A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism

Molecular Autism

Volumn 2, Issue 1, 2011, Pages

  Hussman, John P ^a   Chung, Ren Hua ^b   Griswold, Anthony J ^b   Jaworski, James M ^b   Salyakina, Daria ^b   Ma, Deqiong ^b   Konidari, Ioanna ^b   Whitehead, Patrice L ^b   Vance, Jeffery M ^b   Martin, Eden R ^b   Cuccaro, Michael L ^b   Gilbert, John R ^b   Haines, Jonathan L ^c   Pericak Vance, Margaret A ^b  

^a Hussman Foundation   (United States)

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

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTISM; COMPUTER SIMULATION; CONTROLLED STUDY; DENDRITE; FAMILY; FOLLOW UP; GENE LINKAGE DISEQUILIBRIUM; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; NERVE FIBER; NERVE FIBER GROWTH; NOISE REDUCTION; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 79960938123     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-2-1     Document Type: Article

References (89)

1. Test for linear trends in proportions and frequencies. Armitage P, Biometrics 1955 11 375 386 10.2307/3001775
2. Genome-wide association studies for complex traits: consensus, uncertainty and challenges. McCarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, Ioannidis JP, Hirschhorn JN, Nat Rev Genet 2008 9 356 369 10.1038/nrg2344 18398418 (Pubitemid 351556063)
3. Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Zaykin DV, Westfall PH, Young SS, Karnoub MA, Wagner MJ, Ehm MG, Hum Hered 2002 53 79 91 10.1159/000057986 12037407 (Pubitemid 34621657)
4. Regression-based association analysis with clustered haplotypes through use of genotypes. Tzeng JY, Wang CH, Kao JT, Hsiao CK, Am J Hum Genet 2006 78 231 242 10.1086/500025 16365833 (Pubitemid 43157563)
5. A new association test using haplotype similarity. Sha Q, Chen HS, Zhang S, Genet Epidemiol 2007 31 577 593 10.1002/gepi.20230 17443704 (Pubitemid 350246543)
6. Generalized T2 test for genome association studies. Xiong M, Zhao J, Boerwinkle E, Am J Hum Genet 2002 70 1257 1268 10.1086/340392 11923914 (Pubitemid 34450575)
7. A new multimarker test for family-based association studies. Rakovski CS, Xu X, Lazarus R, Blacker D, Laird NM, Genet Epidemiol 2007 31 9 17 10.1002/gepi.20186 17086514 (Pubitemid 46033527)
8. Haplotypes vs single marker linkage disequilibrium tests: what do we gain? Akey J, Jin L, Xiong M, Eur J Hum Genet 2001 9 291 300 10.1038/sj.ejhg.5200619 11313774 (Pubitemid 32366698)
9. Genome association studies of complex diseases by case-control designs. Fan R, Knapp M, Am J Hum Genet 2003 72 850 868 10.1086/373966 12647259 (Pubitemid 36403305)
10. Follow-up analysis of genome-wide association data identifies novel loci for type 1 diabetes. Grant SF, Qu HQ, Bradfield JP, Marchand L, Kim CE, Glessner JT, Grabs R, Taback SP, Frackelton EC, Eckert AW, DCCT/EDIC Research Group, et al. Diabetes 2009 58 290 295 10.2337/db08-1022 18840781
11. Comprehensive follow-up of the first genome-wide association study of multiple sclerosis identifies KIF21B and TMEM39A as susceptibility loci. International Multiple Sclerosis Genetics Consortium (IMSGC), Hum Mol Genet 2010 19 953 962 10.1093/hmg/ddp542 20007504
12. A twin study of autism in Denmark, Finland, Iceland, Norway, and Sweden. Steffenburg S, Gillberg C, Hellgren L, Andersson L, Gillberg IC, Jakobsson G, Bohman M, J Child Psychol Psychiatry 1989 30 405 416 10.1111/j.1469-7610.1989. tb00254.x 2745591 (Pubitemid 19131643)
13. Autism as a strongly genetic disorder: evidence from a British twin study. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, Rutter M, Psychol Med 1995 25 63 77 10.1017/S0033291700028099 7792363
