A genome-wide association study identifies multiple loci associated with mathematics ability and disability

Genes, Brain and Behavior

Volumn 9, Issue 2, 2010, Pages 234-247

  Docherty, S J ^a   Davis, O S P ^a   Kovas, Y ^a   Meaburn, E L ^a   Dale, P S ^b   Petrill, S A ^c   Schalkwyk, L C ^a   Plomin, R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Allelic association; Cognitive traits; DNA pooling; Mathematical ability; Quantitative trait; SNP microarrays

Indexed keywords

ARTICLE; CORRELATION ANALYSIS; GENE FREQUENCY; GENE IDENTIFICATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SCREENING; GENETIC VARIABILITY; GENOMICS; GENOTYPE; HUMAN; LEARNING DISORDER; MAJOR CLINICAL STUDY; MATHEMATICS; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; TWINS;

CHILD; CHROMOSOME MAPPING; CURRICULUM; DNA; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; INTERNET; LEARNING; LEARNING DISORDERS; LIKELIHOOD FUNCTIONS; MATHEMATICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 77949416390     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2009.00553.x     Document Type: Article

References (73)

1. Alarcón, M., DeFries, J.C., Light, J.G. & Pennington, B.F. (1997) A twin study of mathematics disability. J Learn Disabil 30, 617-623.
2. Alarcón, M., Knopik, V.S. & DeFries, J.C. (2000) Covariation of mathematics achievement and general cognitive ability in twins. J Sch Psychol 38, 63-77.
3. American Psychiatric Association. (1994) Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association, Washington, DC.
4. Balding, D.J. (2006) A tutorial on statistical methods for population association studies. Nat Rev Genet 7, 781-791.
5. Barratt, B.J., Payne, F., Rance, H.E., Nutland, S., Todd, J.A. & Clayton, D.G. (2002) Identification of the sources of error in allele frequency estimations from pooled DNA indicates an optimal experimental design. Ann Hum Genet 66, 393-405.
6. Bates, D. & Sarkar, D. (2006) lme4: Linear Mixed-Effects Models Using S4 Classes. http://CRAN R-project org, R package version 0 9975-1.
7. Bonora, E., Lamb, J.A., Barnby, G. et al. (2005) Mutation screening and association analysis of six candidate genes for autism on chromosome 7q. Eur J Hum Genet 13, 198-207.
8. Bortolotto, Z.A., Clarke, V.R.J., Delany, C.M., Parry, M.C., Smolders, I., Vignes, M., Ho, K.H., Miu, P., Brinton, B.T., Fantaske, R., Ogden, A., Gates, M., Ornstein, P.L., Lodge, D., Bleakman, D. & Collingridge, G.L. (1999) Kainate receptors are involved in synaptic plasticity. Nature 402, 297-301.
9. Butcher, L.M., Meaburn, E., Liu, L., Hill, L., Al-Chalabi, A., Plomin, R., Schalkwyk, L. & Craig, I.W. (2004) Genotyping pooled DNA on microarrays: a systematic genome screen of thousands of SNPs in large samples to detect QTLs for complex traits. Behav Genet 34, 549-555.
10. Butcher, L.M., Meaburn, E., Dale, P.S., Sham, P., Schalkwyk, L.C., Craig, I.W. & Plomin, R. (2005a) Association analysis of mild mental impairment using DNA pooling to screen 432 brain-expressed single-nucleotide polymorphisms. Mol Psychiatry 10, 384-392.
11. Butcher, L.M., Meaburn, E., Knight, J., Sham, P., Schalkwyk, L.C., Craig, I.W. & Plomin, R. (2005b) SNPs, microarrays, and pooled DNA: identification of four loci associated with mild mental impairment in a sample of 6000 children. Hum Mol Genet 14, 1315-1325.
12. Butcher, L.M., Davis, O.S.P., Craig, I.W. & Plomin, R. (2008) Genome-wide quantitative trait locus association scan of general cognitive ability using pooled DNA and 500K single nucleotide polymorphism microarrays. Genes Brain Behav 7, 435-446.
13. Chakraborti, S., Mandal, M., Das, S., Mandal, A. & Chakraborti, T. (2003) Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253, 269-285.
