Evidence for schizophrenia susceptibility alleles in the Indian population: An association of neurodevelopmental genes in case-control and familial samples

Schizophrenia Research

Volumn 162, Issue 1-3, 2015, Pages 112-117

  Jajodia, Ajay ^a   Kaur, Harpreet ^a   Kumari, Kalpana ^b   Gupta, Meenal ^a   Baghel, Ruchi ^a   Srivastava, Ankit ^a   Sood, Mamta ^b   Chadda, Rakesh Kumar ^b   Jain, Sanjeev ^c   Kukreti, Ritushree ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^c NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

Author keywords

Meta analysis; PGC; Rs1062613; Rs548181; Schizophrenia; TDT

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 4; SEROTONIN 2A RECEPTOR; EBF1 PROTEIN, HUMAN; ERBB4 PROTEIN, HUMAN; HTR3A PROTEIN, HUMAN; SEROTONIN 3 RECEPTOR; TRANSACTIVATOR PROTEIN;

ADULT; ALLELE; ARTICLE; CASE CONTROL STUDY; CONTROLLED STUDY; DISEASE SEVERITY; DRAVIDIAN PEOPLE; EBF1 GENE; ERBB4 GENE; FEMALE; GENE; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; GRM7 GENE; HTR3A GENE; HUMAN; INDIA; INDO-EUROPEAN PEOPLE; INTRON; MAJOR CLINICAL STUDY; MALE; NERVE CELL DIFFERENTIATION; NRG1 GENE; PRIORITY JOURNAL; PROMOTER REGION; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM; STT3A GENE; ASIAN CONTINENTAL ANCESTRY GROUP; CAUCASIAN; FAMILY; GENETIC PREDISPOSITION; GENETICS; GENOTYPING TECHNIQUE; META ANALYSIS; MIDDLE AGED;

ADULT; ASIAN CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; FAMILY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPING TECHNIQUES; HUMANS; INDIA; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTOR, ERBB-4; RECEPTORS, SEROTONIN, 5-HT3; SCHIZOPHRENIA; TRANS-ACTIVATORS;

EID: 84923218060     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2014.12.031     Document Type: Article

References (62)

