Pathway-based genome-wide association studies for plasma triglycerides in obese females and normal-weight controls

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Jiao, Hongxiao ^a   Wang, Kai ^b   Yang, Fuhua ^a   Grant, Struan F A ^c,d   Hakonarson, Hakon ^c,d   Price, R Arlen ^d   Li, Wei Dong ^a,d  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER G1; PROTEIN BCL 6; TRIACYLGLYCEROL; GENETIC MARKER;

ABCG1 GENE; ADULT; ARTICLE; ASTN2 GENE; BCL6 GENE; BODY MASS; CONTROLLED STUDY; EUROPEAN AMERICAN; FEMALE; GENE; GENE FUNCTION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; OBESITY; QUANTITATIVE TRAIT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRIACYLGLYCEROL BLOOD LEVEL; VITAMIN METABOLISM; BLOOD; CASE CONTROL STUDY; GENETIC MARKER; GENETICS; GENOME-WIDE ASSOCIATION STUDY;

ADULT; CASE-CONTROL STUDIES; FEMALE; GENETIC MARKERS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; OBESITY; POLYMORPHISM, SINGLE NUCLEOTIDE; TRIGLYCERIDES;

EID: 84943389086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134923     Document Type: Article

References (56)

1. Maher B. Personal genomes: The case of the missing heritability. Nature. 2008; 456(7218):18-21. doi:10.1038/456018a PMID: 18987709
2. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, et al. Finding the missing heritability of complex diseases. Nature. 2009; 461(7265):747-53. doi: 10.1038/nature08494 PMID: 19812666
3. Wang LL, Jia PL, Wolfinger RD, Chen X, Zhao ZM. Gene set analysis of genome-wide association studies: Methodological issues and perspectives. Genomics. 2011; 98(1):1-8. doi: 10.1016/j.ygeno.2011.04.006 PMID: 21565265
4. Yaspan BL, Veatch OJ. Strategies for pathway analysis from GWAS data. Current protocols in human genetics / editorial board, Jonathan L Haines [et al]. 2011;Chapter 1:Unit1 20.
5. Elbers CC, van Eijk KR, Franke L, Mulder F, van der Schouw YT, Wijmenga C, et al. Using genomewide pathway analysis to unravel the etiology of complex diseases. Genetic epidemiology. 2009; 33 (5):419-31. doi: 10.1002/gepi.20395 PMID: 19235186
6. Wang K, Li M, Hakonarson H. Analysing biological pathways in genome-wide association studies. Nature reviews Genetics. 2010; 11(12):843-54. doi: 10.1038/nrg2884 PMID: 21085203
7. Lee D, Lee GK, Yoon KA, Lee JS. Pathway-Based Analysis Using Genome-wide Association Data from a Korean Non-Small Cell Lung Cancer Study. PloS one. 2013; 8(6).
8. Schadt EE. Molecular networks as sensors and drivers of common human diseases. Nature. 2009; 461 (7261):218-23. doi: 10.1038/nature08454 PMID: 19741703
9. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(43):15545-50. PMID: 16199517
10. Wang K, Li M, Bucan M. Pathway-based approaches for analysis of genomewide association studies. American journal of human genetics. 2007; 81(6):1278-83. PMID: 17966091
11. Wang K, Zhang H, Kugathasan S, Annese V, Bradfield JR, Russell RK, et al. Diverse Genome-wide Association Studies Associate the IL12/IL23 Pathway with Crohn Disease. American journal of human genetics. 2009; 84(3):399-405. doi: 10.1016/j.ajhg.2009.01.026 PMID: 19249008
12. Liu YJ, Guo YF, Zhang LS, Pei YF, Yu N, Yu P, et al. Biological Pathway-Based Genome-Wide Association Analysis Identified the Vasoactive Intestinal Peptide (VIP) Pathway Important for Obesity. Obesity. 2010; 18(12):2339-46. doi: 10.1038/oby.2010.83 PMID: 20379146
13. Perry JR, McCarthy MI, Hattersley AT, Zeggini E, Weedon MN, Frayling TM. Interrogating type 2 diabetes genome-wide association data using a biological pathway-based approach. Diabetes. 2009; 58 (6):1463-7. doi: 10.2337/db08-1378 PMID: 19252133
