Variants in the 1q21 risk region are associated with a visual endophenotype of autism and schizophrenia

Genes, Brain and Behavior

Volumn 13, Issue 2, 2014, Pages 144-151

  Goodbourn, P T ^a,b   Bosten, J M ^a   Bargary, G ^a,c   Hogg, R E ^a,d   Lawrance Owen, A J ^a   Mollon, J D ^a  

^a UK   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

^c CITY UNIVERSITY   (United Kingdom)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Autism; Endophenotype; Frequency doubling; Genome wide association study; Schizophrenia; Visual sensitivity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLIGIN;

5' UNTRANSLATED REGION; ADOLESCENT; ADULT; ALLELE; ARTICLE; AUTISM; CHROMOSOME 1Q; CONTROLLED STUDY; ENDOPHENOTYPE; FEMALE; GENE LOCUS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RISK FACTOR; SCHIZOPHRENIA; SENSITIVITY ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; VISION TEST; YOUNG ADULT;

AUTISM; ENDOPHENOTYPE; FREQUENCY DOUBLING; GENOME-WIDE ASSOCIATION STUDY; SCHIZOPHRENIA; VISUAL SENSITIVITY;

ADOLESCENT; ADULT; ALLELES; AUTISTIC DISORDER; CARRIER PROTEINS; CHROMOSOMES, HUMAN, PAIR 21; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SCHIZOPHRENIA; VISUAL ACUITY;

EID: 84892996170     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12096     Document Type: Article

References (66)