1. Adkins D.E., Khachane A.N., McClay J.L., Aberg K., Bukszar J., Sullivan P.F., van den Oord E.J. SNP-based analysis of neuroactive ligand-receptor interaction pathways implicates PGE2 as a novel mediator of antipsychotic treatment response: data from the CATIE study. Schizophr. Res. 2012, 135(1-3):200-201.
2. Anderson C.A., Pettersson F.H., Clarke G.M., Cardon L.R., Morris A.P., Zondervan K.T. Data quality control in genetic case-control association studies. Nat. Protoc. 2010, 5(9):1564-1573.
3. Ayalew M., Le-Niculescu H., Levey D.F., Jain N., Changala B., Patel S.D., Winiger E., Breier A., Shekhar A., Amdur R., Koller D., Nurnberger J.I., Corvin A., Geyer M., Tsuang M.T., Salomon D., Schork N.J., Fanous A.H., O'Donovan M.C., Niculescu A.B. Convergent functional genomics of schizophrenia: from comprehensive understanding to genetic risk prediction. Mol. Psychiatry 2012, 17(9):887-905.
4. Bae J.S., Pasaje C.F., Park B.L., Cheong H.S., Kim J.H., Kim J.Y., Shin J.G., Park C.S., Kim B.J., Lee C.S., Lee M., Choi W.H., Shin T.M., Hwang J., Shin H.D., Woo S.I. Genetic association analysis of ERBB4 polymorphisms with the risk of schizophrenia and SPEM abnormality in a Korean population. Brain Res. 2012, 1466:146-151.
5. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38(8):1083-1152.
6. Barrett J.C., Fry B., Maller J., Daly M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21(2):263-265.
7. Bergen S.E., Petryshen T.L. Genome-wide association studies of schizophrenia: does bigger lead to better results?. Curr. Opin. Psychiatr 2012, 25(2):76-82.
8. Bousman C.A., Yung A.R., Pantelis C., Ellis J.A., Chavez R.A., Nelson B., Lin A., Wood S.J., Amminger G.P., Velakoulis D., McGorry P.D., Everall I.P., Foley D.L. Effects of NRG1 and DAOA genetic variation on transition to psychosis in individuals at ultra-high risk for psychosis. Transl. Psychiatry 2013, 3:e251.
9. Cannon T.D. Candidate gene studies in the GWAS era: the MET proto-oncogene, neurocognition, and schizophrenia. Am. J. Psychiatry 2010, 167(4):369-372.
10. Chen S., Velardez M.O., Warot X., Yu Z.X., Miller S.J., Cros D., Corfas G. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J. Neurosci. 2006, 26(12):3079-3086.
11. Choi K.H., Zepp M.E., Higgs B.W., Weickert C.S., Webster M.J. Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development. J. Psychiatry Neurosci. 2009, 34(6):450-458.
12. Colantuoni C., Hyde T.M., Mitkus S., Joseph A., Sartorius L., Aguirre C., Creswell J., Johnson E., Deep-Soboslay A., Herman M.M., Lipska B.K., Weinberger D.R., Kleinman J.E. Age-related changes in the expression of schizophrenia susceptibility genes in the human prefrontal cortex. Brain Struct. Funct. 2008, 213(1-2):255-271.
13. de Bakker P.I., Yelensky R., Pe'er I., Gabriel S.B., Daly M.J., Altshuler D. Efficiency and power in genetic association studies. Nat. Genet. 2005, 37(11):1217-1223.
14. Derks E.M., Ophoff R.A. Replication and refinement of the role of rs548181 in schizophrenia: results from a family based study. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2013, 162B(1):75-77.
15. Emamian E.S., Hall D., Birnbaum M.J., Karayiorgou M., Gogos J.A. Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat. Genet. 2004, 36(2):131-137.
16. Enomoto A., Asai N., Namba T., Wang Y., Kato T., Tanaka M., Tatsumi H., Taya S., Tsuboi D., Kuroda K., Kaneko N., Sawamoto K., Miyamoto R., Jijiwa M., Murakumo Y., Sokabe M., Seki T., Kaibuchi K., Takahashi M. Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 2009, 63(6):774-787.
17. Ganda C., Schwab S.G., Amir N., Heriani H., Irmansyah I., Kusumawardhani A., Nasrun M., Widyawati I., Maier W., Wildenauer D.B. A family-based association study of DNA sequence variants in GRM7 with schizophrenia in an Indonesian population. Int. J. Neuropsychopharmacol. 2009, 12(9):1283-1289.
