Meta-Analysis Identifies Gene-by-Environment Interactions as Demonstrated in a Study of 4,965 Mice

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Kang, Eun Yong ^a   Han, Buhm ^b,c,d   Furlotte, Nicholas ^a   Joo, Jong Wha J ^e   Shih, Diana ^e   Davis, Richard C ^e   Lusis, Aldons J ^e,f   Eskin, Eleazar ^a,f  

^a Department of Civil and Environmental Engineering   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c LABORATORY FOR MOLECULAR MEDICINE   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL;

ARTICLE; ENVIRONMENTAL FACTOR; GENE IDENTIFICATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC MODEL; GENOME; GENOTYPE ENVIRONMENT INTERACTION; INTERMETHOD COMPARISON; META ANALYSIS; MOUSE; NONHUMAN;

ANIMALS; CHOLESTEROL, HDL; ENVIRONMENT; GENE-ENVIRONMENT INTERACTION; GENOME; MICE; MODELS, THEORETICAL; QUANTITATIVE TRAIT LOCI;

EID: 84896739351     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004022     Document Type: Article

References (74)

1. Gerke J, Lorenz K, Ramnarine S, Cohen B, (2010) Gene-environment interactions at nu- cleotide resolution. PLoS Genet 6: e1001144.
2. Murea M, Ma L, Freedman BI, (2012) Genetic and environmental factors associated with type 2 diabetes and diabetic vascular complications. Rev Diabet Stud 9: 6-22.
3. Smith EN, Kruglyak L, (2008) Gene-environment interaction in yeast gene expression. PLoS Biol 6: e83.
4. Talmud PJ, (2007) Gene-environment interaction and its impact on coronary heart disease risk. Nutr Metab Cardiovasc Dis 17: 148-52.
5. Forsyth JK, Ellman LM, Tanskanen A, Mustonen U, Huttunen MO, et al. (2012) Genetic risk for schizophrenia, obstetric complications, and adolescent school outcome: Evidence for gene-environment interaction. Schizophr Bull 39: 1067-76.
6. Orozco LD, Bennett BJ, Farber CR, Ghazalpour A, Pan C, et al. (2012) Unraveling inammatory responses using systems genetics and gene-environment interactions in macrophages. Cell 151: 658-70.
7. Dai X, Wu C, He Y, Gui L, Zhou L, et al. (2013) A genome-wide association study for serum bilirubin levels and gene-environment interaction in a chinese population. Genet Epidemiol 37: 293-300.
8. Patel CJ, Chen R, Kodama K, Ioannidis JPA, Butte AJ, (2013) Systematic identification of interaction effects between genome- and environment-wide associations in type 2 diabetes mellitus. Hum Genet 132: 495-508.
9. Wu C, Kraft P, Zhai K, Chang J, Wang Z, et al. (2012) Genome-wide association analyses of esophageal squamous cell carcinoma in chinese identify multiple susceptibility loci and gene-environment interactions. Nat Genet 44: 1090-7.
10. Ma J, Xiao F, Xiong M, Andrew AS, Brenner H, et al. (2012) Natural and orthogonal interaction framework for modeling gene-environment interactions with application to lung cancer. Hum Hered 73: 185-94.
11. Gao J, Nalls MA, Shi M, Joubert BR, Hernandez DG, et al. (2012) An exploratory analysis on gene-environment interactions for parkinson disease. Neurobiol Aging 33: 2528.e1-6.
12. Wei S, Wang LEE, McHugh MK, Han Y, Xiong M, et al. (2012) Genome-wide gene- environment interaction analysis for asbestos exposure in lung cancer susceptibility. Carcinogenesis 33: 1531-7.
13. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics 38: 904.
14. Devlin B, Roeder K, Wasserman L, (2001) Genomic control, a new approach to genetic- based association studies. Theor Popul Biol 60: 155-66.
