Evidence for association of cell adhesion molecules pathway and NLGN1 polymorphisms with schizophrenia in Chinese Han population

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Zhang, Zhengrong ^a,b   Yu, Hao ^c   Jiang, Sisi ^a,b   Liao, Jinmin ^a,b   Lu, Tianlan ^a,b   Wang, Lifang ^a,b   Zhang, Dai ^a,b,c   Yue, Weihua ^a,b  

^a PEKING UNIVERSITY SIXTH HOSPITAL   (China)

^b PEKING UNIVERSITY   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; HLA A ANTIGEN; HLA C ANTIGEN; HLA DPB1 ANTIGEN; HLA DRB1 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 3; NEUROLIGIN 1; MESSENGER RNA; NERVE CELL ADHESION MOLECULE;

ADULT; ARTICLE; CD276 GENE; CLDN1 GENE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HAN CHINESE; HLA A GENE; HLA C GENE; HLA DOB GENE; HLA DPB1 GENE; HLA DQA2 GENE; HLA DRB1 GENE; HUMAN; HUMAN TISSUE; ICAM3 GENE; MAJOR CLINICAL STUDY; MALE; MPZ GENE; NEUROLIGIN 1 GENE; NRCAM GENE; REPLICATION STUDY; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM; ASIAN CONTINENTAL ANCESTRY GROUP; CASE CONTROL STUDY; CHINA; CHROMOSOMAL MAPPING; GENE EXPRESSION PROFILING; GENE LINKAGE DISEQUILIBRIUM; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPE; METABOLISM; QUANTITATIVE TRAIT LOCUS; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; ASIAN CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; CHINA; CHROMOSOME MAPPING; FEMALE; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RNA, MESSENGER; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84956692077     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144719     Document Type: Article

References (58)

1. Andreasen NC. Symptoms, signs, and diagnosis of schizophrenia. Lancet. 1995; 346(8973):477-81. PMID: 7637483.
2. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature. 2010; 468(7321):203-12. doi: 10.1038/nature09563 PMID: 21068828.
3. Sullivan PF, Kendler KS, Neale MC. Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Archives of general psychiatry. 2003; 60(12):1187-92. doi: 10.1001/archpsyc.60.12. 1187 PMID: 14662550.
4. Singh S, Kumar A, Agarwal S, Phadke SR, Jaiswal Y. Genetic insight of schizophrenia: past and future perspectives. Gene. 2014; 535(2):97-100. doi: 10.1016/j.gene.2013.09.110 PMID: 24140491.
5. Giusti-Rodriguez P, Sullivan PF. The genomics of schizophrenia: update and implications. The Journal of clinical investigation. 2013; 123(11):4557-63. doi: 10.1172/JCI66031 PMID: 24177465; PubMed Central PMCID: PMC3809776.
6. Mowry BJ, Gratten J. The emerging spectrum of allelic variation in schizophrenia: current evidence and strategies for the identification and functional characterization of common and rare variants. Molecular psychiatry. 2013; 18(1):38-52. doi: 10.1038/mp.2012.34 PMID: 22547114.
7. Schizophrenia Working Group of the Psychiatric Genomics C. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014; 511(7510):421-7. doi: 10.1038/nature13595 PMID: 25056061; PubMed Central PMCID: PMC4112379.
8. Aberg KA, Liu Y, Bukszar J, McClay JL, Khachane AN, Andreassen OA, et al. A comprehensive familybased replication study of schizophrenia genes. JAMA psychiatry. 2013; 70(6):573-81. doi: 10.1001/jamapsychiatry.2013.288 PMID: 23894747.
9. O'Donovan MC, Craddock N, Norton N, Williams H, Peirce T, Moskvina V, et al. Identification of loci associated with schizophrenia by genome-wide association and follow-up. Nature genetics. 2008; 40 (9):1053-5. doi: 10.1038/ng.201 PMID: 18677311.
10. Ripke S, O'Dushlaine C, Chambert K, Moran JL, Kahler AK, Akterin S, et al. Genome-wide association analysis identifies 13 new risk loci for schizophrenia. Nature genetics. 2013; 45(10):1150-9. doi: 10. 1038/ng.2742 PMID: 23974872; PubMed Central PMCID: PMC3827979.
11. Wang K, Li M, Hakonarson H. Analysing biological pathways in genome-wide association studies. Nature reviews Genetics. 2010; 11(12):843-54. doi: 10.1038/nrg2884 PMID: 21085203.
