Fine Mapping on Chromosome 10q22-q23 Implicates Neuregulin 3 in Schizophrenia

American Journal of Human Genetics

Volumn 84, Issue 1, 2009, Pages 21-34

  Chen, Pei Lung ^a   Avramopoulos, Dimitrios ^a   Lasseter, Virginia K ^a   McGrath, John A ^a   Fallin, M Daniele ^b   Liang, Kung Yee ^b   Nestadt, Gerald ^a   Feng, Ningping ^a   Steel, Gary ^a   Cutting, Andrew S ^a   Wolyniec, Paula ^a   Pulver, Ann E ^a,b   Valle, David ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEU DIFFERENTIATION FACTOR;

ADULT; ARTICLE; CENTRAL NERVOUS SYSTEM; CHINESE; CHROMOSOME 10Q; CONTROLLED STUDY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; FEMALE; GENE DELETION; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENOTYPE PHENOTYPE CORRELATION; HERITABILITY; HUMAN; INTERVIEW; INTRON; JEW; LINKAGE ANALYSIS; MAJOR CLINICAL STUDY; MALE; MEDICAL ASSESSMENT; PARALOGY; PATHOGENESIS; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; QUANTITATIVE TRAIT; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM; TAIWAN;

CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 10; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LINKAGE (GENETICS); MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; SCHIZOPHRENIA; YOUNG ADULT;

EID: 58049209657     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2008.12.005     Document Type: Article

References (77)

1. Eaton W.W. Epidemiology of schizophrenia. Epidemiol. Rev. 7 (1985) 105-126
2. McGue M., and Gottesman I.I. The genetic epidemiology of schizophrenia and the design of linkage studies. Eur. Arch. Psychiatry Clin. Neurosci. 240 (1991) 174-181
3. Tsuang M.T., Gilbertson M.W., and Faraone S.V. The genetics of schizophrenia. Current knowledge and future directions. Schizophr. Res. 4 (1991) 157-171
4. Cardno A.G., and Gottesman I.I. Twin studies of schizophrenia: from bow-and-arrow concordances to star wars Mx and functional genomics. Am. J. Med. Genet. 97 (2000) 12-17
5. Owen M.J., Craddock N., and Jablensky A. The genetic deconstruction of psychosis. Schizophr. Bull. 33 (2007) 905-911
6. Badner J.A., and Gershon E.S. Meta-analysis of whole-genome linkage scans of bipolar disorder and schizophrenia. Mol. Psychiatry 7 (2002) 405-411
7. Lewis C.M., Levinson D.F., Wise L.H., DeLisi L.E., Straub R.E., Hovatta I., Williams N.M., Schwab S.G., Pulver A.E., Faraone S.V., et al. Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: schizophrenia. Am. J. Hum. Genet. 73 (2003) 34-48
8. Crow T.J. How and why genetic linkage has not solved the problem of psychosis: review and hypothesis. Am. J. Psychiatry 164 (2007) 13-21
9. Norton N., Williams H.J., and Owen M.J. An update on the genetics of schizophrenia. Curr. Opin. Psychiatry 19 (2006) 158-164
10. Sanders A.R., Duan J., Levinson D.F., Shi J., He D., Hou C., Burrell G.J., Rice J.P., Nertney D.A., Olincy A., et al. No significant association of 14 candidate genes with schizophrenia in a large European ancestry sample: implications for psychiatric genetics. Am. J. Psychiatry 165 (2008) 497-506
11. St Clair D., Blackwood D., Muir W., Carothers A., Walker M., Spowart G., Gosden C., and Evans H.J. Association within a family of a balanced autosomal translocation with major mental illness. Lancet 336 (1990) 13-16