15. Furlotte NA, Kang EY, Van Nas A, Farber CR, Lusis AJ, et al. (2012) Increasing asso- ciation mapping power and resolution in mouse genetic studies through the use of meta- analysis for structured populations. Genetics 191: 959-67.
16. Han B, Eskin E, (2012) Interpreting meta-analyses of genome-wide association studies. PLoS Genet 8: e1002555.
17. Flint J, Eskin E, (2012) Genome-wide association studies in mice. Nature Reviews Genetics 13: 807.
18. Bennett BJ, Farber CR, Orozco L, Kang HM, Ghazalpour A, et al. (2010) A high- resolution association mapping panel for the dissection of complex traits in mice. Genome Res 20: 281-90.
19. Ghazalpour A, Rau CD, Farber CR, Bennett BJ, Orozco LD, et al. (2012) Hybrid mouse diversity panel: a panel of inbred mouse strains suitable for analysis of complex genetic traits. Mamm Genome 23: 680-92.
20. Valdar W, Solberg LC, Gauguier D, Burnett S, Klenerman P, et al. (2006) Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat Genet 38: 879-87.
21. Yalcin B, Nicod J, Bhomra A, Davidson S, Cleak J, et al. (2010) Commercially available outbred mice for genome-wide association studies. PLoS Genet 6: e1001085.
22. Aylor DL, Valdar W, Foulds-Mathes W, Buus RJ, Verdugo RA, et al. (2011) Genetic analysis of complex traits in the emerging collaborative cross. Genome Res 21: 1213-22.
23. Warden CH, Hedrick CC, Qiao JH, Castellani LW, Lusis AJ, (1993) Atherosclerosis in transgenic mice overexpressing apolipoprotein a-ii. Science 261: 469-72.
24. DerSimonian R, Laird N, (1986) Meta-analysis in clinical trials. Control Clin Trials 7: 177-88.
25. Cochran WG (2009) The Combination of Estimates from Different Experiments. doi: 10.2307/3001666.
26. Higgins JPT, Thompson SG, (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539-58.
27. Niswender CM, Willis BS, Wallen A, Sweet IR, Jetton TL, et al. (2005) Cre recombinase- dependent expression of a constitutively active mutant allele of the catalytic subunit of protein kinase a. Genesis 43: 109-19.
28. Manning AK, LaValley M, Liu CTT, Rice K, An P, et al. (2011) Meta-analysis of gene- environment interaction: joint estimation of snp and snp×environment regression coeffi- cients. Genetic Epidemiology 35: 11.
29. Kirby A, Kang HM, Wade CM, Cotsapas C, Kostem E, et al. (2010) Fine mapping in 94 inbred mouse strains using a high-density haplotype resource. Genetics 185: 1081-95.
30. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, et al. (2004) The collaborative cross, a community resource for the genetic analysis of complex traits. Nat Genet 36: 1133-7.
31. Ioannidis JPA, Patsopoulos NA, Evangelou E, (2007) Heterogeneity in meta-analyses of genome-wide association investigations. PLoS One 2: e841.
32. Ioannidis JPA, Patsopoulos NA, Evangelou E, (2007) Uncertainty in heterogeneity esti- mates in meta-analyses. BMJ 335: 914-6.
33. Han B, Eskin E, (2011) Random-effects model aimed at discovering associations in meta- analysis of genome-wide association studies. Am J Hum Genet 88: 586-98.
34. Hardy RJ, Thompson SG, (1996) A likelihood approach to meta-analysis with random effects. Stat Med 15: 619-29.
35. Lin DYY, Sullivan PF, (2009) Meta-analysis of genome-wide association studies with over- lapping subjects. Am J Hum Genet 85: 862-72.
36. Devlin B, Roeder K, Bacanu SA, (2001) Unbiased methods for population-based association studies. Genet Epidemiol 21: 273-84.
37. Voight BF, Pritchard JK, (2005) Confounding from cryptic relatedness in case-control association studies. PLoS Genet 1: e32.