12. Sun YV. Integration of biological networks and pathways with genetic association studies. Human genetics. 2012; 131(10):1677-86. doi: 10.1007/s00439-012-1198-7 PMID: 22777728; PubMed Central PMCID: PMC3432693.
13. Askland K, Read C, O'Connell C, Moore JH. Ion channels and schizophrenia: a gene set-based analytic approach to GWAS data for biological hypothesis testing. Human genetics. 2012; 131(3):373-91. doi: 10.1007/s00439-011-1082-x PMID: 21866342; PubMed Central PMCID: PMC3278516.
14. Yu H, Bi W, Liu C, Zhao Y, Zhang D, Yue W. A hypothesis-driven pathway analysis reveals myelinrelated pathways that contribute to the risk of schizophrenia and bipolar disorder. Progress in neuropsychopharmacology & biological psychiatry. 2014; 51:140-5. doi: 10.1016/j.pnpbp.2014.01.006 PMID: 24447946.
15. Jia P, Wang L, Meltzer HY, Zhao Z. Common variants conferring risk of schizophrenia: a pathway analysis of GWAS data. Schizophrenia research. 2010; 122(1-3):38-42. doi: 10.1016/j.schres.2010.07. 001 PMID: 20659789; PubMed Central PMCID: PMC2933424.
16. O'Dushlaine C, Kenny E, Heron E, Donohoe G, Gill M, Morris D, et al. Molecular pathways involved in neuronal cell adhesion and membrane scaffolding contribute to schizophrenia and bipolar disorder susceptibility. Molecular psychiatry. 2011; 16(3):286-92. doi: 10.1038/mp.2010.7 PMID: 20157312.
17. Hargreaves A, Anney R, O'Dushlaine C, Nicodemus KK, Schizophrenia Psychiatric Genome-Wide Association Study C, Wellcome Trust Case Control C, et al. The one and the many: effects of the cell adhesion molecule pathway on neuropsychological function in psychosis. Psychological medicine. 2014; 44(10):2177-87. doi: 10.1017/S0033291713002663 PMID: 24284030.
18. Yang X, Hou D, Jiang W, Zhang C. Intercellular protein-protein interactions at synapses. Protein & cell. 2014; 5(6):420-44. doi: 10.1007/s13238-014-0054-z PMID: 24756565; PubMed Central PMCID: PMC4026422.
19. Elangbam CS, Qualls CW Jr, Dahlgren RR. Cell adhesion molecules - update. Veterinary pathology. 1997; 34(1):61-73. PMID: 9150551.
20. Benson DL, Schnapp LM, Shapiro L, Huntley GW. Making memories stick: cell-adhesion molecules in synaptic plasticity. Trends in cell biology. 2000; 10(11):473-82. PMID: 11050419.
21. Wright JW, Kramar EA, Meighan SE, Harding JW. Extracellular matrix molecules, long-term potentiation, memory consolidation and the brain angiotensin system. Peptides. 2002; 23(1):221-46. PMID: 11814638.
22. Honer WG, Falkai P, Young C, Wang T, Xie J, Bonner J, et al. Cingulate cortex synaptic terminal proteins and neural cell adhesion molecule in schizophrenia. Neuroscience. 1997; 78(1):99-110. PMID: 9135092.
23. Vawter MP, Howard AL, Hyde TM, Kleinman JE, Freed WJ. Alterations of hippocampal secreted NCAM in bipolar disorder and synaptophysin in schizophrenia. Molecular psychiatry. 1999; 4(5):467-75. PMID: 10523820.
24. Yue W, Yang Y, Zhang Y, Lu T, Hu X, Wang L, et al. A case-control association study of NRXN1 polymorphisms with schizophrenia in Chinese Han population. Behavioral and brain functions: BBF. 2011; 7:7. doi: 10.1186/1744-9081-7-7 PMID: 21477380; PubMed Central PMCID: PMC3080281.
25. Sun C, Cheng MC, Qin R, Liao DL, Chen TT, Koong FJ, et al. Identification and functional characterization of rare mutations of the neuroligin-2 gene (NLGN2) associated with schizophrenia. Human molecular genetics. 2011; 20(15):3042-51. doi: 10.1093/hmg/ddr208 PMID: 21551456; PubMed Central PMCID: PMC3131045.
26. Andreassen OA, Harbo HF, Wang Y, Thompson W, Schork A, Mattingsdal M, et al. Genetic pleiotropy between multiple sclerosis and schizophrenia but not bipolar disorder: differential involvement of immune-related gene loci. Molecular psychiatry. 2014.