14. A case-control family history study of autism. Bolton P, Macdonald H, Pickles A, Rios P, Goode S, Crowson M, Bailey A, Rutter M, J Child Psychol Psychiatry Allied Disciplines 1994 35 877 900 10.1111/j.1469-7610.1994.tb02300.x (Pubitemid 24213267)
15. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders (DSM-IV), Text Revision Washington, DC: American Psychiatric Press 2000
16. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C, Autism Research International Sibpair Study, et al. Nat Genet 2003 34 27 29 10.1038/ng1136 12669065 (Pubitemid 36548785)
17. Structural variation of chromosomes in autism spectrum disorder. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, et al. Am J Hum Genet 2008 82 477 488 10.1016/j.ajhg.2007.12.009 18252227
18. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS, Salyakina D, Imielinski M, Bradfield JP, Sleiman PM, et al. Nature 2009 459 528 533 10.1038/nature07999 19404256
19. A genome-wide association study of autism reveals a common novel risk locus at 5p14.1. Ma D, Salyakina D, Jaworski JM, Konidari I, Whitehead PL, Andersen AN, Hoffman JD, Slifer SH, Hedges DJ, Cukier HN, et al. Ann Hum Genet 2009 73 263 273 10.1111/j.1469-1809.2009.00523.x 19456320
20. A genome-wide linkage and association scan reveals novel loci for autism. Weiss LA, Arking DE, Gene Discovery Project of Johns Hopkins & the Autism Consortium, Daly MJ, Chakravarti A, Nature 2009 461 802 808 10.1038/nature08490 19812673
21. Functional impact of global rare copy number variation in autism spectrum disorders. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, et al. Nature 2010 2010 466 7304 368 372 10.1038/nature09146
22. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, Fauchereau F, Nygren G, Rastam M, Gillberg IC, Anckarsater H, et al. Nat Genet 2007 39 25 27 10.1038/ng1933 17173049 (Pubitemid 46026497)
23. PTEN mutation in a family with Cowden syndrome and autism. Goffin A, Hoefsloot LH, Bosgoed E, Swillen A, Fryns JP, Am J Med Genet 2001 105 521 524 10.1002/ajmg.1477 11496368 (Pubitemid 32729819)
24. Association of INPP1, PIK3CG, and TSC2 gene variants with autistic disorder: implications for phosphatidylinositol signalling in autism. Serajee FJ, Nabi R, Zhong H, Mahbubul Huq AH, J Med Genet 2003 40 119 10.1136/jmg.40.11.e119 14627686
25. Genetics of autism: complex aetiology for a heterogeneous disorder. Folstein SE, Rosen-Sheidley B, Nat Rev Genet 2001 2 943 955 10.1038/35103559 11733747 (Pubitemid 33691091)
26. Screening of nine candidate genes for autism on chromosome 2q reveals rare nonsynonymous variants in the cAMP-GEFII gene. Bacchelli E, Blasi F, Biondolillo M, Lamb JA, Bonora E, Barnby G, Parr J, Beyer KS, Klauck SM, Poustka A, International Molecular Genetic Study of Autism Consortium (IMGSAC), et al. Mol Psychiatry 2003 8 916 924 10.1038/sj.mp.4001340 14593429 (Pubitemid 37421698)
27. MeCP2 involvement in the regulation of neuronal alpha-tubulin production. Abuhatzira L, Shemer R, Razin A, Hum Mol Genet 2009 18 1415 1423 10.1093/hmg/ddp048 19174478
28. Association of the homeobox transcription factor, ENGRAILED 2, 3, with autism spectrum disorder. Gharani N, Benayed R, Mancuso V, Brzustowicz LM, Millonig JH, Mol Psychiatry 2004 9 474 484 10.1038/sj.mp.4001498 15024396 (Pubitemid 38903503)
29. Candidate-gene screening and association analysis at the autism-susceptibility locus on chromosome 16p: evidence of association at GRIN2A and ABAT. Barnby G, Abbott A, Sykes N, Morris A, Weeks DE, Mott R, Lamb J, Bailey AJ, Monaco AP, Am J Hum Genet 2005 76 950 966 10.1086/430454 15830322 (Pubitemid 40705432)