14. Chiang, H.M. & Lin, Y.H. (2007) Mathematical ability of students with Asperger syndrome and high-functioning autism: a review of literature. Autism 11, 547-556.
15. Craig, D.W., Huentelman, M.J., Hu-Lince, D., Zismann, V.L., Kruer, M.C., Lee, A.M., Puffenberger, E.G., Pearson, J.M. & Stephan, D.A. (2005) Identification of disease causing loci using an array-based genotyping approach on pooled DNA. BMC Genomics 6, 138.
16. Crnokrak, P. & Roff, D.A. (1995) Dominance variance: associations with selection and fitness. Heredity 75, 530-540.
17. Davis, O.S.P., Plomin, R. & Schalkwyk, L.C. (2009) The SNPMaP package for R: a framework for genome-wide association using DNA pooling on microarrays. Bioinformatics 25, 281-283.
18. Docherty, S.J., Butcher, L.M., Schalkwyk, L. & Plomin, R. (2007) Applicability of DNA pools on 500K SNP microarrays for cost-effective initial screens in genomewide association studies. BMC Genomics 8, 214.
19. Donnelly, P. (2008) Progress and challenges in genome-wide association studies in humans. Nature 456, 728-731.
20. Freeman, B., Smith, N., Curtis, C., Huckett, L., Mill, J. & Craig, I.W. (2003) DNA from buccal swabs recruited by mail: evaluation of storage effects on long-term stability and suitability for multiplex polymerase chain reaction genotyping. Behav Genet 33, 67-72.
21. Gratacòs M., Costas J., de Cid R. et al. The Psychiatric Genetics Network Group. (2008) Identification of new putative susceptibility genes for several psychiatric disorders by association analysis of regulatory and non-synonymous SNPs of 306 genes involved in neurotransmission and neurodevelopment. Am J Med Genet B: Neuropsychiatr Genet 150B, 808-816.
22. Gross-Tsur, V., Manor, O. & Shalev, R.S. (1996) Developmental dyscalculia: prevalence and demographic features. Dev Med Child Neurol 38, 25-33.
23. Grumet M. (1997) Nr-CAM: a cell adhesion molecule with ligand and receptor functions. Cell Tissue Res 290, 423-428.
24. Harlaar, N., Spinath, F.M., Dale, P. & Plomin, R. (2005) Genetic influences on word recognition abilities and disabilities: a study of 7-year-old twins. J Child Psychol Psychiatry 46, 373-384.
25. Haworth, C.M., Harlaar, N., Kovas, Y., Davis, O.S., Oliver, B.R., Hayiou-Thomas, M.E., Frances, J., Busfield, P., McMillan, A., Dale, P.S. & Plomin, R. (2007) Internet cognitive testing of large samples needed in genetic research. Twin Res Hum Genet 10, 554-563.
26. Hoffman, K.B. (1998) The relationship between adhesion molecules and neuronal plasticity. Cell Mol Neurobiol 18, 461-475.
27. Hoge, R.D. & Coladarci, T. (1989) Teacher-based judgments of academic achievement: a review of literature. Rev Educ Res 59, 297-313.
28. Hornef, N., Olbrich, H., Horvath, J., Zariwala, M.A., Fliegauf, M., Loges, N.T., Wildhaber, J., Noone, P.G., Kennedy, M., Antonarakis, S.E., Blouin, J.L., Bartoloni, L., Nusslein, T., Ahrens, P., Griese, M., Kuhl, H., Sudbrak, R., Knowles, M.R., Reinhardt, R. & Omran, H. (2006) DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am J Respir Crit Care Med 174, 120-126.
29. Huettner, J.E. (2003) Kainate receptors and synaptic transmission. Prog Neurobiol 70, 387-407.
30. Husén, T. (1959) Psychological Twin Research. Almqvist & Wiksell, Stockholm.
31. Hutcheson, H.B., Olson, L.M., Bradford, Y., Folstein, S.E., Santangelo, S.L., Sutcliffe, J.S. & Haines, J.L. (2004) Examination of NRCAM, LRRN3, KIAA0716, and LAMB1 as autism candidate genes. BMC Med Genet 5, 12.
32. Ibanez-Tallon, I., Pagenstecher, A., Fliegauf, M., Olbrich, H., Kispert, A., Ketelsen, U.P., North, A., Heintz, N. & Omran, H. (2004) Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet 13, 2133-2141.