12. Fanous A.H., and Kendler K.S. Genetic heterogeneity, modifier genes, and quantitative phenotypes in psychiatric illness: searching for a framework. Mol. Psychiatry 10 (2005) 6-13
13. Craddock N., and Owen M.J. The beginning of the end for the Kraepelinian dichotomy. Br. J. Psychiatry 186 (2005) 364-366
14. Jablensky A. Subtyping schizophrenia: implications for genetic research. Mol. Psychiatry 11 (2006) 815-836
15. Serretti A., Lilli R., Lorenzi C., Lattuada E., and Smeraldi E. DRD4 exon 3 variants associated with delusional symptomatology in major psychoses: a study on 2,011 affected subjects. Am. J. Med. Genet. 105 (2001) 283-290
16. Wilcox M.A., Faraone S.V., Su J., Van Eerdewegh P., and Tsuang M.T. Genome scan of three quantitative traits in schizophrenia pedigrees. Biol. Psychiatry 52 (2002) 847-854
17. Fanous A.H., van den Oord E.J., Riley B.P., Aggen S.H., Neale M.C., O'Neill F.A., Walsh D., and Kendler K.S. Relationship between a high-risk haplotype in the DTNBP1 (dysbindin) gene and clinical features of schizophrenia. Am. J. Psychiatry 162 (2005) 1824-1832
18. Fanous A.H., Neale M.C., Webb B.T., Straub R.E., Amdur R.L., O'Neill F.A., Walsh D., Riley B.P., and Kendler K.S. A genome-wide scan for modifier loci in schizophrenia. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 144 (2007) 589-595
19. Hall J., Whalley H.C., Job D.E., Baig B.J., McIntosh A.M., Evans K.L., Thomson P.A., Porteous D.J., Cunningham-Owens D.G., Johnstone E.C., et al. A neuregulin 1 variant associated with abnormal cortical function and psychotic symptoms. Nat. Neurosci. 9 (2006) 1477-1478
20. Freedman R., Adams C.E., Adler L.E., Bickford P.C., Gault J., Harris J.G., Nagamoto H.T., Olincy A., Ross R.G., Stevens K.E., et al. Inhibitory neurophysiological deficit as a phenotype for genetic investigation of schizophrenia. Am. J. Med. Genet. 97 (2000) 58-64
21. Nicodemus K.K., Luna A., Vakkalanka R., Goldberg T., Egan M., Straub R.E., and Weinberger D.R. Further evidence for association between ErbB4 and schizophrenia and influence on cognitive intermediate phenotypes in healthy controls. Mol. Psychiatry 11 (2006) 1062-1065
22. Fallin M.D., Lasseter V.K., Wolyniec P.S., McGrath J.A., Nestadt G., Valle D., Liang K.Y., and Pulver A.E. Genomewide linkage scan for schizophrenia susceptibility loci among Ashkenazi Jewish families shows evidence of linkage on chromosome 10q22. Am. J. Hum. Genet. 73 (2003) 601-611
23. Faraone S.V., Hwu H.G., Liu C.M., Chen W.J., Tsuang M.M., Liu S.K., Shieh M.H., Hwang T.J., Ou-Yang W.C., Chen C.Y., et al. Genome scan of Han Chinese schizophrenia families from Taiwan: confirmation of linkage to 10q22.3. Am. J. Psychiatry 163 (2006) 1760-1766
24. Balciuniene J., Feng N., Iyadurai K., Hirsch B., Charnas L., Bill B.R., Easterday M.C., Staaf J., Oseth L., Czapansky-Beilman D., et al. Recurrent 10q22-q23 deletions: a genomic disorder on 10q associated with cognitive and behavioral abnormalities. Am. J. Hum. Genet. 80 (2007) 938-947
25. Fallin M.D., Lasseter V.K., Avramopoulos D., Nicodemus K.K., Wolyniec P.S., McGrath J.A., Steel G., Nestadt G., Liang K.Y., Huganir R.L., et al. Bipolar I disorder and schizophrenia: a 440-single-nucleotide polymorphism screen of 64 candidate genes among Ashkenazi Jewish case-parent trios. Am. J. Hum. Genet. 77 (2005) 918-936