30. Investigation of autism and GABA receptor subunit genes in multiple ethnic groups. Collins AL, Ma D, Whitehead PL, Martin ER, Wright HH, Abramson RK, Hussman JP, Haines JL, Cuccaro ML, Gilbert JR, Pericak-Vance MA, Neurogenetics 2006 7 167 174 10.1007/s10048-006-0045-1 16770606 (Pubitemid 44078294)
31. Genome-wide significance levels and weighted hypothesis testing. Roeder K, Wasserman L, Stat Sci 2009 24 398 413 10.1214/09-STS289 20711421
32. Sensor noise suppression. de Cheveigne A, Simon JZ, J Neurosci Methods 2008 168 195 202 10.1016/j.jneumeth.2007.09.012 17963844
33. Generating Linkage Disequilibrium Patterns in Data Simulations using genomeSIMLA. Edwards TL, Bush WS, Turner SD, Dudek SM, Torstenson ES, Schmidt M, Martin E, Ritchie MD, Lect Notes Comput Sci 2008 4973 24 35 full-text 19779634
34. The APL test: extension to general nuclear families and haplotypes and the examination of its robustness. Chung RH, Hauser ER, Martin ER, Hum Hered 2006 61 189 199 10.1159/000094774 16877866 (Pubitemid 44357216)
35. AGRE. http://www.agre.org/
36. Vineland Adaptive Behavior Scales. Sparrow SS, Balla D, Cicchetti D, MN: AGS 1984
37. Vineland Adaptive Behavior Scales. Sparrow SS, Cicchetti DV, Balla D, MN: AGS 2 2005
38. Population structure and eigenanalysis. Patterson N, Price AL, Reich D, PLoS Genet 2006 2 190 10.1371/journal.pgen.0020190 17194218 (Pubitemid 46045188)
39. The structure of haplotype blocks in the human genome. Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, et al. Science 2002 296 2225 2229 10.1126/science.1069424 12029063 (Pubitemid 34680308)
40. Truncated product method for combining P-values. Zaykin DV, Zhivotovsky LA, Westfall PH, Weir BS, Genet Epidemiol 2002 22 170 185 10.1002/gepi.0042 11788962 (Pubitemid 34081490)
41. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Huang da W, Sherman BT, Lempicki RA, Nat Protoc 2009 4 44 57 10.1038/nprot.2008.211 19131956
42. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA, Genome Biol 2003 4 3 10.1186/gb-2003-4-5-p3 12734009
43. DAVID Bioinformatics Resources 6.7. http://david.abcc.ncifcrf.gov/
44. Power of association and linkage tests when the disease alleles are unobserved. Tu IP, Whittemore AS, Am J Human Genetics 1999 64 641 649 10.1086/302253 (Pubitemid 129500548)
45. Galaxy. http://www.main.g2.bx.psu.edu/
46. Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. Andrews MR, Czvitkovich S, Dassie E, Vogelaar CF, Faissner A, Blits B, Gage FH, French-Constant C, Fawcett JW, J Neurosci 2009 29 5546 5557 10.1523/JNEUROSCI.0759-09.2009 19403822
47. More than just synaptic building blocks: scaffolding proteins of the post-synaptic density regulate dendritic patterning. Vessey JP, Karra D, J Neurochem 2007 102 324 332 10.1111/j.1471-4159.2007.04662.x 17596209 (Pubitemid 47000606)
48. Gene ontology: Tool for the unification of biology. the gene ontology consortium. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Nat Genet 2000 5 25 29 (Pubitemid 30257031)
49. Genetic analysis of complex diseases. Muller-Myhsok B, Abel L, Science 1997 275 1328 9 author reply 1329-30 9064791
50. Curses - winner's and otherwise - in genetic epidemiology. Kraft P, Epidemiology 2008 19 649 51 discussion 657-8 10.1097/EDE.0b013e318181b865 18703928
51. Searching for ways out of the autism maze: genetic, epigenetic and environmental clues. Persico AM, Bourgeron T, Trends Neurosci 2006 29 349 358 10.1016/j.tins.2006.05.010 16808981 (Pubitemid 44108247)
52. Neuroanatomic observations of the brain in autism: a review and future directions. Bauman ML, Kemper TL, Int J Dev Neurosci 2005 23 183 187 10.1016/j.ijdevneu.2004.09.006 15749244 (Pubitemid 40313551)
53. Hippocampus in autism: a Golgi analysis. Raymond GV, Bauman ML, Kemper TL, Acta Neuropathol 1996 91 117 119 10.1007/s004010050401 8773156