18. Goff D.C., Coyle J.T. The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am. J. Psychiatry 2001, 158(9):1367-1377.
19. Harrison P.J., Owen M.J. Genes for schizophrenia? Recent findings and their pathophysiological implications. Lancet 2003, 361(9355):417-419.
20. Hatzimanolis A., McGrath J.A., Wang R., Li T., Wong P.C., Nestadt G., Wolyniec P.S., Valle D., Pulver A.E., Avramopoulos D. Multiple variants aggregate in the neuregulin signaling pathway in a subset of schizophrenia patients. Transl. Psychiatry 2013, 3:e264.
21. He Z., Wang K.C., Koprivica V., Ming G., Song H.J. Knowing how to navigate: mechanisms of semaphorin signaling in the nervous system. Sci. STKE 2002, 2002(119):re1.
22. IGVC The Indian Genome Variation database (IGVdb): a project overview. Hum. Genet. 2005, 118(1):1-11.
23. Jha P., Sinha S., Kanchan K., Qidwai T., Narang A., Singh P.K., Pati S.S., Mohanty S., Mishra S.K., Sharma S.K., Awasthi S., Venkatesh V., Jain S., Basu A., Xu S., Mukerji M., Habib S. Deletion of the APOBEC3B gene strongly impacts susceptibility to falciparum malaria. Infect. Genet. Evol. 2012, 12(1):142-148.
24. Karam C.S., Ballon J.S., Bivens N.M., Freyberg Z., Girgis R.R., Lizardi-Ortiz J.E., Markx S., Lieberman J.A., Javitch J.A. Signaling pathways in schizophrenia: emerging targets and therapeutic strategies. Trends Pharmacol. Sci. 2010, 31(8):381-390.
25. Kazeem G.R., Farrall M. Integrating case-control and TDT studies. Ann. Hum. Genet. 2005, 69(Pt 3):329-335.
26. Kilpatrick L.A., Labus J.S., Coveleskie K., Hammer C., Rappold G., Tillisch K., Bueller J.A., Suyenobu B., Jarcho J.M., McRoberts J.A., Niesler B., Mayer E.A. The HTR3A polymorphism c. -42C>T is associated with amygdala responsiveness in patients with irritable bowel syndrome. Gastroenterology 2011, 140(7):1943-1951.
27. Kim J.Y., Liu C.Y., Zhang F., Duan X., Wen Z., Song J., Feighery E., Lu B., Rujescu D., St Clair D., Christian K., Callicott J.H., Weinberger D.R., Song H., Ming G.L. Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 2012, 148(5):1051-1064.
28. Kolk S.M., Gunput R.A., Tran T.S., van den Heuvel D.M., Prasad A.A., Hellemons A.J., Adolfs Y., Ginty D.D., Kolodkin A.L., Burbach J.P., Smidt M.P., Pasterkamp R.J. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J. Neurosci. 2009, 29(40):12542-12557.
29. Kukshal P., Bhatia T., Bhagwat A.M., Gur R.E., Gur R.C., Deshpande S.N., Nimgaonkar V.L., Thelma B.K. Association study of neuregulin-1 gene polymorphisms in a North Indian schizophrenia sample. Schizophr. Res. 2013, 144(1-3):24-30.
30. Law A.J., Kleinman J.E., Weinberger D.R., Weickert C.S. Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum. Mol. Genet. 2007, 16(2):129-141.
31. Liu Y., Li Z., Zhang M., Deng Y., Yi Z., Shi T. Exploring the pathogenetic association between schizophrenia and type 2 diabetes mellitus diseases based on pathway analysis. BMC Med. Genet. 2013, 6(Suppl. 1):S17.
32. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neuroscience 2008, 9(6):437-452.
33. Moghaddam B. Bringing order to the glutamate chaos in schizophrenia. Neuron 2003, 40(5):881-884.
34. Munafo M.R., Thiselton D.L., Clark T.G., Flint J. Association of the NRG1 gene and schizophrenia: a meta-analysis. Mol. Psychiatry 2006, 11(6):539-546.
35. Need A.C., Keefe R.S., Ge D., Grossman I., Dickson S., McEvoy J.P., Goldstein D.B. Pharmacogenetics of antipsychotic response in the CATIE trial: a candidate gene analysis. Eur. J. Hum. Genet. 2009, 17(7):946-957.