27. Yue WH, Wang HF, Sun LD, Tang FL, Liu ZH, Zhang HX, et al. Genome-wide association study identifies a susceptibility locus for schizophrenia in Han Chinese at 11p11.2. Nature genetics. 2011; 43 (12):1228-31. doi: 10.1038/ng.979 PMID: 22037552.
28. Sudhof TC. Neuroligins and neurexins link synaptic function to cognitive disease. Nature. 2008; 455 (7215):903-11. doi: 10.1038/nature07456 PMID: 18923512; PubMed Central PMCID: PMC2673233.
29. Choi YB, Li HL, Kassabov SR, Jin I, Puthanveettil SV, Karl KA, et al. Neurexin-neuroligin transsynaptic interaction mediates learning-related synaptic remodeling and long-term facilitation in aplysia. Neuron. 2011; 70(3):468-81. doi: 10.1016/j.neuron.2011.03.020 PMID: 21555073; PubMed Central PMCID: PMC3136118.
30. Blundell J, Blaiss CA, Etherton MR, Espinosa F, Tabuchi K, Walz C, et al. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010; 30(6):2115-29. doi: 10.1523/JNEUROSCI.4517-09. 2010 PMID: 20147539; PubMed Central PMCID: PMC2824441.
31. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, Wood S, et al. Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature. 2009; 459(7246):569-73. doi: 10.1038/nature07953 PMID: 19404257
32. Lewis CM, Ng MY, Butler AW, Cohen-Woods S, Uher R, Pirlo K, et al. Genome-wide association study of major recurrent depression in the UK population. The American journal of psychiatry. 2010.
33. Li MX, Kwan JS, Sham PC. HYST: a hybrid set-based test for genome-wide association studies, with application to protein-protein interaction-based association analysis. American journal of human genetics. 2012; 91(3):478-88. doi: 10.1016/j.ajhg.2012.08.004 PMID: 22958900; PubMed Central PMCID: PMC3511992.
34. Li MX, Gui HS, Kwan JS, Sham PC. GATES: a rapid and powerful gene-based association test using extended Simes procedure. American journal of human genetics. 2011; 88(3):283-93. doi: 10.1016/j. ajhg.2011.01.019 PMID: 21397060; PubMed Central PMCID: PMC3059433.
35. Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, et al. The structure of haplotype blocks in the human genome. Science. 2002; 296(5576):2225-9. doi: 10.1126/science.1069424 PMID: 12029063.
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for wholegenome association and population-based linkage analyses. American journal of human genetics. 2007; 81(3):559-75. doi: 10.1086/519795 PMID: 17701901; PubMed Central PMCID: PMC1950838.
37. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. 2003; 327(7414):557-60. doi: 10.1136/bmj.327.7414.557 PMID: 12958120; PubMed Central PMCID: PMC192859.
38. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7(3):177-88. PMID: 3802833.
39. Benita Y, Cao Z, Giallourakis C, Li C, Gardet A, Xavier RJ. Gene enrichment profiles reveal T-cell development, differentiation, and lineage-specific transcription factors including ZBTB25 as a novel NF-AT repressor. Blood. 2010; 115(26):5376-84. doi: 10.1182/blood-2010-01-263855 PMID: 20410506; PubMed Central PMCID: PMC2902135.
40. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatio-temporal transcriptome of the human brain. Nature. 2011; 478(7370):483-9. doi: 10.1038/nature10523 PMID: 22031440; PubMed Central PMCID: PMC3566780.
41. Murphy A, Chu JH, Xu M, Carey VJ, Lazarus R, Liu A, et al. Mapping of numerous disease-associated expression polymorphisms in primary peripheral blood CD4+ lymphocytes. Human molecular genetics. 2010; 19(23):4745-57. doi: 10.1093/hmg/ddq392 PMID: 20833654; PubMed Central PMCID: PMC2972694.
42. Zou F, Chai HS, Younkin CS, Allen M, Crook J, Pankratz VS, et al. Brain expression genome-wide association study (eGWAS) identifies human disease-associated variants. PLoS genetics. 2012; 8(6): e1002707. doi: 10.1371/journal.pgen.1002707 PMID: 22685416; PubMed Central PMCID: PMC3369937.
43. Bray NJ. Gene expression in the etiology of schizophrenia. Schizophrenia bulletin. 2008; 34(3):412-8. doi: 10.1093/schbul/sbn013 PMID: 18334509; PubMed Central PMCID: PMC2632437.