33. Jawaid, A., Bader, J.S., Purcell, S., Cherny, S.S. & Sham, P.C. (2002) Optimal selection strategies for QTL mapping using pooled DNA samples. Eur JHum Genet 10, 125-132.
34. Kirov, G., Nikolov, I., Georgieva, L., Moskvina, V., Owen, M.J. & O'Donovan, M.C. (2006) Pooled DNA genotyping on Affymetrix SNP genotyping arrays. BMC Genomics 7, 27.
35. Kovas, Y., Harlaar, N., Petrill, S.A. & Plomin, R. (2005) 'Generalist genes' and mathematics in 7-year-old twins. Intelligence 33, 473-489.
36. Kovas, Y., Haworth, C.M.A., Dale, P.S. & Plomin, R. (2007a) The genetic and environmental origins of learning abilities and disabilities in the early school years. Monogr Soc Res Child Dev 72, 1-144.
37. Kovas, Y., Haworth, C.M.A., Petrill, S.A. & Plomin, R. (2007b) Mathematical ability of 10-year-old boys and girls: Genetic and environmental etiology of normal and low performance. J Learn Disabil 40, 554-567.
38. Kovas, Y., Petrill, S.A. & Plomin, R. (2007c) The origins of diverse domains of mathematics: generalist genes but specialist environments. J Educ Psychol 99, 128-139.
39. Kraft, P. (2008) Curses-winner's and otherwise-in genetic epidemiology. Epidemiology 19, 649-651.
40. Law J., Nye C., Harkness A., Harris F. & Boyle J. (1998) Screening for speech and language delay: a systematic review of the literature. Health Technol Assess 2, 1-184.
41. Light, J.G., DeFries, J.C. & Olson, R.K. (1998) Multivariate behavioral genetic analysis of achievement and cognitive measures in reading-disabled and control twin pairs. Hum Biol 70, 215-237.
42. Liu, Q.R., Drgon, T., Walther, D., Johnson, C., Poleskaya, O., Hess, J. & Uhl, G.R. (2005) Pooled association genome scanning: validation and use to identify addiction vulnerability loci in two samples. Proc Natl Acad Sci U S A 102, 11864-11869.
43. Loehlin, J.C. & Nichols, J. (1976) Heredity, Environment and Personality . University of Texas, Austin.
44. Markowitz, E.M., Willemsen, G., Trumbetta, S.L., van Beijsterveldt, T.C.E.M. & Boomsma, D.I. (2005) The etiology of mathematical and reading (dis)ability covariation in a sample of Dutch twins. Twin Res Hum Genet 8, 585-593.
45. Marui, T., Funatogawa, I., Koishi, S., Yamamoto, K., Matsumoto, H., Hashimoto, O., Nanba, E., Nishida, H., Sugiyama, T. & Kasai, K. (2008) Association of the neuronal cell adhesion molecule (NRCAM) gene variants with autism. Int J Neuropsychopharmacol 12, 1-10.
46. Mazzocco, M.M.M. & Myers, G.F. (2003) Complexities in identifying and defining mathematics learning disability in the primary school age years. Ann Dyslexia 53, 218-253.
47. McCarthy, M.I., Abecasis, G.R., Cardon, L.R., Goldstein, D.B., Little, J., Ioannidis, J.P.A. & Hirschhorn, J.N. (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9, 356-369.
48. McGrath, L.M., Smith, S.D. & Pennington, B.F. (2006) Breakthroughs in the search for dyslexia candidate genes. Trends Mol Med 12, 333-341.
49. Meaburn, E., Butcher, L.M., Liu, L., Fernandes, C., Hansen, V., Al Chalabi, A., Plomin, R., Craig, I. & Schalkwyk, L.C. (2005) Genotyping DNA pools on microarrays: tackling the QTL problem of large samples and large numbers of SNPs. BMC Genomics 6, 52-60.
50. Meaburn, E., Butcher, L.M., Schalkwyk, L.C. & Plomin, R. (2006) Genotyping pooled DNA using 100K SNP microarrays: A step towards genomewide association scans. Nucleic Acids Res 34, e28.
51. Meaburn, E.L., Harlaar, N., Craig, I.W., Schalkwyk, L.C. & Plomin, R. (2007) Quantitative trait locus association scan of early reading disability and ability using pooled DNA and 100K SNP microarrays in a sample of 5760 children. Mol Psychiatry 13, 729-740.
