Brain expression genome-wide association study (eGWAS) identifies human disease-associated variants

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Zou, Fanggeng ^a   Chai, High Seng ^b   Younkin, Curtis S ^a   Allen, Mariet ^a   Crook, Julia ^c   Pankratz, V Shane ^b   Carrasquillo, Minerva M ^a   Rowley, Christopher N ^a   Nair, Asha A ^b   Middha, Sumit ^b   Maharjan, Sooraj ^b   Nguyen, Thuy ^a   Ma, Li ^a   Malphrus, Kimberly G ^a   Palusak, Ryan ^a   Lincoln, Sarah ^a   Bisceglio, Gina ^a   Georgescu, Constantin ^a   Kouri, Naomi ^a   Kolbert, Christopher P ^b   Jen, Jin ^b   Haines, Jonathan L ^d   Mayeux, Richard ^e   Pericak Vance, Margaret A ^f   Farrer, Lindsay A ^g   Schellenberg, Gerard D ^h   Petersen, Ronald C ^b   Graff Radford, Neill R ^c   Dickson, Dennis W ^a   Younkin, Steven G ^a   Ertekin Taner, Nilüfer ^a,c   more..

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c MAYO CLINIC   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Taub Institute for Research on Alzheimer's Disease and the Aging Brain and the Gertrude H Sergievsky Center   (United States)

^f UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^g BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENETIC ASSOCIATION; GENETIC RISK; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; INSULIN DEPENDENT DIABETES MELLITUS; PARKINSON DISEASE; PROGRESSIVE SUPRANUCLEAR PALSY; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; TEMPORAL CORTEX; ULCERATIVE COLITIS; AUTOPSY; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; META ANALYSIS; METABOLISM; TEMPORAL LOBE;

RNA;

ALZHEIMER DISEASE; AUTOPSY; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA; TEMPORAL LOBE;

EID: 84864066707     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002707     Document Type: Article

References (61)