26. Guo S.Z., Huang K., Shi Y.Y., Tang W., Zhou J., Feng G.Y., Zhu S.M., Liu H.J., Chen Y., Sun X.D., et al. A case-control association study between the GRID1 gene and schizophrenia in the Chinese Northern Han population. Schizophr. Res. 93 (2007) 385-390
27. Benzel I., Bansal A., Browning B.L., Galwey N.W., Maycox P.R., McGinnis R., Smart D., St Clair D., Yates P., and Purvis I. Interactions among genes in the ErbB-Neuregulin signalling network are associated with increased susceptibility to schizophrenia. Behav. Brain Funct. 3 (2007) 31
28. McGrath J.A., Avramopoulos D., Lasseter V.K., Wolyniec P.S., Fallin M.D., Liang K.-Y., Nestadt G., Thornquist M.H., Luke J.R., Chen P.-L., et al. Familiality of novel factorial dimensions of schizophrenia. Arch. Gen. Psychiatry (2009) in press
29. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. Fourth Edition (1994), American Psychiatric Association, Washington, DC
30. Cannon-Spoor H.E., Potkin S.G., and Wyatt R.J. Measurement of premorbid adjustment in chronic schizophrenia. Schizophr. Bull. 8 (1982) 470-484
31. George V.T., and Elston R.C. Generalized modulus power transformations. Commun. Statist. Theory Meth. 17 (1988) 2933-2952
32. The International HapMap Consortium. A haplotype map of the human genome. Nature 437 (2005) 1299-1320
33. The International HapMap Consortium. The International HapMap Project. Nature 426 (2003) 789-796
34. Dausset J., Cann H., Cohen D., Lathrop M., Lalouel J.M., and White R. Centre d'etude du polymorphisme humain (CEPH): collaborative genetic mapping of the human genome. Genomics 6 (1990) 575-577
35. Dudbridge, F. (2006) UNPHASED user guide. Technical Report 2006/5, MRC Biostatistics Unit, Cambridge, UK.
36. Dudbridge F. Likelihood-based association analysis for nuclear families and unrelated subjects with missing genotype data. Hum. Hered. 66 (2008) 87-98
37. Spielman R.S., McGinnis R.E., and Ewens W.J. Transmission test for linkage disequilibrium: the insulin gene region and insulin-dependent diabetes mellitus (IDDM). Am. J. Hum. Genet. 52 (1993) 506-516
38. Laird N.M., Horvath S., and Xu X. Implementing a unified approach to family-based tests of association. Genet. Epidemiol. 19 Suppl 1 (2000) S36-S42
39. Abecasis G.R., Cardon L.R., and Cookson W.O. A general test of association for quantitative traits in nuclear families. Am. J. Hum. Genet. 66 (2000) 279-292
40. O'Connell J.R., and Weeks D.E. PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am. J. Hum. Genet. 63 (1998) 259-266
41. Barrett J.C., Fry B., Maller J., and Daly M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 (2005) 263-265
42. Chang Y.P., Liu X., Kim J.D., Ikeda M.A., Layton M.R., Weder A.B., Cooper R.S., Kardia S.L., Rao D.C., Hunt S.C., et al. Multiple genes for essential-hypertension susceptibility on chromosome 1q. Am. J. Hum. Genet. 80 (2007) 253-264
43. Nicodemus K.K., Liu W., Chase G.A., Tsai Y.Y., and Fallin M.D. Comparison of type I error for multiple test corrections in large single-nucleotide polymorphism studies using principal components versus haplotype blocking algorithms. BMC Genet. 6 Suppl 1 (2005) S78
44. Gabriel S.B., Schaffner S.F., Nguyen H., Moore J.M., Roy J., Blumenstiel B., Higgins J., DeFelice M., Lochner A., Faggart M., et al. The structure of haplotype blocks in the human genome. Science 296 (2002) 2225-2229
45. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., and Wheeler D.L. GenBank: update. Nucleic Acids Res. 32 (2004) D23-D26
