A Likelihood Ratio-Based Mann-Whitney Approach Finds Novel Replicable Joint Gene Action for Type 2 Diabetes

Genetic Epidemiology

Volumn 36, Issue 6, 2012, Pages 583-593

  Lu, Qing ^a   Wei, Changshuai ^a   Ye, Chengyin ^a   Li, Ming ^a   Elston, Robert C ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Forward selection; Gene gene interaction; Genome wide search

Indexed keywords

ALLELE; ARTICLE; COMPUTER; GENE ACTIVITY; GENE FREQUENCY; GENE INTERACTION; GENE LOCUS; GENE REPLICATION; GENETIC ASSOCIATION; GENOTYPE; KERNEL METHOD; NON INSULIN DEPENDENT DIABETES MELLITUS; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC HYPERMUTATION;

ALGORITHMS; DIABETES MELLITUS, TYPE 2; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MODELS, STATISTICAL; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84865074859     PISSN: 07410395     EISSN: 10982272     Source Type: Journal    
DOI: 10.1002/gepi.21651     Document Type: Article

References (54)

1. Altshuler D, Hirschhorn JN, Klannemark M, Lindgren CM, Vohl MC, Nemesh J, Lane CR, Schaffner SF, Bolk S, Brewer C, Tuomi T, Gaudet D, Hudson TJ, Daly M, Groop L, Lander ES. 2000. The common PPARgamma Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes. Nat Genet 1:76-80.
2. Breiman L. 1996. Bagging predictors. Mach Learn 2:123-140.
3. Cordell HJ. 2009. Detecting gene-gene interactions that underlie human diseases. Nat Rev Genet 6:392-404.
4. Cornelis MC, Qi L, Zhang C, Kraft P, Manson J, Cai T, Hunter DJ, Hu FB. 2009. Joint effects of common genetic variants on the risk for type 2 diabetes in U.S. men and women of European ancestry. Ann Intern Med 8:541-550.
5. Culverhouse RC, Saccone NL, Stitzel JA, Wang JC, Steinbach JH, Goate AM, Schwantes-An TH, Grucza RA, Stevens VL, Bierut LJ. 2011. Uncovering hidden variance: pair-wise SNP analysis accounts for additional variance in nicotine dependence. Hum Genet 2:177-188.
6. DeLong ER, DeLong DM, Clarke-Pearson DL. 1988. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 3:837-845.
7. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, Moore JH, Nadeau JH. 2010. Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet 6:446-450.
8. Elston RC. 1981. Segregation analysis. Adv Hum Genet 11:63-120.
9. Frayling TM. 2007. Genome-wide association studies provide new insights into type 2 diabetes aetiology. Nat Rev Genet 9:657-662.
10. Gloyn AL, Weedon MN, Owen KR, Turner MJ, Knight BA, Hitman G, Walker M, Levy JC, Sampson M, Halford S, McCarthy MI, Hattersley AT, Frayling TM. 2003. Large-scale association studies of variants in genes encoding the pancreatic beta-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) confirm that the KCNJ11 E23K variant is associated with type 2 diabetes. Diabetes 2:568-572.
11. Goldstein DB. 2009. Common genetic variation and human traits. N Engl J Med 17:1696-1698.
12. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J, Helgason A, Stefansson H, Emilsson V, Helgadottir A, Styrkarsdottir U, Magnusson KP, Walters GB, Palsdottir E, Jonsdottir T, Gudmundsdottir T, Gylfason A, Saemundsdottir J, Wilensky RL, Reilly MP, Rader DJ, Bagger Y, Christiansen C, Gudnason V, Sigurdsson G, Thorsteinsdottir U, Gulcher JR, Kong A, Stefansson K. 2006. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 3:320-323.
13. Hardy J, Singleton A. 2009. Genomewide association studies and human disease. N Engl J Med 17:1759-1768.