14. Miller M. The epidemiology of triglyceride as a coronary artery disease risk factor. Clinical cardiology. 1999; 22(6 Suppl):II1-6. PMID: 10376190
15. Patel A, Barzi F, Jamrozik K, Lam TH, Ueshima H, Whitlock G, et al. Serum triglycerides as a risk factor for cardiovascular diseases in the Asia-Pacific region. Circulation. 2004; 110(17):2678-86. PMID: 15492305
16. Wei EH, Ali YB, Lyon J, Wang HJ, Nelson R, Dolinsky VW, et al. Loss of TGH/Ces3 in Mice Decreases Blood Lipids, Improves Glucose Tolerance, and Increases Energy Expenditure. Cell metabolism. 2010; 11(3):183-93. doi: 10.1016/j.cmet.2010.02.005 PMID: 20197051
17. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010; 466(7307):707-13. doi: 10.1038/nature09270 PMID: 20686565
18. Willer CJ, Schmidt EM, Sengupta S, Peloso GM, Gustafsson S, Kanoni S, et al. Discovery and refinement of loci associated with lipid levels. Nature genetics. 2013; 45(11):1274-83. doi:10.1038/ng.2797 PMID: 24097068
19. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, Rieder MJ, et al. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nature genetics. 2008; 40(2):189-97. doi: 10.1038/ng.75 PMID: 18193044
20. Kooner JS, Chambers JC, Aguilar-Salinas CA, Hinds DA, Hyde CL, Warnes GR, et al. Genome-wide scan identifies variation in MLXIPL associated with plasma triglycerides. Nature genetics. 2008; 40 (2):149-51. doi: 10.1038/ng.2007.61 PMID: 18193046
21. Shen GQ, Li L, Wang QK. Genetic variant R952Q in LRP8 is associated with increased plasma triglyceride levels in patients with early-onset CAD and MI. Annals of human genetics. 2012; 76(3):193-9. doi: 10.1111/j.1469-1809.2012.00705.x PMID: 22404453
22. Zhang K, Chang S, Cui S, Guo L, Zhang L, Wang J. ICSNPathway: identify candidate causal SNPs and pathways from genome-wide association study by one analytical framework. Nucleic acids research. 2011; 39(Web Server issue):W437-43. doi: 10.1093/nar/gkr391 PMID: 21622953
23. Wang K, Li WD, Zhang CK, Wang Z, Glessner JT, Grant SF, et al. A genome-wide association study on obesity and obesity-related traits. PloS one. 2011; 6(4):e18939. doi:10.1371/journal.pone.0018939 PMID: 21552555
24. Wilson PM, Fryer RH, Fang Y, Hatten ME. Astn2, a novel member of the astrotactin gene family, regulates the trafficking of ASTN1 during glial-guided neuronal migration. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010; 30(25):8529-40.
25. Vrijenhoek T, Buizer-Voskamp JE, van der Stelt I, Strengman E, Sabatti C, Geurts van Kessel A, et al. Recurrent CNVs disrupt three candidate genes in schizophrenia patients. American journal of human genetics. 2008; 83(4):504-10. doi:10.1016/j.ajhg.2008.09.011 PMID: 18940311
26. Kathiresan S, Manning AK, Demissie S, D'Agostino RB, Surti A, Guiducci C, et al. A genome-wide association study for blood lipid phenotypes in the Framingham Heart Study. BMC Med Genet. 2007; 8 Suppl 1:S17. PMID: 17903299
27. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, Hu T, et al. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet. 2008; 40(5):638-45. doi: 10.1038/ng.120 PMID: 18372903
28. Fogarty MP, Xiao R, Prokunina-Olsson L, Scott LJ, Mohlke KL. Allelic expression imbalance at high-density lipoprotein cholesterol locus MMAB-MVK. Human molecular genetics. 2010; 19(10):1921-9. doi: 10.1093/hmg/ddq067 PMID: 20159775
29. Kondos SC, Hatfaludi T, Voskoboinik I, Trapani JA, Law RHP, Whisstock JC, et al. The structure and function of mammalian membrane-attack complex/perforin-like proteins. Tissue Antigens. 2010; 76 (5):341-51. doi: 10.1111/j.1399-0039.2010.01566.x PMID: 20860583
30. Adams NC, Tomoda T, Cooper M, Dietz G, Hatten ME. Mice that lack astrotactin have slowed neuronal migration. Development. 2002; 129(4):965-72. PMID: 11861479
