Interaction between variants in CLU and MS4A4E modulates Alzheimer's disease risk

Alzheimer's and Dementia

Volumn 12, Issue 2, 2016, Pages 121-129

  Ebbert, Mark T W ^a   Boehme, Kevin L ^a   Wadsworth, Mark E ^a   Staley, Lyndsay A ^a   Mukherjee, Shubhabrata ^b   Crane, Paul K ^b   Ridge, Perry G ^a   Kauwe, John S K ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

ADGC; ADNI; Alzheimer's disease; CD33; CLU; Epistasis; Meta analysis; MS4A4E

Indexed keywords

APOLIPOPROTEIN E4; CD33 ANTIGEN; CD33 PROTEIN, HUMAN; CLU PROTEIN, HUMAN; CLUSTERIN; MEMBRANE PROTEIN; MS4A4E PROTEIN, HUMAN;

ADULT; ALLELE; ALZHEIMER DISEASE; ARTICLE; CLU GENE; CONTROLLED STUDY; EPISTASIS; FEMALE; GENE; GENE FREQUENCY; GENE INTERACTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; MS4A4E GENE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; GENETIC PREDISPOSITION; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; META ANALYSIS; PROCEDURES; RISK FACTOR;

ALLELES; ALZHEIMER DISEASE; APOLIPOPROTEIN E4; CLUSTERIN; EPISTASIS, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MEMBRANE PROTEINS; RISK FACTORS; SIALIC ACID BINDING IG-LIKE LECTIN 3;

EID: 84957843348     PISSN: 15525260     EISSN: 15525279     Source Type: Journal    
DOI: 10.1016/j.jalz.2015.08.163     Document Type: Article

References (45)