54. Dendritic anomalies in disorders associated with mental retardation. Kaufmann WE, Moser HW, Cereb Cortex 2000 10 981 991 10.1093/cercor/10.10.981 11007549
55. Dendritic cytoskeletal protein expression in mental retardation: an immunohistochemical study of the neocortex in Rett syndrome. Kaufmann WE, MacDonald SM, Altamura CR, Cereb Cortex 2000 10 992 1004 10.1093/cercor/10.10. 992 11007550
56. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Wegiel J, Kuchna I, Nowicki K, Imaki H, Wegiel J, Marchi E, Ma SY, Chauhan A, Chauhan V, Bobrowicz TW, et al. Acta Neuropathol 2010 119 755 770 10.1007/s00401-010-0655-4 20198484
57. Minicolumnar pathology in autism. Casanova MF, Buxhoeveden DP, Switala AE, Roy E, Neurology 2002 58 428 432 11839843 (Pubitemid 34150918)
58. Radial cytoarchitecture and patterns of cortical connectivity in autism. Casanova M, Trippe J, Philos Trans R Soc Lond B Biol Sci 2009 364 1433 1436 10.1098/rstb.2008.0331 19528027
59. The nature of brain dysfunction in autism: functional brain imaging studies. Minshew NJ, Keller TA, Curr Opin Neurol 2010 23 124 130 10.1097/WCO.0b013e32833782d4 20154614
60. Mammalian Pumilio 2 regulates dendrite morphogenesis and synaptic function. Vessey JP, Schoderboeck L, Gingl E, Luzi E, Riefler J, Di Leva F, Karra D, Thomas S, Kiebler MA, Macchi P, Proc Natl Acad Sci USA 2010 107 3222 3227 10.1073/pnas.0907128107 20133610
61. Chondroitin sulfate proteoglycans in neural development and plasticity. Maeda N, Fukazawa N, Ishii M, Front Biosci 2010 15 626 644 10.2741/3637 20036837
62. Receptor type protein tyrosine phosphatase zeta-pleiotrophin signaling controls endocytic trafficking of DNER that regulates neuritogenesis. Fukazawa N, Yokoyama S, Eiraku M, Kengaku M, Maeda N, Mol Cell Biol 2008 28 4494 4506 10.1128/MCB.00074-08 18474614 (Pubitemid 351977749)
63. A Drosophila homolog of the polyglutamine disease gene SCA2 is a dosage-sensitive regulator of actin filament formation. Satterfield TF, Jackson SM, Pallanck LJ, Genetics 2002 162 1687 1702 12524342 (Pubitemid 36114656)
64. Semaphorin 4D signaling requires the recruitment of phospholipase C gamma into the plexin-B1 receptor complex. Swiercz JM, Worzfeld T, Offermanns S, Mol Cell Biol 2009 29 6321 6334 10.1128/MCB.00103-09 19805522
65. The semaphorin 4D-plexin-B signalling complex regulates dendritic and axonal complexity in developing neurons via diverse pathways. Vodrazka P, Korostylev A, Hirschberg A, Swiercz JM, Worzfeld T, Deng S, Fazzari P, Tamagnone L, Offermanns S, Kuner R, Eur J Neurosci 2009 30 1193 1208 10.1111/j.1460-9568. 2009.06934.x 19788569
66. Cadherin-8 and N-cadherin differentially regulate pre- and postsynaptic development of the hippocampal mossy fiber pathway. Bekirov IH, Nagy V, Svoronos A, Huntley GW, Benson DL, Hippocampus 2008 18 349 363 10.1002/hipo.20395 18064706 (Pubitemid 351543932)
67. Gordon-Weeks PR, Neuronal Growth Cones Cambridge; New York: Cambridge University Press 2000
68. Bagnard D, Axon Growth and Guidance New York; Texas: Springer Science and Business Media; Landes Bioscience 2007
69. CAM-FGF receptor interactions: a model for axonal growth. Doherty P, Walsh FS, Mol Cell Neurosci 1996 8 99 111 10.1006/mcne.1996.0049 (Pubitemid 26386700)
70. Regulation of cell adhesion by protein-tyrosine phosphatases: II. Cell-cell adhesion. Sallee JL, Wittchen ES, Burridge K, J Biol Chem 2006 281 16189 16192 10.1074/jbc.R600003200 16497667
71. Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM, Neuron 1998 21 1093 1100 10.1016/S0896-6273(00)80626-1 9856464 (Pubitemid 29018078)
72. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. Noren NK, Liu BP, Burridge K, Kreft B, J Cell Biol 2000 150 567 580 10.1083/jcb.150.3.567 10931868 (Pubitemid 30641401)
73. A novel and evolutionarily conserved PtdIns(3,4,5)P3-binding domain is necessary for DOCK180 signalling. Cote JF, Motoyama AB, Bush JA, Vuori K, Nat Cell Biol 2005 7 797 807 10.1038/ncb1280 16025104 (Pubitemid 41079052)
74. Kalirin loss results in cortical morphological alterations. Xie Z, Cahill ME, Penzes P, Mol Cell Neurosci 2010 43 81 89 10.1016/j.mcn.2009.09.006 19800004
75. MEGAP impedes cell migration via regulating actin and microtubule dynamics and focal complex formation. Yang Y, Marcello M, Endris V, Saffrich R, Fischer R, Trendelenburg MF, Sprengel R, Rappold G, Exp Cell Res 2006 312 2379 2393 10.1016/j.yexcr.2006.04.001 16730001 (Pubitemid 43928953)
76. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Schwamborn JC, Puschel AW, Nat Neurosci 2004 7 923 929 10.1038/nn1295 15286792 (Pubitemid 39129500)
77. Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Liu C, Takahashi M, Li Y, Song S, Dillon TJ, Shinde U, Stork PJ, Mol Cell Biol 2008 28 7109 7125 10.1128/MCB.01060-08 18824540
78. Molecules and mechanisms involved in the generation and migration of cortical interneurons. Hernandez-Miranda LR, Parnavelas JG, Chiara F, ASN Neuro 2010 2 00031 10.1042/AN20090053 20360946
79. Cadherin-11 interacts with the FGF receptor and induces neurite outgrowth through associated downstream signalling. Boscher C, Mege RM, Cell Signal 2008 20 1061 1072 10.1016/j.cellsig.2008.01.008 18302981
80. A critical importance of polyamine site in NMDA receptors for neurite outgrowth and fasciculation at early stages of P19 neuronal differentiation. Georgiev D, Taniura H, Kambe Y, Takarada T, Yoneda Y, Exp Cell Res 2008 314 2603 2617 10.1016/j.yexcr.2008.06.009 18586028
81. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Williams EJ, Furness J, Walsh FS, Doherty P, Neuron 1994 13 583 594 10.1016/0896-6273(94)90027-2 7917292 (Pubitemid 24300164)
82. F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Falk J, Bonnon C, Girault JA, Faivre-Sarrailh C, Biol Cell 2002 94 327 334 10.1016/S0248-4900(02)00006-0 12500940 (Pubitemid 35402316)
83. Sema4D-plexin-B1 implicated in regulation of dendritic spine density through RhoA/ROCK pathway. Lin X, Ogiya M, Takahara M, Yamaguchi W, Furuyama T, Tanaka H, Tohyama M, Inagaki S, Neurosci Lett 2007 428 1 6 10.1016/j.neulet. 2007.09.045 17950529 (Pubitemid 47633811)
84. Control of neuronal growth cone navigation by asymmetric inositol 1,4,5-trisphosphate signals. Akiyama H, Matsu-ura T, Mikoshiba K, Kamiguchi H, Sci Signal 2009 2 a34 10.1126/scisignal.2000196 19602704
85. Src-dependent tyrosine phosphorylation at the tips of growth cone filopodia promotes extension. Robles E, Woo S, Gomez TM, J Neurosci 2005 25 7669 7681 10.1523/JNEUROSCI.2680-05.2005 16107653 (Pubitemid 41170623)
86. Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nishiyama M, Hoshino A, Tsai L, Henley JR, Goshima Y, Tessier-Lavigne M, Poo MM, Hong K, Nature 2003 423 990 995 10.1038/nature01751 12827203 (Pubitemid 36806914)
87. Phosphoinositides and Rho proteins spatially regulate actin polymerization to initiate and maintain directed movement in a one-dimensional model of a motile cell. Dawes AT, Edelstein-Keshet L, Biophys J 2007 92 744 768 10.1529/biophysj.106.090514 17098793 (Pubitemid 46203207)
88. The role of the Rho GTPases in neuronal development. Govek EE, Newey SE, Van Aelst L, Genes Dev 2005 19 1 49 10.1101/gad.1256405 15630019 (Pubitemid 40095815)
89. Development and regulation of dendritic spine synapses. Calabrese B, Wilson MS, Halpain S, Physiology (Bethesda) 2006 21 38 47 16443821 (Pubitemid 43752516)