38. Lange K, (2002) Mathematical and statistical methods for genetic analysis. Springer Verlag.
39. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, et al. (2006) A unified mixed- model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38: 203-8.
40. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics 178: 1709.
41. Lippert C, Quon G, Kang EY, Kadie CM, Listgarten J, et al. (2013) The benefits of selecting phenotype-specific variants for applications of mixed models in genomics. Scientific Reports 3: 1815.
42. Listgarten J, Lippert C, Kang EY, Xiang J, Kadie CM, et al. (2013) A powerful and efficient set test for genetic markers that handles confounders. Bioinformatics 29: 1526-1533.
43. Stephens M, Balding DJ, (2009) Bayesian statistical methods for genetic association stud- ies. Nat Rev Genet 10: 681-90.
44. Parks BW, Nam E, Org E, Kostem E, Norheim F, et al. (2013) Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab 17: 141-52.
45. Davis RC, van Nas A, Castellani LW, Zhao Y, Zhou Z, et al. (2012) Systems genetics of susceptibility to obesity-induced diabetes in mice. Physiol Genomics 44: 1-13.
46. Wang S, Yehya N, Schadt E, Wang H, Drake T, et al. (2006) Genetic and genomic analysis of a fat mass trait with complex inheritance reveals marked sex specificity. PLoS genetics 2: e15.
47. van Nas A, Ingram-Drake L, Sinsheimer JS, Wang SS, Schadt EE, et al. (2010) Expression quantitative trait loci: replication, tissue- and sex-specificity in mice. Genetics 185: 1059-68.
48. van den Maagdenberg AM, Hofker MH, Krimpenfort PJ, de Bruijn I, van Vlijmen B, et al. (1993) Transgenic mice carrying the apolipoprotein e3-leiden gene exhibit hyperlipopro- teinemia. J Biol Chem 268: 10540-5.
49. Jiang XC, Agellon LB, Walsh A, Breslow JL, Tall A, (1992) Dietary cholesterol increases transcription of the human cholesteryl ester transfer protein gene in transgenic mice. dependence on natural anking sequences. J Clin Invest 90: 1290-5.
50. Takasuga S, Horie Y, Sasaki J, Sun-Wada GHH, Kawamura N, et al. (2013) Critical roles of type iii phosphatidylinositol phosphate kinase in murine embryonic visceral endoderm and adult intestine. Proc Natl Acad Sci U S A 110: 1726-31.
51. He C, Bassik MC, Moresi V, Sun K, Wei Y, et al. (2012) Exercise-induced bcl2-regulated autophagy is required for muscle glucose homeostasis. Nature 481: 511-5.
52. Plump AS, Azrolan N, Odaka H, Wu L, Jiang X, et al. (1997) Apoa-i knockout mice: characterization of hdl metabolism in homozygotes and identification of a post-rna mechanism of apoa-i up-regulation in heterozygotes. J Lipid Res 38: 1033-47.
53. Liegel R, Chang B, Dubielzig R, Sidjanin DJ, (2011) Blind sterile 2 (bs2), a hypomorphic mutation in agps, results in cataracts and male sterility in mice. Mol Genet Metab 103: 51-9.
54. Hofmann JJ, Zovein AC, Koh H, Radtke F, Weinmaster G, et al. (2010) Jagged1 in the portal vein mesenchyme regulates intrahepatic bile duct development: insights into alagille syndrome. Development 137: 4061-72.
55. Farese RV, Sajan MP, Yang H, Li P, Mastorides S, et al. (2007) Muscle-specific knockout of pkc-lambda impairs glucose transport and induces metabolic and diabetic syndromes. J Clin Invest 117: 2289-301.
56. Qiao JH, Tripathi J, Mishra NK, Cai Y, Tripathi S, et al. (1997) Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am J Pathol 150: 1687-99.
57. Stanford KI, Wang L, Castagnola J, Song D, Bishop JR, et al. (2010) Heparan sulfate 2-o-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem 285: 286-94.