1. B.D. James, S.E. Leurgans, L.E. Hebert, P.A. Scherr, K. Yaffe, and D.A. Bennett Contribution of Alzheimer disease to mortality in the United States Neurology 82 2014 1045 1050
2. P.G. Ridge, S. Mukherjee, P.K. Crane, J.S.K. Kauwe Alzheimer's Disease Genetics Consortium Alzheimer's disease: Analyzing the missing heritability PLoS One 8 2013 e79771
3. M.T.W. Ebbert, P.G. Ridge, A.R. Wilson, A.R. Sharp, M. Bailey, M.C. Norton, and et al. Population-based Analysis of Alzheimer's disease risk alleles implicates genetic interactions Biol Psychiatry 75 2014 732 737
4. K. Sleegers, K. Bettens, A. De Roeck, C.V. Cauwenberghe, E. Cuyvers, J. Verheijen, and et al. A 22-single nucleotide polymorphism Alzheimer risk score correlates with family history, onset age, and cerebrospinal fluid Aβ42 Alzheimers Dement 11 2015 1452 1460
5. J.M. Bullock, C. Medway, M. Cortina-Borja, J.C. Turton, J.A. Prince, C.A. Ibrahim-Verbaas, and et al. Discovery by the Epistasis Project of an epistatic interaction between the GSTM3 gene and the HHEX/IDE/KIF11 locus in the risk of Alzheimer's disease Neurobiol Aging 34 2013 1309.e1 1309.e7
6. O. Combarros, M. Cortina-Borja, A.D. Smith, and D.J. Lehmann Epistasis in sporadic Alzheimer's disease Neurobiol Aging 30 2009 1333 1349
7. J.S.K. Kauwe, S. Bertelsen, K. Mayo, C. Cruchaga, R. Abraham, P. Hollingworth, and et al. Suggestive synergy between genetic variants in TF and HFE as risk factors for Alzheimer's disease Am J Med Genet Part B Neuropsychiatr Genet 153B 2010 955 959
8. A.C. Naj, G. Jun, G.W. Beecham, L.S. Wang, B.N. Vardarajan, J. Buros, and et al. Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease Nat Genet 43 2011 436 441
9. D. Harold, R. Abraham, P. Hollingworth, R. Sims, A. Gerrish, M.L. Hamshere, and et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease Nat Genet 41 2009 1088 1093
10. S. Seshadri, A.L. Fitzpatrick, M.A. Ikram, A.L. DeStefano, V. Gudnason, M. Boada, et al. CHARGE Consortium, GERAD1 Consortium, EADI1 Consortium Genome-wide analysis of genetic loci associated with Alzheimer disease JAMA 303 2010 1832 1840
11. X. Hu, E. Pickering, Y.C. Liu, S. Hall, H. Fournier, E. Katz, et al. the Alzheimer's Disease Neuroimaging Initiative Meta-Analysis for genome-wide association study identifies multiple variants at the BIN1 locus associated with late-onset Alzheimer's disease PLoS One 6 2011 e16616
12. R.J. Guerreiro, J. Beck, J.R. Gibbs, I. Santana, M.N. Rossor, J.M. Schott, and et al. Genetic variability in CLU and its association with Alzheimer's disease PLoS One 5 2010 e9510
13. K. Bettens, N. Brouwers, H. Van Miegroet, A. Gil, S. Engelborghs, P.P. De Deyn, and et al. Follow-up study of susceptibility loci for Alzheimer's disease and onset age identified by genome-wide association J Alzheimers Dis 19 2010 1169 1175
14. L. Bertram, M.B. McQueen, K. Mullin, D. Blacker, and R.E. Tanzi Systematic meta-analyses of Alzheimer disease genetic association studies: The AlzGene database Nat Genet 39 2007 17 23
15. J.C. Lambert, C.A. Ibrahim-Verbaas, D. Harold, A.C. Naj, R. Sims, C. Bellenguez, et al. European Alzheimer's Disease Initiative (EADI) Genetic and Environmental Risk in Alzheimer's Disease (GERAD) Alzheimer's Disease Genetic Consortium (ADGC) Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease Nat Genet 45 2013 1452 1458
16. E.M. Bradshaw, L.B. Chibnik, B.T. Keenan, L. Ottoboni, T. Raj, A. Tang, et al. The Alzheimer Disease Neuroimaging Initiative CD33 Alzheimer's disease locus: Altered monocyte function and amyloid biology Nat Neurosci 16 2013 848 850
17. A. Griciuc, A. Serrano-Pozo, A.R. Parrado, A.N. Lesinski, C.N. Asselin, K. Mullin, and et al. Alzheimer's disease risk gene CD33 inhibits microglial uptake of amyloid beta Neuron 78 2013 631 643
18. C.M. Karch, A.T. Jeng, P. Nowotny, J. Cady, C. Cruchaga, and A.M. Goate Expression of novel Alzheimer's disease risk genes in control and Alzheimer's disease brains PLoS One 7 2012 e50976
19. T.M. Lancaster, L.M. Brindley, K.E. Tansey, R.C. Sims, K. Mantripragada, M.J. Owen, and et al. Alzheimer's disease risk variant in CLU is associated with neural inefficiency in healthy individuals Alzheimers Dement 11 2014 1144 1152
20. M.N. Braskie, N. Jahanshad, J.L. Stein, M. Barysheva, K.L. McMahon, G.I. de Zubicaray, and et al. Common Alzheimer's disease risk variant within the CLU gene affects white matter microstructure in young adults J Neurosci 31 2011 6764 6770