36. Ng M.Y., Levinson D.F., Faraone S.V., Suarez B.K., DeLisi L.E., Arinami T., Riley B., Paunio T., Pulver A.E., Irmansyah, Holmans P.A., Escamilla M., Wildenauer D.B., Williams N.M., Laurent C., Mowry B.J., Brzustowicz L.M., Maziade M., Sklar P., Garver D.L., Abecasis G.R., Lerer B., Fallin M.D., Gurling H.M., Gejman P.V., Lindholm E., Moises H.W., Byerley W., Wijsman E.M., Forabosco P., Tsuang M.T., Hwu H.G., Okazaki Y., Kendler K.S., Wormley B., Fanous A., Walsh D., O'Neill F.A., Peltonen L., Nestadt G., Lasseter V.K., Liang K.Y., Papadimitriou G.M., Dikeos D.G., Schwab S.G., Owen M.J., O'Donovan M.C., Norton N., Hare E., Raventos H., Nicolini H., Albus M., Maier W., Nimgaonkar V.L., Terenius L., Mallet J., Jay M., Godard S., Nertney D., Alexander M., Crowe R.R., Silverman J.M., Bassett A.S., Roy M.A., Merette C., Pato C.N., Pato M.T., Roos J.L., Kohn Y., Amann-Zalcenstein D., Kalsi G., McQuillin A., Curtis D., Brynjolfson J., Sigmundsson T., Petursson H., Sanders A.R., Duan J., Jazin E., Myles-Worsley M., Karayiorgou M., Lewis C.M. Meta-analysis of 32 genome-wide linkage studies of schizophrenia. Mol. Psychiatry 2009, 14(8):774-785.
37. Nicodemus K.K., Luna A., Vakkalanka R., Goldberg T., Egan M., Straub R.E., Weinberger D.R. Further evidence for association between ErbB4 and schizophrenia and influence on cognitive intermediate phenotypes in healthy controls. Mol. Psychiatry 2006, 11(12):1062-1065.
38. Niesler B., Flohr T., Nothen M.M., Fischer C., Rietschel M., Franzek E., Albus M., Propping P., Rappold G.A. Association between the 5' UTR variant C178T of the serotonin receptor gene HTR3A and bipolar affective disorder. Pharmacogenetics 2001, 11(6):471-475.
39. Ohtsuki T., Koga M., Ishiguro H., Horiuchi Y., Arai M., Niizato K., Itokawa M., Inada T., Iwata N., Iritani S., Ozaki N., Kunugi H., Ujike H., Watanabe Y., Someya T., Arinami T. A polymorphism of the metabotropic glutamate receptor mGluR7 (GRM7) gene is associated with schizophrenia. Schizophr. Res. 2008, 101(1-3):9-16.
40. Pitcher G.M., Kalia L.V., Ng D., Goodfellow N.M., Yee K.T., Lambe E.K., Salter M.W. Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors. Nat. Med. 2011, 17(4):470-478.
41. Price A.L., Patterson N.J., Plenge R.M., Weinblatt M.E., Shadick N.A., Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 2006, 38(8):904-909.
42. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155(2):945-959.
43. 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. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007, 81(3):559-575.
44. Putnam D.K., Sun J., Zhao Z. Exploring schizophrenia drug-gene interactions through molecular network and pathway modeling. AMIA Annual Symposium Proceedings/AMIA Symposium 2011, 1127-1133.
45. Rajkumar A.P., Poonkuzhali B., Kuruvilla A., Srivastava A., Jacob M., Jacob K.S. Outcome definitions and clinical predictors influence pharmacogenetic associations between HTR3A gene polymorphisms and response to clozapine in patients with schizophrenia. Psychopharmacology (Berlin) 2012, 224(3):441-449.
46. Reich D., Thangaraj K., Patterson N., Price A.L., Singh L. Reconstructing Indian population history. Nature 2009, 461(7263):489-494.
47. Ruiz-Canada C., Kelleher D.J., Gilmore R. Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell 2009, 136(2):272-283.
48. Schizophrenia Psychiatric Genome-Wide Association Study Consortium Genome-wide association study identifies five new schizophrenia loci. Nat. Genet. 2011, 43(10):969-976.
49. Shamir A., Kwon O.B., Karavanova I., Vullhorst D., Leiva-Salcedo E., Janssen M.J., Buonanno A. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J. Neurosci. 2012, 32(9):2988-2997.
50. Shi Y., Li Z., Xu Q., Wang T., Li T., Shen J., Zhang F., Chen J., Zhou G., Ji W., Li B., Xu Y., Liu D., Wang P., Yang P., Liu B., Sun W., Wan C., Qin S., He G., Steinberg S., Cichon S., Werge T., Sigurdsson E., Tosato S., Palotie A., Nothen M.M., Rietschel M., Ophoff R.A., Collier D.A., Rujescu D., Clair D.S., Stefansson H., Stefansson K., Ji J., Wang Q., Li W., Zheng L., Zhang H., Feng G., He L. Common variants on 8p12 and 1q24.2 confer risk of schizophrenia. Nat. Genet. 2011, 43(12):1224-1227.
