Functional genetic variation at the NRGN gene and schizophrenia: Evidence from a gene-based case-control study and gene expression analysis

American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics

Volumn 159 B, Issue 4, 2012, Pages 405-413

  Ohi, Kazutaka ^a,b,c   Hashimoto, Ryota ^a,b,d   Yasuda, Yuka ^a,b   Fukumoto, Motoyuki ^a,b   Yamamori, Hidenaga ^a,b   Umeda Yano, Satomi ^a   Okada, Takeya ^a,b   Kamino, Kouzin ^a,c   Morihara, Takashi ^a   Iwase, Masao ^a   Kazui, Hiroaki ^a   Numata, Shusuke ^e   Ikeda, Masashi ^b,f   Ohnuma, Tohru ^g   Iwata, Nakao ^b,f   Ueno, Shu ichi ^h   Ozaki, Norio ^b,i   Ohmori, Tetsuro ^e   Arai, Heii ^g   Takeda, Masatoshi ^a,d  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c Yamato Mental Medical Center   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKUSHIMA   (Japan)

^f FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^h EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

ⁱ NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Gene expression; Genome wide association study (GWAS); neurogranin (NRGN); Schizophrenia; Single nucleotide polymorphism (SNP)

Indexed keywords

NEUROGRANIN;

ADULT (18-64); ARTICLE; CASE CONTROL STUDY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; HAPLOTYPE; HUMAN; HUMAN CELL; JAPANESE; LYMPHOBLAST; MAJOR CLINICAL STUDY (<50); MALE; PRIORITY JOURNAL; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; ASIAN CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOME, HUMAN; HAPLOTYPES; HUMANS; JAPAN; MALE; MIDDLE AGED; NEUROGRANIN; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER; SCHIZOPHRENIA;

EID: 84860647956     PISSN: 15524841     EISSN: 1552485X     Source Type: Journal    
DOI: 10.1002/ajmg.b.32043     Document Type: Article

References (32)