21. P. Hollingworth, D. Harold, R. Sims, A. Gerrish, J.-C. Lambert, M.M. Carrasquillo, et al. Alzheimer's Disease Neuroimaging Initiative CHARGE consortium EADI1 consortium Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease Nat Genet 43 2011 429 435
22. M.T. Ebbert, P.G. Ridge, and J.S. Kauwe Bridging the gap between statistical and biological epistasis in Alzheimer's disease Biomed Res Int 2015 2015 870123
23. K.L. Boehme, S. Mukherjee, P.K. Crane, and J.S.K. Kauwe ADGC 1000 Genomes combined data workflow Accessed October 12, 2015 Available at kauwelab.byu.edu/Portals/22/adgc-combined-1000G-09192014.pdf
24. J.C. Breitner, B.W. Wyse, J.C. Anthony, K.A. Welsh-Bohmer, D.C. Steffens, M.C. Norton, and et al. APOE-epsilon4 count predicts age when prevalence of AD increases, then declines: the Cache County Study Neurology 53 1999 321 331
25. S. Purcell, B. Neale, K. Todd-Brown, L. Thomas, M.A.R. Ferreira, D. Bender, and et al. PLINK: A tool set for whole-genome association and population-based linkage analyses Am J Hum Genet 81 2007 559 575
26. C.C. Chang, C.C. Chow, L.C. Tellier, S. Vattikuti, S.M. Purcell, and J.J. Lee Second-generation PLINK: Rising to the challenge of larger and richer datasets GigaScience 4 2015 7
27. J.E. Wigginton, D.J. Cutler, and G.R. Abecasis A note on exact tests of Hardy-Weinberg equilibrium Am J Hum Genet 76 2005 887 893
28. J. Graffelman, and V. Moreno The mid p-value in exact tests for Hardy-Weinberg equilibrium Stat Appl Genet Mol Biol 12 2013 433 448
29. R Development Core Team R: A language and environment for statistical computing 2011 R Foundation for Statistical Computing Vienna, Austria
30. C.J. Willer, Y. Li, and G.R. Abecasis METAL: Fast and efficient meta-analysis of genome wide association scans Bioinformatics 26 2010 2190 2191
31. M. Cortina-Borja, A.D. Smith, O. Combarros, and D. Lehmann The synergy factor: A statistic to measure interactions in complex diseases BMC Res Notes 2 2009 105
32. T. Lumley rmeta: Meta-analysis R package version 2.16 Accessed October 12, 2015 2012 Available at http://CRAN.R-project.org/package=rmeta
33. A.P. Boyle, E.L. Hong, M. Hariharan, Y. Cheng, M.A. Schaub, M. Kasowski, and et al. Annotation of functional variation in personal genomes using RegulomeDB Genome Res 22 2012 1790 1797
34. X. Chang, and K. Wang wANNOVAR: Annotating genetic variants for personal genomes via the web J Med Genet 49 2012 433 436
35. J.C. Barrett, B. Fry, J. Maller, and M.J. Daly Haploview: Analysis and visualization of LD and haplotype maps Bioinformatics 21 2005 263 265
36. Consortium T 1000 GP An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
37. NHLBI GO Exome sequencing project (ESP) Accessed October 12, 2015 Available at http://evs.gs.washington.edu/EVS/
38. J.M. Schwarz, C. Rödelsperger, M. Schuelke, and D. Seelow MutationTaster evaluates disease-causing potential of sequence alterations Nat Methods 7 2010 575 576
39. M.T. Ebbert, M.E. Wadsworth, K.L. Boehme, K.L. Hoyt, A.R. Sharp, B.D. O'Fallon, and et al. Variant Tool Chest: An improved tool to analyze and manipulate variant call format (VCF) files BMC Bioinformatics 15 2014 S12
40. T. Zeller, P. Wild, S. Szymczak, M. Rotival, A. Schillert, R. Castagne, and et al. Genetics and beyond - the transcriptome of human monocytes and disease susceptibility PLoS One 5 2010 e10693
41. T. Jonsson, J.K. Atwal, S. Steinberg, J. Snaedal, P.V. Jonsson, S. Bjornsson, and et al. A mutation in APP protects against Alzheimer's disease and age-related cognitive decline Nature 488 2012 96 99
42. R. Guerreiro, A. Wojtas, J. Bras, M. Carrasquillo, E. Rogaeva, E. Majounie, and et al. TREM2 variants in Alzheimer's disease N Engl J Med 368 2013 117 127
43. C. Sassi, J. Bras, J.R. Gibbs, D.G. Hernandez, M.K. Lupton, J. Powell, et al. UK Brain Expression Consortium Alzheimer's Research UK Consortium Rare coding variants in the phospholipase D3 gene confer risk for Alzheimer's disease Nature 505 2014 550 554
44. J.J. Yerbury, S. Poon, S. Meehan, B. Thompson, J.R. Kumita, C.M. Dobson, and et al. The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures FASEB J 21 2007 2312 2322
45. G. Jun, C.A. Ibrahim-Verbaas, M. Vronskaya, J.C. Lambert, J. Chung, A.C. Naj, and et al. A novel Alzheimer disease locus located near the gene encoding tau protein Mol Psychiatry 21 2016 108 117