44. Bacanu SA, Chen J, Sun J, Richardson K, Lai CQ, Zhao Z, et al. Functional SNPs are enriched for schizophrenia association signals. Molecular psychiatry. 2014; 19(3):276-7. doi: 10.1038/mp.2013.33 PMID: 23546170.
45. Yang TP, Beazley C, Montgomery SB, Dimas AS, Gutierrez-Arcelus M, Stranger BE, et al. Genevar: a database and Java application for the analysis and visualization of SNP-gene associations in eQTL studies. Bioinformatics. 2010; 26(19):2474-6. doi: 10.1093/bioinformatics/btq452 PMID: 20702402; PubMed Central PMCID: PMC2944204.
46. Ramasamy A, Trabzuni D, Guelfi S, Varghese V, Smith C, Walker R, et al. Genetic variability in the regulation of gene expression in ten regions of the human brain. Nature neuroscience. 2014; 17(10):1418-28. doi: 10.1038/nn.3801 PMID: 25174004; PubMed Central PMCID: PMC4208299.
47. Dimas AS, Deutsch S, Stranger BE, Montgomery SB, Borel C, Attar-Cohen H, et al. Common regulatory variation impacts gene expression in a cell type-dependent manner. Science. 2009; 325 (5945):1246-50. doi: 10.1126/science.1174148 PMID: 19644074; PubMed Central PMCID: PMC2867218.
48. Mighdoll MI, Tao R, Kleinman JE, Hyde TM. Myelin, myelin-related disorders, and psychosis. Schizophrenia research. 2015; 161(1):85-93. doi: 10.1016/j.schres.2014.09.040 PMID: 25449713.
49. Sanes JR, Yamagata M. Many paths to synaptic specificity. Annual review of cell and developmental biology. 2009; 25:161-95. doi: 10.1146/annurev.cellbio.24.110707.175402 PMID: 19575668.
50. Feinberg K, Eshed-Eisenbach Y, Frechter S, Amor V, Salomon D, Sabanay H, et al. A glial signal consisting of gliomedin and NrCAM clusters axonal Na+ channels during the formation of nodes of Ranvier. Neuron. 2010; 65(4):490-502. doi: 10.1016/j.neuron.2010.02.004 PMID: 20188654; PubMed Central PMCID: PMC2831809.
51. Sakurai T. The role of NrCAM in neural development and disorders - beyond a simple glue in the brain. Molecular and cellular neurosciences. 2012; 49(3):351-63. doi: 10.1016/j.mcn.2011.12.002 PMID: 22182708.
52. Corvin A, Morris DW. Genome-wide association studies: findings at the major histocompatibility complex locus in psychosis. Biological psychiatry. 2014; 75(4):276-83. doi: 10.1016/j.biopsych.2013.09. 018 PMID: 24199664.
53. Brown AS. Prenatal infection as a risk factor for schizophrenia. Schizophrenia bulletin. 2006; 32 (2):200-2. doi: 10.1093/schbul/sbj052 PMID: 16469941; PubMed Central PMCID: PMC2632220.
54. Bundy H, Stahl D, MacCabe JH. A systematic review and meta-analysis of the fertility of patients with schizophrenia and their unaffected relatives. Acta psychiatrica Scandinavica. 2011; 123(2):98-106. doi: 10.1111/j.1600-0447.2010.01623.x PMID: 20958271.
55. Eaton WW, Byrne M, Ewald H, Mors O, Chen CY, Agerbo E, et al. Association of schizophrenia and autoimmune diseases: linkage of Danish national registers. The American journal of psychiatry. 2006; 163(3):521-8. doi: 10.1176/appi.ajp.163.3.521 PMID: 16513876.
56. Reissner C, Klose M, Fairless R, Missler M. Mutational analysis of the neurexin/neuroligin complex reveals essential and regulatory components. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(39):15124-9. doi: 10.1073/pnas.0801639105 PMID: 18812509; PubMed Central PMCID: PMC2551626.
57. Song JY, Ichtchenko K, Sudhof TC, Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96(3):1100-5. PMID: 9927700; PubMed Central PMCID: PMC15357.
58. Millson A, Lagrave D, Willis MJ, Rowe LR, Lyon E, South ST. Chromosomal loss of 3q26.3-3q26.32, involving a partial neuroligin 1 deletion, identified by genomic microarray in a child with microcephaly, seizure disorder, and severe intellectual disability. American journal of medical genetics Part A. 2012; 158A(1):159-65. doi: 10.1002/ajmg.a.34349 PMID: 22106001.