51. Shibata H., Tani A., Chikuhara T., Kikuta R., Sakai M., Ninomiya H., Tashiro N., Iwata N., Ozaki N., Fukumaki Y. Association study of polymorphisms in the group III metabotropic glutamate receptor genes, GRM4 and GRM7, with schizophrenia. Psychiatry Res. 2009, 167(1-2):88-96.
52. Shrimal S., Trueman S.F., Gilmore R. Extreme C-terminal sites are posttranslocationally glycosylated by the STT3B isoform of the OST. J. Cell Biol. 2013, 201(1):81-95.
53. Silberberg G., Darvasi A., Pinkas-Kramarski R., Navon R. The involvement of ErbB4 with schizophrenia: association and expression studies. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2006, 141B(2):142-148.
54. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., Brynjolfsson J., Gunnarsdottir S., Ivarsson O., Chou T.T., Hjaltason O., Birgisdottir B., Jonsson H., Gudnadottir V.G., Gudmundsdottir E., Bjornsson A., Ingvarsson B., Ingason A., Sigfusson S., Hardardottir H., Harvey R.P., Lai D., Zhou M., Brunner D., Mutel V., Gonzalo A., Lemke G., Sainz J., Johannesson G., Andresson T., Gudbjartsson D., Manolescu A., Frigge M.L., Gurney M.E., Kong A., Gulcher J.R., Petursson H., Stefansson K. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 2002, 71(4):877-892.
55. Tandon R., Keshavan M.S., Nasrallah H.A. Schizophrenia, "just the facts" what we know in 2008. 2. Epidemiology and etiology. Schizophr. Res. 2008, 102(1-3):1-18.
56. Thirunavukkarasu P., Vijayakumari A.A., John J.P., Halahalli H.N., Paul P., Sen S., Purushottam M., Jain S. An exploratory association study of the influence of dysbindin and neuregulin polymorphisms on brain morphometry in patients with schizophrenia and healthy subjects from South India. Asian J. Psychiatry 2014, 10:62-68.
57. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., Nord A.S., Kusenda M., Malhotra D., Bhandari A., Stray S.M., Rippey C.F., Roccanova P., Makarov V., Lakshmi B., Findling R.L., Sikich L., Stromberg T., Merriman B., Gogtay N., Butler P., Eckstrand K., Noory L., Gochman P., Long R., Chen Z., Davis S., Baker C., Eichler E.E., Meltzer P.S., Nelson S.F., Singleton A.B., Lee M.K., Rapoport J.L., King M.C., Sebat J. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008, 320(5875):539-543.
58. Wilkening S., Chen B., Bermejo J.L., Canzian F. Is there still a need for candidate gene approaches in the era of genome-wide association studies?. Genomics 2009, 93(5):415-419.
59. Williams N.M., Preece A., Spurlock G., Norton N., Williams H.J., Zammit S., O'Donovan M.C., Owen M.J. Support for genetic variation in neuregulin 1 and susceptibility to schizophrenia. Mol. Psychiatry 2003, 8(5):485-487.
60. Yang J.Z., Si T.M., Ruan Y., Ling Y.S., Han Y.H., Wang X.L., Zhou M., Zhang H.Y., Kong Q.M., Liu C., Zhang D.R., Yu Y.Q., Liu S.Z., Ju G.Z., Shu L., Ma D.L., Zhang D. Association study of neuregulin 1 gene with schizophrenia. Mol. Psychiatry 2003, 8(7):706-709.
61. Yin M., Liu S., Yin Y., Li S., Li Z., Wu X., Zhang B., Ang S.L., Ding Y., Zhou J. Ventral mesencephalon-enriched genes that regulate the development of dopaminergic neurons in vivo. J. Neurosci. 2009, 29(16):5170-5182.
62. Yue W.H., Wang H.F., Sun L.D., Tang F.L., Liu Z.H., Zhang H.X., Li W.Q., Zhang Y.L., Zhang Y., Ma C.C., Du B., Wang L.F., Ren Y.Q., Yang Y.F., Hu X.F., Wang Y., Deng W., Tan L.W., Tan Y.L., Chen Q., Xu G.M., Yang G.G., Zuo X.B., Yan H., Ruan Y.Y., Lu T.L., Han X., Ma X.H., Cai L.W., Jin C., Zhang H.Y., Yan J., Mi W.F., Yin X.Y., Ma W.B., Liu Q., Kang L., Sun W., Pan C.Y., Shuang M., Yang F.D., Wang C.Y., Yang J.L., Li K.Q., Ma X., Li L.J., Yu X., Li Q.Z., Huang X., Lv L.X., Li T., Zhao G.P., Huang W., Zhang X.J., Zhang D. Genome-wide association study identifies a susceptibility locus for schizophrenia in Han Chinese at 11p11.2. Nat. Genet. 2011, 43(12):1228-1231.