1. Ertekin-Taner N, (2011) Gene expression endophenotypes: a novel approach for gene discovery in Alzheimer's disease. Mol Neurodegener 6: 31.
2. Murphy A, Chu JH, Xu M, Carey VJ, Lazarus R, et al. (2010) Mapping of numerous disease-associated expression polymorphisms in primary peripheral blood CD4+ lymphocytes. Hum Mol Genet 19: 4745-4757.
3. Nicolae DL, Gamazon E, Zhang W, Duan S, Dolan ME, et al. (2010) Trait-associated SNPs are more likely to be eQTLs: annotation to enhance discovery from GWAS. PLoS Genet 6: e1000888 doi:10.1371/journal.pgen.1000888.
4. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, et al. (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422: 297-302.
5. Cheung VG, Conlin LK, Weber TM, Arcaro M, Jen KY, et al. (2003) Natural variation in human gene expression assessed in lymphoblastoid cells. Nat Genet 33: 422-425.
6. Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, et al. (2004) Genetic analysis of genome-wide variation in human gene expression. Nature 430: 743-747.
7. Monks SA, Leonardson A, Zhu H, Cundiff P, Pietrusiak P, et al. (2004) Genetic inheritance of gene expression in human cell lines. Am J Hum Genet 75: 1094-1105.
8. Cheung VG, Spielman RS, Ewens KG, Weber TM, Morley M, et al. (2005) Mapping determinants of human gene expression by regional and genome-wide association. Nature 437: 1365-1369.
9. Stranger BE, Forrest MS, Clark AG, Minichiello MJ, Deutsch S, et al. (2005) Genome-wide associations of gene expression variation in humans. PLoS Genet 1: e78 doi:10.1371/journal.pgen.0010078.
10. Stranger BE, Nica AC, Forrest MS, Dimas A, Bird CP, et al. (2007) Population genomics of human gene expression. Nat Genet 39: 1217-1224.
11. Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, et al. (2007) Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315: 848-853.
12. Dixon AL, Liang L, Moffatt MF, Chen W, Heath S, et al. (2007) A genome-wide association study of global gene expression. Nat Genet 39: 1202-1207.
13. Dausset J, Cann H, Cohen D, Lathrop M, Lalouel JM, et al. (1990) Centre d'etude du polymorphisme humain (CEPH): collaborative genetic mapping of the human genome. Genomics 6: 575-577.
14. (2005) A haplotype map of the human genome. Nature 437: 1299-1320.
15. Stranger BE, Forrest MS, Clark AG, Minichiello MJ, Deutsch S, et al. (2005) Genome-wide associations of gene expression variation in humans. PLoS Genet 1: e78 doi:10.1371/journal.pgen.0010078.
16. Goring HH, Curran JE, Johnson MP, Dyer TD, Charlesworth J, et al. (2007) Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nat Genet 39: 1208-1216.
17. Rotival M, Zeller T, Wild PS, Maouche S, Szymczak S, et al. (2011) Integrating genome-wide genetic variations and monocyte expression data reveals trans-regulated gene modules in humans. PLoS Genet 7: e1002367 doi:10.1371/journal.pgen.1002367.
18. Dimas AS, Deutsch S, Stranger BE, Montgomery SB, Borel C, et al. (2009) Common regulatory variation impacts gene expression in a cell type-dependent manner. Science 325: 1246-1250.
19. Ding J, Gudjonsson JE, Liang L, Stuart PE, Li Y, et al. (2010) Gene expression in skin and lymphoblastoid cells: Refined statistical method reveals extensive overlap in cis-eQTL signals. Am J Hum Genet 87: 779-789.
20. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, et al. (2008) Genetics of gene expression and its effect on disease. Nature 452: 423-428.
21. Zhong H, Beaulaurier J, Lum PY, Molony C, Yang X, et al. (2010) Liver and adipose expression associated SNPs are enriched for association to type 2 diabetes. PLoS Genet 6: e1000932 doi:10.1371/journal.pgen.1000932.
22. Grundberg E, Adoue V, Kwan T, Ge B, Duan QL, et al. (2011) Global analysis of the impact of environmental perturbation on cis-regulation of gene expression. PLoS Genet 7: e1001279 doi:10.1371/journal.ppat.1001279.
23. Schadt EE, Molony C, Chudin E, Hao K, Yang X, et al. (2008) Mapping the genetic architecture of gene expression in human liver. PLoS Biol 6: e107 doi:10.1371/journal.pbio.0060107.
24. Myers AJ, Gibbs JR, Webster JA, Rohrer K, Zhao A, et al. (2007) A survey of genetic human cortical gene expression. Nat Genet 39: 1494-1499.
25. Webster JA, Gibbs JR, Clarke J, Ray M, Zhang W, et al. (2009) Genetic control of human brain transcript expression in Alzheimer disease. Am J Hum Genet 84: 445-458.
26. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, et al. (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A 106: 9362-9367.
27. Hoglinger GU, Melhem NM, Dickson DW, Sleiman PM, Wang LS, et al. (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet 43: 699-705.
28. Naj AC, Jun G, Beecham GW, Wang LS, Vardarajan BN, et al. (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat Genet 43: 436-441.
29. Carrasquillo MM, Zou F, Pankratz VS, Wilcox SL, Ma L, et al. (2009) Genetic variation in PCDH11X is associated with susceptibility to late-onset Alzheimer's disease. Nat Genet 41: 192-198.
30. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445.
31. Barry WT, Kernagis DN, Dressman HK, Griffis RJ, Hunter JD, et al. (2010) Intratumor heterogeneity and precision of microarray-based predictors of breast cancer biology and clinical outcome. J Clin Oncol 28: 2198-2206.
32. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, et al. (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41: 1308-1312.
33. Fuchs J, Nilsson C, Kachergus J, Munz M, Larsson EM, et al. (2007) Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication. Neurology 68: 916-922.
34. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, et al. (2010) Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 74: 97-109.
35. Han JW, Zheng HF, Cui Y, Sun LD, Ye DQ, et al. (2009) Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet 41: 1234-1237.
36. Graham RR, Kozyrev SV, Baechler EC, Reddy MV, Plenge RM, et al. (2006) A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat Genet 38: 550-555.
37. Graham RR, Kyogoku C, Sigurdsson S, Vlasova IA, Davies LR, et al. (2007) Three functional variants of IFN regulatory factor 5 (IRF5) define risk and protective haplotypes for human lupus. Proc Natl Acad Sci U S A 104: 6758-6763.
38. Anderson CA, Boucher G, Lees CW, Franke A, D'Amato M, et al. (2011) Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 43: 246-252.
39. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A, et al. (2009) Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat Genet.
40. Lambert JC, Heath S, Even G, Campion D, Sleegers K, et al. (2009) Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 41: 1094-1099.
41. Reiman EM, Webster JA, Myers AJ, Hardy J, Dunckley T, et al. (2007) GAB2 alleles modify Alzheimer's risk in APOE epsilon4 carriers. Neuron 54: 713-720.
42. van Es MA, Veldink JH, Saris CG, Blauw HM, van Vught PW, et al. (2009) Genome-wide association study identifies 19p13.3 (UNC13A) and 9p21.2 as susceptibility loci for sporadic amyotrophic lateral sclerosis. Nat Genet 41: 1083-1087.
43. Laaksovirta H, Peuralinna T, Schymick JC, Scholz SW, Lai SL, et al. (2010) Chromosome 9p21 in amyotrophic lateral sclerosis in Finland: a genome-wide association study. Lancet Neurol 9: 978-985.
44. Dejesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, et al. (2011) Expanded GGGGCC Hexanucleotide Repeat in Noncoding Region of C9ORF72 Causes Chromosome 9p-Linked FTD and ALS. Neuron 72: 245-256.
45. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, et al. (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72: 257-268.
46. Lee W, Glaeser H, Smith LH, Roberts RL, Moeckel GW, et al. (2005) Polymorphisms in human organic anion-transporting polypeptide 1A2 (OATP1A2): implications for altered drug disposition and central nervous system drug entry. J Biol Chem 280: 9610-9617.
47. Hollingworth P, Harold D, Sims R, Gerrish A, Lambert JC, et al. (2011) Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nat Genet 43: 429-435.
48. Seshadri S, Fitzpatrick AL, Ikram MA, DeStefano AL, Gudnason V, et al. (2010) Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA 303: 1832-1840.
49. Allen M, Zou F, Chai HS, Younkin CS, Crook J, et al. (2012) Novel late-onset Alzheimer's disease loci variants associate with brain gene expression. Neurology in-press.
50. Atz M, Walsh D, Cartagena P, Li J, Evans S, et al. (2007) Methodological considerations for gene expression profiling of human brain. J Neurosci Methods 163: 295-309.
51. Braak H, Braak E, (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 82: 239-259.
52. Caffrey TM, Joachim C, Paracchini S, Esiri MM, Wade-Martins R, (2006) Haplotype-specific expression of exon 10 at the human MAPT locus. Hum Mol Genet 15: 3529-3537.
53. Caffrey TM, Joachim C, Wade-Martins R, (2008) Haplotype-specific expression of the N-terminal exons 2 and 3 at the human MAPT locus. Neurobiol Aging 29: 1923-1929.
54. Myers AJ, Pittman AM, Zhao AS, Rohrer K, Kaleem M, et al. (2007) The MAPT H1c risk haplotype is associated with increased expression of tau and especially of 4 repeat containing transcripts. Neurobiol Dis 25: 561-570.
55. McKhann G, Drachman D, Folstein M, Katzman R, Price D, et al. (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34: 939-944.
56. Du P, Kibbe WA, Lin SM, (2008) lumi: a pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548.
57. Lin SM, Du P, Huber W, Kibbe WA, (2008) Model-based variance-stabilizing transformation for Illumina microarray data. Nucleic Acids Res 36: e11.
58. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575.
59. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904-909.
60. Westfall PH, Zaykin DV, Young SS, (2002) Multiple tests for genetic effects in association studies. Methods Mol Biol 184: 143-168.
61. Willer CJ, Li Y, Abecasis GR, (2010) METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26: 2190-2191.