52. Newton-Cheh, C. & Hirschhorn, J.N. (2005) Genetic association studies of complex traits: design and analysis issues. Mutat Res 573, 54-69.
53. nferNelson. (2001) Maths 5-14 Series. nferNelson Publishing Company Ltd, London.
54. Oliver, B., Harlaar, N., Hayiou-Thomas, M.E., Kovas, Y., Walker, S.O., Petrill, S.A., Spinath, F.M. & Plomin, R. (2004) A twin study of teacher-reported mathematics performance and low performance in 7-year-olds. J Educ Psychol 96, 504-517.
55. Oliver, B. & Plomin, R. (2007) Twins Early Development Study (TEDS): a multivariate, longitudinal genetic investigation of language, cognition and behaviour problems from childhood through adolescence. Twin Res Hum Genet 10, 96-105.
56. Paracchini, S., Scerri, T. & Monaco, A.P. (2007) The genetic lexicon of dyslexia. Annu Rev Genomics Hum Genet 8, 57-79.
57. Pearson, J.V., Huentelman, M.J., Halperin, R.F. et al. (2007) Identification of the genetic basis for complex disorders by use of pooling-based genomewide single-nucleotide-polymorphism association studies. Am J Hum Genet 80, 126-139.
58. Plomin, R., Haworth, C.M.A. & Davis, O.S.P. (2009) Common disorders are quantitative traits. Nat Rev Genet 10, 872-878.
59. Plomin, R. & Kovas, Y. (2005) Generalist genes and learning disabilities. Psychol Bull 131, 592-617.
60. Plomin, R., DeFries, J.C., McClearn, G.E. & McGuffin, P. (2008) Behavioral Genetics, 5th edn. Worth Publishers, New York.
61. Purcell, S., Cherny, S.S. & Sham, P.C. (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19, 149-150.
62. QCA. (2001) National Curriculum in Action, Mathematics Level Descriptions. Accessed 01/09/2006, at http://www.ncaction.org.uk/subjects/ maths/levels.htm.
63. R Development Core Team. (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/.
64. Seshadri, S., DeStefano, A., Au, R., Massaro, J., Beiser, A., Kelly-Hayes, M., Kase, C., D'Agostino, R., DeCarli, C., Atwood, L. & Wolf, P. (2007) Genetic correlates of brain aging on MRI and cognitive test measures: a genome-wide association and linkage analysis in the Framingham study. BMC Med Genet 8, S15.
65. Skol, A.D., Scott, L.J., Abecasis, G.R. & Boehnke, M. (2006) Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies. Nat Genet 38, 209-213.
66. Smith, A. (2004) Making Mathematics Count: The Report of Professor Adrian Smith's Inquiry into Post-14 Mathematics Education. Department for Education and Skills.
67. Steer, S., Abkevich, V., Gutin, A. et al. (2007) Genomic DNA pooling for whole-genome association scans in complex disease: empirical demonstration of efficacy in rheumatoid arthritis. Genes Immun 8, 57-68.
68. The International HapMap Consortium. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861.
69. Thompson, L.A., Detterman, D.K. & Plomin, R. (1991) Associations between cognitive abilities and scholastic achievement: genetic overlap but environmental differences. Psych Sci 2, 158-165.
70. Trouton, A., Spinath, F.M. & Plomin, R. (2002) Twins Early Development Study (TEDS): a multivariate, longitudinal genetic investigation of language, cognition and behaviour problems in childhood. Twin Research 5, 444-448.
71. Wadsworth, S.J., DeFries, J.C., Fulker, D.W. & Plomin, R. (1995) Covariation among measures of cognitive ability and academic achievement in the Colorado Adoption Project: sibling analysis. Person Individ Diff 18, 63-73.
72. Wellcome Trust Case Control Consortium. (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447, 661-678.
73. Woo, T.U., Shrestha, K., Amstrong, C., Minns, M.M., Walsh, J.P. & Benes, F.M. (2007) Differential alterations of kainate receptor subunits in inhibitory interneurons in the anterior cingulate cortex in schizophrenia and bipolar disorder. Schizophr Res 96, 46-61.