Zhou X, Stephens M. Efficient multivariate linear mixed model algorithms for genome-wide association studies. Nat Methods. 2014;11(4):407-9.
45. Galesloot TE, van Steen K, Kiemeney LA, Janss LL, Vermeulen SH. A comparison of multivariate genome-wide association methods. PLoS One. 2014;9(4):e95923.
46. Yang Q, Wang Y. Methods for Analyzing Multivariate Phenotypes in Genetic Association Studies. J Probab Stat. 2012;2012:652569.
47. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Methodol. 1995;57(1):289-300.
48. Numata S, Ye T, Hyde TM, Guitart-Navarro X, Tao R, Wininger M, et al. DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet. 2012;90(2):260-72.
49. Zhu M, Tao Y, He Q, Gao H, Song F, Sun YM, et al. A common GSAP promoter variant contributes to Alzheimer's disease liability. Neurobiol Aging. 2014;35(11):2656. e2651-2657.
50. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.
51. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1-13.
52. Stone JL, Merriman B, Cantor RM, Yonan AL, Gilliam TC, Geschwind DH, et al. Evidence for sex-specific risk alleles in autism spectrum disorder. Am J Hum Genet. 2004;75(6):1117-23.
53. Tabares-Seisdedos R, Rubenstein JL. Chromosome 8p as a potential hub for developmental neuropsychiatric disorders: implications for schizophrenia, autism and cancer. Mol Psychiatry. 2009;14(6):563-89.
54. Holmans PA, Riley B, Pulver AE, Owen MJ, Wildenauer DB, Gejman PV, et al. Genomewide linkage scan of schizophrenia in a large multicenter pedigree sample using single nucleotide polymorphisms. Mol Psychiatry. 2009;14(8):786-95.
55. Koide T, Aleksic B, Ito Y, Usui H, Yoshimi A, Inada T, et al. A two-stage case-control association study of the dihydropyrimidinase-like 2 gene (DPYSL2) with schizophrenia in Japanese subjects. J Hum Genet. 2010;55(7):469-72.
56. Cheng C, Chiu HJ, el Loh W, Chan CH, Hwu TM, Liu YR, et al. Association of the ADRA1A gene and the severity of metabolic abnormalities in patients with schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2012;36(1):205-10.
57. Fallin MD, Lasseter VK, Liu Y, Avramopoulos D, McGrath J, Wolyniec PS, et al. Linkage and association on 8p21.2-p21.1 in schizophrenia. Am J Med Genet B Neuropsychiatr Genet. 2011;156(2):188-97.
58. de Lacy N, King BH. Revisiting the relationship between autism and schizophrenia: toward an integrated neurobiology. Annu Rev Clin Psychol. 2013;9:555-87.
59. Crespi BJ. Revisiting Bleuler: relationship between autism and schizophrenia. The British journal of psychiatry: the journal of mental science. 2010;196(6):495. author reply 495-496.
60. Tracy JI, de Leon J, Qureshi G, McCann EM, McGrory A, Josiassen RC. Repetitive behaviors in schizophrenia: a single disturbance or discrete symptoms? Schizophr Res. 1996;20(1-2):221-9.
61. Bieche I, Maucuer A, Laurendeau I, Lachkar S, Spano AJ, Frankfurter A, et al. Expression of stathmin family genes in human tissues: non-neural-restricted expression for SCLIP. Genomics. 2003;81(4):400-10.
62. Ohkawa N, Fujitani K, Tokunaga E, Furuya S, Inokuchi K. The microtubule destabilizer stathmin mediates the development of dendritic arbors in neuronal cells. J Cell Sci. 2007;120(Pt 8):1447-56.
63. Wang X, Bao X, Pal R, Agbas A, Michaelis E. Transcriptomic responses in mouse brain exposed to chronic excess of the neurotransmitter glutamate. BMC Genomics. 2010;11(1):360.
64. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, et al. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 2012;22(9):1790-7.
65. Hu VW, Nguyen A, Kim KS, Steinberg ME, Sarachana T, Scully MA, et al. Gene expression profiling of lymphoblasts from autistic and nonaffected sib pairs: altered pathways in neuronal development and steroid biosynthesis. PLoS One. 2009;4(6):e5775.
66. Whalley K. Autism: Converging pathways. Nat Rev Neurosci. 2011;12(7):372.
67. Betancur C, Sakurai T, Buxbaum JD. The emerging role of synaptic cell-adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci. 2009;32(7):402-12.
68. Geschwind DH. Genetics of autism spectrum disorders. Trends Cogn Sci. 2011;15(9):409-16.
69. Papanikolaou K, Paliokosta E, Gyftodimou J, Kolaitis G, Vgenopoulou S, Sarri C, et al. A case of partial trisomy of chromosome 8p associated with autism. J Autism Dev Disord. 2006;36(5):705-9.
70. Ozgen HM, Staal WG, Barber JC, de Jonge MV, Eleveld MJ, Beemer FA, et al. A novel 6.14 Mb duplication of chromosome 8p21 in a patient with autism and self mutilation. J Autism Dev Disord. 2009;39(2):322-9.
71. Ludemann N, Clement A, Hans VH, Leschik J, Behl C, Brandt R. O-glycosylation of the tail domain of neurofilament protein M in human neurons and in spinal cord tissue of a rat model of amyotrophic lateral sclerosis (ALS). J Biol Chem. 2005;280(36):31648-58.
72. Goldman B, Rebolj M, Rygaard C, Preisler S, Ejegod DM, Lynge E, et al. Patterns of cervical coinfection with multiple human papilloma virus types in a screening population in Denmark. Vaccine. 2013;31(12):1604-9.
73. Ribich S, Tasic B, Maniatis T. Identification of long-range regulatory elements in the protocadherin-alpha gene cluster. Proc Natl Acad Sci U S A. 2006;103(52):19719-24.
74. Smallwood A, Ren B. Genome organization and long-range regulation of gene expression by enhancers. Curr Opin Cell Biol. 2013;25(3):387-94.
75. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol. 2009;29(10):2570-81.
76. Tang G, Gudsnuk K, Kuo SH, Cotrina ML, Rosoklija G, Sosunov A, et al. Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron. 2014;83(5):1131-43.
77. Hagberg H, Mallard C, Rousset CI, Thornton C. Mitochondria: hub of injury responses in the developing brain. The Lancet Neurology. 2014;13(2):217-32.
78. Lambert JC, Ibrahim-Verbaas CA, Harold D, Naj AC, Sims R, Bellenguez C, et al. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat Genet. 2013;45(12):1452-8.
79. Taniyama Y, Weber DS, Rocic P, Hilenski L, Akers ML, Park J, et al. Pyk2- and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol Cell Biol. 2003;23(22):8019-29.
80. Kim HG, Kishikawa S, Higgins AW, Seong IS, Donovan DJ, Shen Y, et al. Disruption of neurexin 1 associated with autism spectrum disorder. Am J Hum Genet. 2008;82(1):199-207.
81. Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J, Liu XQ, et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet. 2007;39(3):319-28.
82. Bertocchi C, Vaman Rao M, Zaidel-Bar R. Regulation of adherens junction dynamics by phosphorylation switches. J Signal Transduct. 2012;2012:125295.
83. Martin ER, Monks SA, Warren LL, Kaplan NL. A test for linkage and association in general pedigrees: the pedigree disequilibrium test. Am J Hum Genet. 2000;67(1):146-54.