58. Morgan H, Beck T, Blake A, Gates H, Adams N, et al. (2010) Europhenome: a repository for high-throughput mouse phenotyping data. Nucleic Acids Res 38: D577-85.
59. Leshan RL, Greenwald-Yarnell M, Patterson CM, Gonzalez IE, Myers MG, (2012) Leptin action through hypothalamic nitric oxide synthase-1-expressing neurons controls energy balance. Nat Med 18: 820-3.
60. Nakata S, Tsutsui M, Shimokawa H, Suda O, Morishita T, et al. (2008) Spontaneous myocardial infarction in mice lacking all nitric oxide synthase isoforms. Circulation 117: 2211-23.
61. Li LO, Ellis JM, Paich HA, Wang S, Gong N, et al. (2009) Liver-specific loss of long chain acyl-coa synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J Biol Chem 284: 27816-26.
62. Nishina PM, Naggert JK, Verstuyft J, Paigen B, (1994) Atherosclerosis in genetically obese mice: the mutants obese, diabetes, fat, tubby, and lethal yellow. Metabolism 43: 554-8.
63. Ciraolo E, Iezzi M, Marone R, Marengo S, Curcio C, et al. (2008) Phosphoinositide 3- kinase p110beta activity: key role in metabolism and mammary gland cancer but not development. Sci Signal 1: ra3.
64. Gupta S, Pablo AM, Jiang Xc, Wang N, Tall AR, et al. (1997) Ifn-gamma potentiates atherosclerosis in apoe knock-out mice. J Clin Invest 99: 2752-61.
65. Kim I, Ahn SHH, Inagaki T, Choi M, Ito S, et al. (2007) Differential regulation of bile acid homeostasis by the farnesoid x receptor in liver and intestine. J Lipid Res 48: 2664-72.
66. Wiedmer T, Zhao J, Li L, Zhou Q, Hevener A, et al. (2004) Adiposity, dyslipidemia, and insulin resistance in mice with targeted deletion of phospholipid scramblase 3 (plscr3). Proc Natl Acad Sci U S A 101: 13296-301.
67. Fan CY, Pan J, Chu R, Lee D, Kluckman KD, et al. (1996) Hepatocellular and hepatic peroxisomal alterations in mice with a disrupted peroxisomal fatty acyl-coenzyme a oxidase gene. J Biol Chem 271: 24698-710.
68. Sainsbury A, Baldock PA, Schwarzer C, Ueno N, Enriquez RF, et al. (2003) Synergistic effects of y2 and y4 receptors on adiposity and bone mass revealed in double knockout mice. Mol Cell Biol 23: 5225-33.
69. Edmondson AC, Braund PS, Stylianou IM, Khera AV, Nelson CP, et al. (2011) Dense genotyping of candidate gene loci identifies variants associated with high-density lipoprotein cholesterol. Circ Cardiovasc Genet 4: 145-55.
70. Foresti O, Ruggiano A, Hannibal-Bach HK, Ejsing CS, Carvalho P, (2013) Sterol home- ostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase doa10/teb4. eLife 2: e00953.
71. Liu SPP, Li YSS, Chen YJJ, Chiang EPP, Li AFY, et al. (2007) Glycine n- methyltransferase-/- mice develop chronic hepatitis and glycogen storage disease in the liver. Hepatology 46: 1413-25.
72. Bourre JM, Cl_ement M, G_erard D, Chaudi_ere J, (1989) Alterations of cholesterol synthe- sis precursors (7-dehydrocholesterol, 7-dehydrodesmosterol, desmosterol) in dysmyelinat- ing neurological mutant mouse (quaking, shiverer and trembler) in the pns and the cns. Biochim Biophys Acta 1004: 387-90.
73. Fujino T, Asaba H, Kang MJJ, Ikeda Y, Sone H, et al. (2003) Low-density lipoprotein receptor-related protein 5 (lrp5) is essential for normal cholesterol metabolism and glucose- induced insulin secretion. Proc Natl Acad Sci U S A 100: 229-34.
74. Kawahara Y, Grimberg A, Teegarden S, Mombereau C, Liu S, et al. (2008) Dysregulated editing of serotonin 2c receptor mrnas results in energy dissipation and loss of fat mass. J Neurosci 28: 12834-44.