14. Healy JA, Nilsson KR, Hohmeier HE, Berglund J, Davis J, Hoffman J, Kohler M, Li LS, Berggren PO, Newgard CB, Bennett V. 2010. Cholinergic augmentation of insulin release requires ankyrin-B. Sci Signal 113:ra19.
15. Hirschhorn JN. 2009. Genomewide association studies-illuminating biologic pathways. N Engl J Med 17:1699-1701.
16. Hirschhorn JN, Daly MJ. 2005. Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 2:95-108.
17. Kirchhoff K, Machicao F, Haupt A, Schafer SA, Tschritter O, Staiger H, Stefan N, Haring HU, Fritsche A. 2008. Polymorphisms in the TCF7L2, CDKAL1 and SLC30A8 genes are associated with impaired proinsulin conversion. Diabetologia 4:597-601.
18. Lehmann EL, D'Abrera HJM. 1975. Nonparametrics Statistical Methods Based on Ranks. San Francisco: Holden-Day.
19. Li M, Ye C, Fu W, Elston RC, Lu Q. 2011. Detecting genetic interactions for quantitative traits with U-statistics. Genet Epidemiol 6:457-468.
20. Li WD, Dong C, Li D, Garrigan C, Price RA. 2004. A quantitative trait locus influencing fasting plasma glucose in chromosome region 18q22-23. Diabetes 9:2487-2491.
21. Liu C, Ackerman HH, Carulli JP. 2011. A genome-wide screen of gene-gene interactions for rheumatoid arthritis susceptibility. Hum Genet 5:473-485.
22. Lu Q, Elston RC. 2008. Using the optimal receiver operating characteristic curve to design a predictive genetic test, exemplified with type 2 diabetes. Am J Hum Genet 3:641-651.
23. Lu Q, Obuchowski N, Won S, Zhu X, Elston RC. 2010. Using the optimal robust receiver operating characteristic (ROC) curve for predictive genetic tests. Biometrics 2:586-593.
24. Maher B. 2008. Personal genomes: the case of the missing heritability. Nature 7218:18-21.
25. Mann HB, Whitney DR. 1947. On a test of whether one of 2 random variables is stochastically larger than the other. Ann Math Stat 1:50-60.
26. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, McCarroll SA, Visscher PM. 2009. Finding the missing heritability of complex diseases. Nature 7265:747-753.
27. Marchini J, Donnelly P, Cardon LR. 2005. Genome-wide strategies for detecting multiple loci that influence complex diseases. Nat Genet 4:413-417.
28. Marchini J, Howie B, Myers S, McVean G, Donnelly P. 2007. A new multipoint method for genome-wide association studies by imputation of genotypes. Nat Genet 7:906-913.
29. McDonough CW, Bostrom MA, Lu L, Hicks PJ, Langefeld CD, Divers J, Mychaleckyj JC, Freedman BI, Bowden DW. 2009. Genetic analysis of diabetic nephropathy on chromosome 18 in African Americans: linkage analysis and dense SNP mapping. Hum Genet 6:805-817.
30. Mohler PJ, Le SS, Denjoy I, Lowe JS, Guicheney P, Caron L, Driskell IM, Schott JJ, Norris K, Leenhardt A, Kim RB, Escande D, Roden DM. 2007. Defining the cellular phenotype of "ankyrin-B syndrome" variants: human ANK2 variants associated with clinical phenotypes display a spectrum of activities in cardiomyocytes. Circulation 4:432-441.
31. Parzen E. 1962. Estimation of a probability density-function and mode. Ann Math Stat 3:1065-1076.
32. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 3:559-575.
33. Ritchie MD, Hahn LW, Roodi N, Bailey LR, Dupont WD, Parl FF, Moore JH. 2001. Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Hum Genet 1:138-147.
34. Rosenblatt M. 1956. Remarks on some nonparametric estimates of a density-function. Ann Math Stat 3:832-837.
35. Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN, Daly MJ, Hughes TE, Groop L, Altshuler D, Almgren P, Florez JC, Meyer J, Ardlie K, Bengtsson BK, Isomaa B, Lettre G, Lindblad U, Lyon HN, Melander O, Newton-Cheh C, Nilsson P, Orho-Melander M, Rastam L, Speliotes EK, Taskinen MR, Tuomi T, Guiducci C, Berglund A, Carlson J, Gianniny L, Hackett R, Hall L, Holmkvist J, Laurila E, Sjogren M, Sterner M, Surti A, Svensson M, Svensson M, Tewhey R, Blumenstiel B, Parkin M, Defelice M, Barry R, Brodeur W, Camarata J, Chia N, Fava M, Gibbons J, Handsaker B, Healy C, Nguyen K, Gates C, Sougnez C, Gage D, Nizzari M, Gabriel SB, Chirn GW, Ma Q, Parikh H, Richardson D, Ricke D, Purcell S. 2007. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 5829:1331-1336.
36. Schaid DJ, McDonnell SK, Hebbring SJ, Cunningham JM, Thibodeau SN. 2005. Nonparametric tests of association of multiple genes with human disease. Am J Hum Genet 5:780-793.
37. Schwarz DF, Konig IR, Ziegler A. 2010. On safari to Random Jungle: a fast implementation of Random Forests for high-dimensional data. Bioinformatics 14:1752-1758.
38. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. 2007. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 5829:1341-1345.
39. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, Boutin P, Vincent D, Belisle A, Hadjadj S, Balkau B, Heude B, Charpentier G, Hudson TJ, Montpetit A, Pshezhetsky AV, Prentki M, Posner BI, Balding DJ, Meyre D, Polychronakos C, Froguel P. 2007. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 7130:881-885.
40. Steinthorsdottir V, Thorleifsson G, Reynisdottir I, Benediktsson R, Jonsdottir T, Walters GB, Styrkarsdottir U, Gretarsdottir S, Emilsson V, Ghosh S, Baker A, Snorradottir S, Bjarnason H, Ng MC, Hansen T, Bagger Y, Wilensky RL, Reilly MP, Adeyemo A, Chen Y, Zhou J, Gudnason V, Chen G, Huang H, Lashley K, Doumatey A, So WY, Ma RC, Andersen G, Borch-Johnsen K, Jorgensen T, van Vliet-Ostaptchouk JV, Hofker MH, Wijmenga C, Christiansen C, Rader DJ, Rotimi C, Gurney M, Chan JC, Pedersen O, Sigurdsson G, Gulcher JR, Thorsteinsdottir U, Kong A, Stefansson K. 2007. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat Genet 6:770-775.
41. Tiwari HK, Elston RC. 1998. Restrictions on components of variance for epistatic models. Theor Popul Biol 2:161-174.
42. Voight BF, Scott LJ, Steinthorsdottir V, Morris AP, Dina C, Welch RP, Zeggini E, Huth C, Aulchenko YS, Thorleifsson G, McCulloch LJ, Ferreira T, Grallert H, Amin N, Wu G, Willer CJ, Raychaudhuri S, McCarroll SA, Langenberg C, Hofmann OM, Dupuis J, Qi L, Segre AV, van HM, Navarro P, Ardlie K, Balkau B, Benediktsson R, Bennett AJ, Blagieva R, Boerwinkle E, Bonnycastle LL, Bengtsson BK, Bravenboer B, Bumpstead S, Burtt NP, Charpentier G, Chines PS, Cornelis M, Couper DJ, Crawford G, Doney AS, Elliott KS, Elliott AL, Erdos MR, Fox CS, Franklin CS, Ganser M, Gieger C, Grarup N, Green T, Griffin S, Groves CJ, Guiducci C, Hadjadj S, Hassanali N, Herder C, Isomaa B, Jackson AU, Johnson PR, Jorgensen T, Kao WH, Klopp N, Kong A, Kraft P, Kuusisto J, Lauritzen T, Li M, Lieverse A, Lindgren CM, Lyssenko V, Marre M, Meitinger T, Midthjell K, Morken MA, Narisu N, Nilsson P, Owen KR, Payne F, Perry JR, Petersen AK, Platou C, Proenca C, Prokopenko I, Rathmann W, Rayner NW, Robertson NR, Rocheleau G, Roden M, Sampson MJ, Saxena R, Shields BM, Shrader P, Sigurdsson G, Sparso T, Strassburger K, Stringham HM, Sun Q, Swift AJ, Thorand B, Tichet J, Tuomi T, van D am RM, van H aeften TW, van HT, van Vliet-Ostaptchouk JV, Walters GB, Weedon MN, Wijmenga C, Witteman J, Bergman RN, Cauchi