46. Ostrer H. A genetic profile of contemporary Jewish populations. Nat. Rev. Genet. 2 (2001) 891-898
47. Neuhausen S.L., Godwin A.K., Gershoni-Baruch R., Schubert E., Garber J., Stoppa-Lyonnet D., Olah E., Csokay B., Serova O., Lalloo F., et al. Haplotype and phenotype analysis of nine recurrent BRCA2 mutations in 111 families: results of an international study. Am. J. Hum. Genet. 62 (1998) 1381-1388
48. Rennert H., Bercovich D., Hubert A., Abeliovich D., Rozovsky U., Bar-Shira A., Soloviov S., Schreiber L., Matzkin H., Rennert G., et al. A novel founder mutation in the RNASEL gene, 471delAAAG, is associated with prostate cancer in Ashkenazi Jews. Am. J. Hum. Genet. 71 (2002) 981-984
49. Stern H.S., Viertelhausen S., Hunter A.G., O'Rourke K., Cappelli M., Perras H., Serfas K., Blumenthall A., Dewar D., Baumann E., et al. APC I1307K increases risk of transition from polyp to colorectal carcinoma in Ashkenazi Jews. Gastroenterology 120 (2001) 392-400
50. Sugimura K., Taylor K.D., Lin Y.C., Hang T., Wang D., Tang Y.M., Fischel-Ghodsian N., Targan S.R., Rotter J.I., and Yang H. A novel NOD2/CARD15 haplotype conferring risk for Crohn disease in Ashkenazi Jews. Am. J. Hum. Genet. 72 (2003) 509-518
51. Service S., DeYoung J., Karayiorgou M., Roos J.L., Pretorious H., Bedoya G., Ospina J., Ruiz-Linares A., Macedo A., Palha J.A., et al. Magnitude and distribution of linkage disequilibrium in population isolates and implications for genome-wide association studies. Nat. Genet. 38 (2006) 556-560
52. McClellan J.M., Susser E., and King M.C. Schizophrenia: a common disease caused by multiple rare alleles. Br. J. Psychiatry 190 (2007) 194-199
53. McKusick V.A. On lumpers and splitters, or the nosology of genetic disease. Perspect. Biol. Med. 12 (1969) 298-312
54. Childs B., Finucci J.M., Preston M.S., and Pulver A.E. Human behavior genetics. Adv. Hum. Genet. 7 (1976) 57-97
55. Watson M.S., Cutting G.R., Desnick R.J., Driscoll D.A., Klinger K., Mennuti M., Palomaki G.E., Popovich B.W., Pratt V.M., Rohlfs E.M., et al. Cystic fibrosis population carrier screening: 2004 revision of American College of Medical Genetics mutation panel. Genet. Med. 6 (2004) 387-391
56. Lakhani V.T., You Y.N., and Wells S.A. The multiple endocrine neoplasia syndromes. Annu. Rev. Med. 58 (2007) 253-265
57. Scriver C.R., Hurtubise M., Konecki D., Phommarinh M., Prevost L., Erlandsen H., Stevens R., Waters P.J., Ryan S., McDonald D., et al. PAHdb 2003: what a locus-specific knowledgebase can do. Hum. Mutat. 21 (2003) 333-344
58. Bobadilla J.L., Macek Jr. M., Fine J.P., and Farrell P.M. Cystic fibrosis: a worldwide analysis of CFTR mutations-correlation with incidence data and application to screening. Hum. Mutat. 19 (2002) 575-606
59. Cohen J.C., Kiss R.S., Pertsemlidis A., Marcel Y.L., McPherson R., and Hobbs H.H. Multiple rare alleles contribute to low plasma levels of HDL cholesterol. Science 305 (2004) 869-872
60. Peralta V., and Cuesta M.J. How many and which are the psychopathological dimensions in schizophrenia? Issues influencing their ascertainment. Schizophr. Res. 49 (2001) 269-285
61. Cardno A.G., Jones L.A., Murphy K.C., Sanders R.D., Asherson P., Owen M.J., and McGuffin P. Dimensions of psychosis in affected sibling pairs. Schizophr. Bull. 25 (1999) 841-850