1. Abecasis, G.R., Altshuler, D., Auton, A., Brooks, L.D., Durbin, R.M., Gibbs, R.A., Hurles, M.E. & McVean, G.A. (2010) A map of human genome variation from population-scale sequencing. Nature 467, 1061-1073.
2. Bourgeron, T. (2009) A synaptic trek to autism. Curr Opin Neurobiol 19, 231-234.
3. Braff, D.L. & Freedman, R. (2002) Endophenotypes in studies of the genetics of schizophrenia. In Davis, K.L., Charney, D., Coyle, J.T. & Nemeroff, C. (eds), Neuropsychopharmacology: The Fifth Generation of Progress. Lippincott Williams & Wilkins, Philadelphia, PA, pp. 703-716.
4. Brainard, D.H. (1997) The psychophysics toolbox. Spat Vis 10, 433-436.
5. Brzustowicz, L.M., Hodgkinson, K.A., Chow, E.W., Honer, W.G. & Bassett, A.S. (2000) Location of a major susceptibility locus for familial schizophrenia on chromosome 1q21-q22. Science 288, 678-682.
6. Butler, P.D., Zemon, V., Schechter, I., Saperstein, A.M., Hoptman, M.J., Lim, K.O., Revheim, N., Silipo, G. & Javitt, D.C. (2005) Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch Gen Psychiatry 62, 495-504.
7. Butler, P.D., Silverstein, S.M. & Dakin, S.C. (2008) Visual perception and its impairment in schizophrenia. Biol Psychiatry 64, 40-47.
8. Casey, J.P., Magalhaes, T., Conroy, J.M. et al. (2012) A novel approach of homozygous haplotype sharing identifies candidate genes in autism spectrum disorder. Hum Genet 131, 565-579.
9. Chen, Y. & Li, M. (2005) Interactions between CAP70 and actinfilin are important for integrity of actin cytoskeleton structures in neurons. Neuropharmacology 49, 1026-1041.
10. Craig, A.M. & Kang, Y. (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17, 43-52.
11. Dakin, S. & Frith, U. (2005) Vagaries of visual perception in autism. Neuron 48, 497-507.
12. Devlin, B. & Roeder, K. (1999) Genomic control for association studies. Biometrics 55, 997-1004.
13. Fanning, A.S. & Anderson, J.M. (1999) PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J Clin Invest 103, 767-772.
14. Feyder, M., Karlsson, R.M., Mathur, P. et al. (2010) Association of mouse Dlg4 (PSD-95) gene deletion and human DLG4 gene variation with phenotypes relevant to autism spectrum disorders and Williams' syndrome. Am J Psychiatry 167, 1508-1517.
15. Goodbourn, P.T., Bosten, J.M., Hogg, R.E., Bargary, G., Lawrance-Owen, A.J. & Mollon, J.D. (2012) Do different 'magnocellular tasks' probe the same neural substrate? Proc Biol Sci 279, 4263-4271.
16. Gottesman, I.I. & Gould, T.D. (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160, 636-645.
17. Gracitelli, C.P.B., Vaz de Lima, F.B., Bressan, R.A. & Paranhos, A. Jr. (2013) Visual field loss in schizophrenia: evaluation of magnocellular pathway dysfunction in schizophrenic patients and their parents. Clin Ophthalmol 7, 1015-1021.
18. Greenaway, R., Davis, G. & Plaisted-Grant, K. (2013) Marked selective impairment in autism on an index of magnocellular function. Neuropsychologia 51, 592-600.
19. Greenwood, T.A., Lazzeroni, L.C., Murray, S.S. et al. (2011) Analysis of 94 candidate genes and 12 endophenotypes for schizophrenia from the Consortium on the Genetics of Schizophrenia. Am J Psychiatry 168, 930-946.
20. Greenwood, T.A., Light, G.A., Swerdlow, N.R., Radant, A.D. & Braff, D.L. (2012) Association analysis of 94 candidate genes and schizophrenia-related endophenotypes. PLoS One 7, e29630.
21. Greenwood, T.A., Swerdlow, N.R., Gur, R.E. et al. (2013) Genome-wide linkage analyses of 12 endophenotypes for schizophrenia from the Consortium on the Genetics of Schizophrenia. Am J Psychiatry 170, 521-532.
22. Grinter, E.J., Maybery, M.T. & Badcock, D.R. (2010) Vision in developmental disorders: is there a dorsal stream deficit? Brain Res Bull 82, 147-160.
23. Gurling, H.M., Kalsi, G., Brynjolfson, J., Sigmundsson, T., Sherrington, R., Mankoo, B.S., Read, T., Murphy, P., Blaveri, E., McQuillin, A., Petursson, H. & Curtis, D. (2001) Genomewide genetic linkage analysis confirms the presence of susceptibility loci for schizophrenia, on chromosomes 1q32.2, 5q33.2, and 8p21-22 and provides support for linkage to schizophrenia, on chromosomes 11q23.3-24 and 20q12.1-11.23. Am J Hum Genet 68, 661-673.
24. Hogg, R.E., Dimitrov, P.N., Dirani, M., Varsamidis, M., Chamberlain, M.D., Baird, P.N., Guymer, R.N. & Vingrys, A.J. (2009) Gene-environment interactions and aging visual function: a classical twin study. Ophthalmology 116, 263-269.
25. Howie, B.N., Donnelly, P. & Marchini, J. (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 5, e1000529.
26. Howie, B., Marchini, J. & Stephens, M. (2011) Genotype imputation with thousands of genomes. G3 (Bethesda) 1, 457-470.
27. Huang, Y.Z., Won, S., Ali, D.W., Wang, Q., Tanowitz, M., Du, Q.S., Pelkey, K.A., Yang, D.J., Xiong, W.C., Salter, M.W. & Mei, L. (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26, 443-455.
28. Hwu, H.G., Liu, C.M., Fann, C.S., Ou-Yang, W.C. & Lee, S.F. (2003) Linkage of schizophrenia with chromosome 1q loci in Taiwanese families. Mol Psychiatry 8, 445-452.
29. International HapMap 3 Consortium (2010) Integrating common and rare genetic variation in diverse human populations. Nature 467, 52-58.
30. International HapMap Consortium (2005) A haplotype map of the human genome. Nature 437, 1299-1320.
31. International HapMap Consortium (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861.
32. International Schizophrenia Consortium (2008) Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455, 237-241.
33. Javitt, D.C. (2003) Peeling the onion: NMDA dysfunction as a unifying model in schizophrenia. Behav Brain Sci 26, 93-94.