1. Baudier J, Deloulme JC, Van Dorsselaer A, Black D, Matthes HW. 1991. Purification and characterization of a brain-specific protein kinase C substrate, neurogranin (p17). Identification of a consensus amino acid sequence between neurogranin and neuromodulin (GAP43) that corresponds to the protein kinase C phosphorylation site and the calmodulin-binding domain. J Biol Chem 266(1): 229-237.
2. Betcheva ET, Mushiroda T, Takahashi A, Kubo M, Karachanak SK, Zaharieva IT, Vazharova RV, Dimova II, Milanova VK, Tolev T, Kirov G, Owen MJ, O'Donovan MC, Kamatani N, Nakamura Y, Toncheva DI. 2009. Case-control association study of 59 candidate genes reveals the DRD2 SNP rs6277 (C957T) as the only susceptibility factor for schizophrenia in the Bulgarian population. J Hum Genet 54(2): 98-107.
3. Cardno AG, Gottesman II. 2000. Twin studies of schizophrenia: From bow-and-arrow concordances to star wars Mx and functional genomics. Am J Med Genet 97(1): 12-17.
4. Dudbridge F. 2003. Pedigree disequilibrium tests for multilocus haplotypes. Genet Epidemiol 25(2): 115-121.
5. Gurling HM, Kalsi G, Brynjolfson J, Sigmundsson T, Sherrington R, Mankoo BS, 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(3): 661-673.
6. Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T, Mori T, Nemoto K, Adachi N, Izumi A, Chiba S, Noguchi H, Suzuki T, Iwata N, Ozaki N, Taguchi T, Kamiya A, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Sawa A, Kunugi H. 2006. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet 15(20): 3024-3033.
7. Hashimoto R, Hashimoto H, Shintani N, Chiba S, Hattori S, Okada T, Nakajima M, Tanaka K, Kawagishi N, Nemoto K, Mori T, Ohnishi T, Noguchi H, Hori H, Suzuki T, Iwata N, Ozaki N, Nakabayashi T, Saitoh O, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Kunugi H, Baba A. 2007. Pituitary adenylate cyclase-activating polypeptide is associated with schizophrenia. Mol Psychiatry 12(11): 1026-1032.
8. Hayashi Y. 2009. Long-term potentiation: Two pathways meet at neurogranin. EMBO J 28(19): 2859-2860.
9. Ikeda M, Aleksic B, Kinoshita Y, Okochi T, Kawashima K, Kushima I, Ito Y, Nakamura Y, Kishi T, Okumura T, Fukuo Y, Williams HJ, Hamshere ML, Ivanov D, Inada T, Suzuki M, Hashimoto R, Ujike H, Takeda M, Craddock N, Kaibuchi K, Owen MJ, Ozaki N, O'Donovan MC, Iwata N. 2011. Genome-wide association study of schizophrenia in a Japanese population. Biol Psychiatry 69(5): 472-478.
10. Li J, Pak JH, Huang FL, Huang KP. 1999. N-methyl-D-aspartate induces neurogranin/RC3 oxidation in rat brain slices. J Biol Chem 274(3): 1294-1300.
11. Li SS, Khalid N, Carlson C, Zhao LP. 2003. Estimating haplotype frequencies and standard errors for multiple single nucleotide polymorphisms. Biostatistics 4(4): 513-522.
12. Li T, Li Z, Chen P, Zhao Q, Wang T, Huang K, Li J, Li Y, Liu J, Zeng Z, Feng G, He L, Shi Y. 2010. Common variants in major histocompatibility complex region and TCF4 gene are significantly associated with schizophrenia in Han Chinese. Biol Psychiatry 68(7): 671-673.
13. Marcotte ER, Srivastava LK, Quirion R. 2003. cDNA microarray and proteomic approaches in the study of brain diseases: Focus on schizophrenia and Alzheimer's disease. Pharmacol Ther 100(1): 63-74.
14. Martinez de Arrieta C, Perez Jurado L, Bernal J, Coloma A. 1997. Structure, organization, and chromosomal mapping of the human neurogranin gene (NRGN). Genomics 41(2): 243-249.
15. Martinez de Arrieta C, Morte B, Coloma A, Bernal J. 1999. The human RC3 gene homolog, NRGN contains a thyroid hormone-responsive element located in the first intron. Endocrinology 140(1): 335-343.
16. Matigian NA, McCurdy RD, Feron F, Perry C, Smith H, Filippich C, McLean D, McGrath J, Mackay-Sim A, Mowry B, Hayward NK. 2008. Fibroblast and lymphoblast gene expression profiles in schizophrenia: Are non-neural cells informative? PLoS ONE 3(6): e2412.
17. Nyholt DR. 2001. Genetic case-control association studies-Correcting for multiple testing. Hum Genet 109(5): 564-567.
18. Nyholt DR. 2004. A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other. Am J Hum Genet 74(4): 765-769.
19. Ohi K, Hashimoto R, Yasuda Y, Yoshida T, Takahashi H, Iike N, Fukumoto M, et al. 2009. Association study of the G72 gene with schizophrenia in a Japanese population: A multicenter study. Schizophr Res 109(1-3): 80-85.
20. Ohi K, Hashimoto R, Yasuda Y, Yoshida T, Takahashi H, Iike N, Iwase M, et al. 2010. The chitinase 3-like 1 gene and schizophrenia: Evidence from a multi-center case-control study and meta-analysis. Schizophr Res 116(2-3): 126-132.
21. Ruano D, Aulchenko YS, Macedo A, Soares MJ, Valente J, Azevedo MH, Hutz MH, Gama CS, Lobato MI, Belmonte-de-Abreu P, Goodman AB, Pato C, Heutink P, Palha JA. 2008. Association of the gene encoding neurogranin with schizophrenia in males. J Psychiatr Res 42(2): 125-133.
22. Skol AD, Scott LJ, Abecasis GR, Boehnke M. 2006. Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies. Nat Genet 38(2): 209-213.
23. Slonimsky A, Levy I, Kohn Y, Rigbi A, Ben-Asher E, Lancet D, Agam G, Lerer B. 2010. Lymphoblast and brain expression of AHI1 and the novel primate-specific gene, C6orf217, in schizophrenia and bipolar disorder. Schizophr Res 120(1-3): 159-166.
24. Smith RL, Knight D, Williams H, Dwyer S, Richards A, Kirov G, O'Donovan MC, Owen MJ. 2011. Analysis of neurogranin (NRGN) in schizophrenia. Am J Med Genet Part B 156B(5): 532-535.
25. Stefansson H, Ophoff RA, Steinberg S, Andreassen OA, Cichon S, Rujescu D, Werge T, et al. 2009. Common variants conferring risk of schizophrenia. Nature 460(7256): 744-747.
26. Stranger BE, Nica AC, Forrest MS, Dimas A, Bird CP, Beazley C, Ingle CE, Dunning M, Flicek P, Koller D, Montgomery S, Tavare S, Deloukas P, Dermitzakis ET. 2007. Population genomics of human gene expression. Nat Genet 39(10): 1217-1224.
27. Sun J, Kuo PH, Riley BP, Kendler KS, Zhao Z. 2008. Candidate genes for schizophrenia: A survey of association studies and gene ranking. Am J Med Genet Part B 147B(7): 1173-1181.
28. Tsuang M. 2000. Schizophrenia: Genes and environment. Biol Psychiatry 47(3): 210-220.
29. Yamada K, Iwayama Y, Hattori E, Iwamoto K, Toyota T, Ohnishi T, Ohba H, Maekawa M, Kato T, Yoshikawa T. 2011. Genome-wide association study of schizophrenia in Japanese population. PLoS ONE 6(6): e20468.
30. Yamaguchi-Kabata Y, Nakazono K, Takahashi A, Saito S, Hosono N, Kubo M, Nakamura Y, Kamatani N. 2008. Japanese population structure, based on SNP genotypes from 7003 individuals compared to other ethnic groups: Effects on population-based association studies. Am J Hum Genet 83(4): 445-456.
31. Yamamori H, Hashimoto R, Verrall L, Yasuda Y, Ohi K, Fukumoto M, Umeda-Yano S, Ito A, Takeda M. 2011. Dysbindin-1 and NRG-1 gene expression in immortalized lymphocytes from patients with schizophrenia. J Hum Genet 56(7): 478-483.
32. Yasuda Y, Hashimoto R, Yamamori H, Ohi K, Fukumoto M, Umeda-Yano S, Mohri I, Ito A, Taniike M, Takeda M. 2011. Gene expression analysis in lymphoblasts derived from patients with autism spectrum disorder. Mol Autism 2(1): 9.