S, Collins FS, Gloyn AL, Gyllensten U, Hansen T, Hide WA, Hitman GA, Hofman A, Hunter DJ, Hveem K, Laakso M, Mohlke KL, Morris AD, Palmer CN, Pramstaller PP, Rudan I, Sijbrands E, Stein LD, Tuomilehto J, Uitterlinden A, Walker M, Wareham NJ, Watanabe RM, Abecasis GR, Boehm BO, Campbell H, Daly MJ, Hattersley AT, Hu FB, Meigs JB, Pankow JS, Pedersen O, Wichmann HE, Barroso I, Florez JC, Frayling TM, Groop L, Sladek R, Thorsteinsdottir U, Wilson JF, Illig T, Froguel P, van Duijn CM, Stefansson K, Altshuler D, Boehnke M, McCarthy MI. 2010. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat Genet 7:579-589.
43. Wan X, Yang C, Yang Q, Xue H, Fan X, Tang NL, Yu W. 2010. BOOST: a fast approach to detecting gene-gene interactions in genome-wide case-control studies. Am J Hum Genet 3:325-340.
44. Wang X, Elston RC, Zhu X. 2010. The meaning of interaction. Hum Hered 4:269-277.
45. Wei Z, Li M, Rebbeck T, Li H. 2008. U-statistics-based tests for multiple genes in genetic association studies. Ann Hum Genet 6:821-833.
46. Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 7145:661-678.
47. Wilcoxon F. 1945. Individual comparisons by ranking methods. Biometr Bull 6:80-83.
48. Woolf B. 1955. On estimating the relation between blood group and disease. Ann Hum Genet 4:251-253.
49. Wu MC, Kraft P, Epstein MP, Taylor DM, Chanock SJ, Hunter DJ, Lin X. 2010. Powerful SNP-set analysis for case-control genome-wide association studies. Am J Hum Genet 6:929-942.
50. Ye C, Cui Y, Wei C, Elston RC, Zhu J, Lu Q. 2011. A non-parametric method for building predictive genetic tests on high-dimensional data. Hum Hered 3:161-170.
51. Yung LS, Yang C, Wan X, Yu W. 2011. GBOOST: a GPU-based tool for detecting gene-gene interactions in genome-wide case control studies. Bioinformatics 9:1309-1310.
52. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, Hu T, de Bakker PI, Abecasis GR, Almgren P, Andersen G, Ardlie K, Bostrom KB, Bergman RN, Bonnycastle LL, Borch-Johnsen K, Burtt NP, Chen H, Chines PS, Daly MJ, Deodhar P, Ding CJ, Doney AS, Duren WL, Elliott KS, Erdos MR, Frayling TM, Freathy RM, Gianniny L, Grallert H, Grarup N, Groves CJ, Guiducci C, Hansen T, Herder C, Hitman GA, Hughes TE, Isomaa B, Jackson AU, Jorgensen T, Kong A, Kubalanza K, Kuruvilla FG, Kuusisto J, Langenberg C, Lango H, Lauritzen T, Li Y, Lindgren CM, Lyssenko V, Marvelle AF, Meisinger C, Midthjell K, Mohlke KL, Morken MA, Morris AD, Narisu N, Nilsson P, Owen KR, Palmer CN, Payne F, Perry JR, Pettersen E, Platou C, Prokopenko I, Qi L, Qin L, Rayner NW, Rees M, Roix JJ, Sandbaek A, Shields B, Sjogren M, Steinthorsdottir V, Stringham HM, Swift AJ, Thorleifsson G, Thorsteinsdottir U, Timpson NJ, Tuomi T, Tuomilehto J, Walker M, Watanabe RM, Weedon MN, Willer CJ, Illig T, Hveem K, Hu FB, Laakso M, Stefansson K, Pedersen O, Wareham NJ, Barroso I, Hattersley AT, Collins FS, Groop L, McCarthy MI, Boehnke M, Altshuler D. 2008. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 5:638-645.
53. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, Timpson NJ, Perry JR, Rayner NW, Freathy RM, Barrett JC, Shields B, Morris AP, Ellard S, Groves CJ, Harries LW, Marchini JL, Owen KR, Knight B, Cardon LR, Walker M, Hitman GA, Morris AD, Doney AS, McCarthy MI, Hattersley AT. 2007. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 5829:1336-1341.
54. Zhang Y, Liu JS. 2007. Bayesian inference of epistatic interactions in case-control studies. Nat Genet 9:1167-1173.