62. McGrath J.A., Nestadt G., Liang K.Y., Lasseter V.K., Wolyniec P.S., Fallin M.D., Thornquist M.H., Luke J.R., and Pulver A.E. Five latent factors underlying schizophrenia: analysis and relationship to illnesses in relatives. Schizophr. Bull. 30 (2004) 855-873
63. Schneider K. Clinical Psychopathology (transl. M.W. Hamilton) (1959), Grune & Stratton, New York
64. Loftus J., Delisi L.E., and Crow T.J. Factor structure and familiality of first-rank symptoms in sibling pairs with schizophrenia and schizoaffective disorder. Br. J. Psychiatry 177 (2000) 15-19
65. Cardno A.G., Sham P.C., Farmer A.E., Murray R.M., and McGuffin P. Heritability of Schneider's first-rank symptoms. Br. J. Psychiatry 180 (2002) 35-38
66. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., Brynjolfsson J., Gunnarsdottir S., Ivarsson O., Chou T.T., et al. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71 (2002) 877-892
67. Munafo M.R., Thiselton D.L., Clark T.G., and Flint J. Association of the NRG1 gene and schizophrenia: a meta-analysis. Mol. Psychiatry 11 (2006) 539-546
68. Zhang D., Sliwkowski M.X., Mark M., Frantz G., Akita R., Sun Y., Hillan K., Crowley C., Brush J., and Godowski P.J. Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Natl. Acad. Sci. USA 94 (1997) 9562-9567
69. Steinthorsdottir V., Stefansson H., Ghosh S., Birgisdottir B., Bjornsdottir S., Fasquel A.C., Olafsson O., Stefansson K., and Gulcher J.R. Multiple novel transcription initiation sites for NRG1. Gene 342 (2004) 97-105
70. Law A.J., Lipska B.K., Weickert C.S., Hyde T.M., Straub R.E., Hashimoto R., Harrison P.J., Kleinman J.E., and Weinberger D.R. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPs associated with the disease. Proc. Natl. Acad. Sci. USA 103 (2006) 6747-6752
71. Tan W., Wang Y., Gold B., Chen J., Dean M., Harrison P.J., Weinberger D.R., and Law A.J. Molecular cloning of a brain-specific, developmentally regulated neuregulin 1 (NRG1) isoform and identification of a functional promoter variant associated with schizophrenia. J. Biol. Chem. 282 (2007) 24343-24351
72. Carteron C., Ferrer-Montiel A., and Cabedo H. Characterization of a neural-specific splicing form of the human neuregulin 3 gene involved in oligodendrocyte survival. J. Cell Sci. 119 (2006) 898-909
73. Hobbs S.S., Coffing S.L., Le A.T., Cameron E.M., Williams E.E., Andrew M., Blommel E.N., Hammer R.P., Chang H., and Riese II D.J. Neuregulin isoforms exhibit distinct patterns of ErbB family receptor activation. Oncogene 21 (2002) 8442-8452
74. Falls D.L. Neuregulins: functions, forms, and signaling strategies. Exp. Cell Res. 284 (2003) 14-30
75. O'Tuathaigh C.M., Babovic D., O'Meara G., Clifford J.J., Croke D.T., and Waddington J.L. Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour. Neurosci. Biobehav. Rev. 31 (2007) 60-78
76. Shifman S., Johannesson M., Bronstein M., Chen S.X., Collier D.A., Craddock N.J., Kendler K.S., Li T., O'Donovan M., O'Neill F.A., et al. Genome-wide association identifies a common variant in the Reelin gene that increases the risk of schizophrenia only in women. PLoS Genet. 4 (2008) e28
77. Wang Y.C., Chen J.Y., Chen M.L., Chen C.H., Lai I.C., Chen T.T., Hong C.J., Tsai S.J., and Liou Y.J. Neuregulin 3 genetic variations and susceptibility to schizophrenia in a Chinese population. Biol. Psychiatry 64 (2008) 1093-1096