34. Kéri, S. & Benedek, G. (2007) Visual contrast sensitivity alterations in inferred magnocellular pathways and anomalous perceptual experiences in people at high-risk for psychosis. Vis Neurosci 24, 183-189.
35. Kéri, S., Kelemen, O., Benedek, G. & Janka, Z. (2004) Vernier threshold in patients with schizophrenia and in their unaffected siblings. Neuropsychology 18, 537-542.
36. Kéri, S., Kelemen, O., Janka, Z. & Benedek, G. (2005a) Visual-perceptual dysfunctions are possible endophenotypes of schizophrenia: evidence from the psychophysical investigation of magnocellular and parvocellular pathways. Neuropsychology 19, 649-656.
37. Kéri, S., Kiss, I., Kelemen, O., Benedek, G. & Janka, Z. (2005b) Anomalous visual experiences, negative symptoms, perceptual organization and the magnocellular pathway in schizophrenia: a shared construct? Psychol Med 35, 1445-1455.
38. King-Smith, P.E., Grigsby, S.S., Vingrys, A.J., Benes, S.C. & Supowit, A. (1994) Efficient and unbiased modifications of the QUEST threshold method: theory, simulations, experimental evaluation and practical implementation. Vision Res 34, 885-912.
39. Kiss, I., Fábián, A., Benedek, G. & Kéri, S. (2010) When doors of perception open: visual contrast sensitivity in never-medicated, first-episode schizophrenia. J Abnorm Psychol 119, 586-593.
40. Kwon, Y.H., Nelson, S.B., Toth, L.J. & Sur, M. (1992) Effect of stimulus contrast and size on NMDA receptor activity in cat lateral geniculate nucleus. J Neurophysiol 68, 182-196.
41. Lawrance-Owen, A.J., Bargary, G., Bosten, J.M., Goodbourn, P.T., Hogg, R.E. & Mollon, J.D. (2013) Genetic association suggests that SMOC1 mediates between prenatal sex hormones and digit ratio. Hum Genet 132, 415-421.
42. Levinson, D.F., Duan, J., Oh, S. et al. (2011) Copy number variants in schizophrenia: confirmation of five previous findings and new evidence for 3q29 microdeletions and VIPR2 duplications. Am J Psychiatry 168, 302-316.
43. Levinson, D.F., Shi, J., Wang, K. et al. (2012) Genome-wide association study of multiplex schizophrenia pedigrees. Am J Psychiatry 169, 963-973.
44. Lohmueller, K.E., Pearce, C.L., Pike, M., Lander, E.S. & Hirschhorn, J.N. (2003) Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat Genet 33, 177-182.
45. Maddess, T. (2011) Frequency-doubling technology and parasol cells. Invest Ophthalmol Vis Sci 52, 3759.
46. McCleery, J.P., Allman, E., Carver, L.J. & Dobkins, K.R. (2007) Abnormal magnocellular pathway visual processing in infants at risk for autism. Biol Psychiatry 62, 1007-1014.
47. Mefford, H.C., Sharp, A.J., Baker, C. et al. (2008) Recurrent rearrangements of chromosome 1q21.1 and variable pediatric phenotypes. N Engl J Med 359, 1685-1699.
48. Meyer, G., Varoqueaux, F., Neeb, A., Oschlies, M. & Brose, N. (2004) The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47, 724-733.
49. Ni, X., Valente, J., Azevedo, M.H., Pato, M.T., Pato, C.N. & Kennedy, J.L. (2007) Connexin 50 gene on human chromosome 1q21 is associated with schizophrenia in matched case control and family-based studies. J Med Genet 44, 532-536.
50. Patterson, N., Price, A.L. & Reich, D. (2006) Population structure and eigenanalysis. PLoS Genet 2, e190.
51. Pelli, D.G. (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10, 437-442.
52. Pemberton, T.J., Wang, C., Li, J.Z. & Rosenberg, N.A. (2010) Inference of unexpected genetic relatedness among individuals in HapMap Phase III. Am J Hum Genet 87, 457-464.
53. Pinto, D., Pagnamenta, A.T., Klei, L. et al. (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466, 368-372.
54. Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. & Reich, D. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38, 904-909.
55. Prigge, J.R. & Schmidt, E.E. (2006) Interaction of protein inhibitor of activated STAT (PIAS) proteins with the TATA-binding protein, TBP. J Biol Chem 281, 12260-12269.
56. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J. & Sham, P.C. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81, 559-575.
57. Rosenbloom, K.R., Sloan, C.A., Malladi, V.S. et al. (2013) ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res 41, D56-D63.
58. Rosli, Y., Bedford, S. & Maddess, T. (2009) Low spatial-frequency channels and the spatial frequency doubling illusion. Invest Ophthalmol Vis Sci 50, 1956-1963.
59. Sanders, S.J., Ercan-Sencicek, A.G., Hus, V. et al. (2011) Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron 70, 863-885.
60. Shaw, S.H., Kelly, M., Smith, A.B., Shields, G., Hopkins, P.J., Loftus, J., Laval, S.H., Vita, A., De Hert, M., Cardon, L.R., Crow, T.J., Sherrington, R. & DeLisi, L.E. (1998) A genome-wide search for schizophrenia susceptibility genes. Am J Med Genet 81, 364-376.
61. Simmons, D.R., Robertson, A.E., McKay, L.S., Toal, E., McAleer, P. & Pollick, F.E. (2009) Vision in autism spectrum disorders. Vision Res 49, 2705-2739.
62. Stefansson, H., Rujescu, D., Cichon, S. et al. (2008) Large recurrent microdeletions associated with schizophrenia. Nature 455, 232-236.
63. Sudhof, T.C. (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911.
64. Szatmari, P., Paterson, A.D., Zwaigenbaum, L. et al. (2007) Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39, 319-328.
65. Watson, A.B. & Pelli, D.G. (1983) QUEST: a Bayesian adaptive psychometric method. Percept Psychophys 33, 113-120.
66. Zheng, Y., Wang, X., Gu, N., Feng, G., Zou, F., Qin, W., Zhang, J., Lin, W., Tao, R., Qian, X. & He, L. (2006) A two-stage linkage analysis of Chinese schizophrenia pedigrees in 10 target chromosomes. Biochem Biophys Res Commun 342, 1049-1057.