31. Lesch K-P, Timmesfeld N, Renner TJ, Halperin R, Röser C, et al. (2008) Molecular genetics of adult ADHD: converging evidence from genome-wide association and extended pedigree linkage studies. Journal of Neural Transmission 115: 1573-1585. doi: 10.1007/s00702-008-0119-3 PMID: 18839057
32. Uno K, Katagiri H, Yamada T, Ishigaki Y, Ogihara T, Imai J, et al. Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity. Science. 2006; 312(5780):1656-9. PMID: 16778057
33. Schwartz MW. Progress in the search for neuronal mechanisms coupling type 2 diabetes to obesity. The Journal of clinical investigation. 2001; 108(7):963-4. PMID: 11581296
34. Kim K-Z, Min J-Y, Kim K, Sung J, Cho S-I. Exploring Trans-acting regulators of gene expression associated with metabolic syndrome: a coupled application of factor analysis and linkage analysis. Genes & Genomics. 2013; 35(1):59-67.
35. Junyent M, Parnell LD, Lai CQ, Lee YC, Smith CE, Arnett DK, et al. Novel variants at KCTD10, MVK, and MMAB genes interact with dietary carbohydrates to modulate HDL-cholesterol concentrations in the Genetics of Lipid Lowering Drugs and Diet Network Study. The American journal of clinical nutrition. 2009; 90(3):686-94. doi: 10.3945/ajcn.2009.27738 PMID: 19605566
36. Li WD, Dong C, Li D, Zhao H, Price RA. An obesity-related locus in chromosome region 12q23-24. Diabetes. 2004; 53(3):812-20. PMID: 14988268
37. Maiti N, Widjaja L, Banerjee R. Proton transfer from histidine 244 may facilitate the 1,2 rearrangement reaction in coenzyme B(12)-dependent methylmalonyl-CoA mutase. The Journal of biological chemistry. 1999; 274(46):32733-7. PMID: 10551831
38. Clarke R, Armitage J. Vitamin supplements and cardiovascular risk: review of the randomized trials of homocysteine-lowering vitamin supplements. Seminars in thrombosis and hemostasis. 2000; 26 (3):341-8. PMID: 11011852
39. Refsum H, Ueland PM, Nygard O, Vollset SE. Homocysteine and cardiovascular disease. Annual review of medicine. 1998; 49:31-62. PMID: 9509248
40. Werstuck GH, Lentz SR, Dayal S, Hossain GS, Sood SK, Shi YY, et al. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. The Journal of clinical investigation. 2001; 107(10):1263-73. PMID: 11375416
41. Shaffer AL, Yu X, He Y, Boldrick J, Chan EP, Staudt LM. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity. 2000; 13(2):199-212. PMID: 10981963
42. Ye BH, Lista F, Lo Coco F, Knowles DM, Offit K, Chaganti RS, et al. Alterations of a zinc finger-encoding gene, BCL-6, in diffuse large-cell lymphoma. Science. 1993; 262(5134):747-50. PMID: 8235596
43. Glauser DA, Schlegel W. The emerging role of FOXO transcription factors in pancreatic beta cells. The Journal of endocrinology. 2007; 193(2):195-207. PMID: 17470511
44. Glauser DA, Schlegel W. The FoxO/Bcl-6/cyclin D2 pathway mediates metabolic and growth factor stimulation of proliferation in Min6 pancreatic beta-cells. Journal of receptor and signal transduction research. 2009; 29(6):293-8. doi: 10.3109/10799890903241824 PMID: 19929250
45. Barish GD, Yu RT, Karunasiri MS, Becerra D, Kim J, Tseng TW, et al. The Bcl6-SMRT/NCoR cistrome represses inflammation to attenuate atherosclerosis. Cell metabolism. 2012; 15(4):554-62. doi: 10.1016/j.cmet.2012.02.012 PMID: 22465074
46. Jonkers IJ, Mohrschladt MF, Westendorp RG, van der Laarse A, Smelt AH. Severe hypertriglyceridemia with insulin resistance is associated with systemic inflammation: reversal with bezafibrate therapy in a randomized controlled trial. The American journal of medicine. 2002; 112(4):275-80. PMID: 11893366
47. Vogel RA, Corretti MC, Plotnick GD. Effect of a single high-fat meal on endothelial function in healthy subjects. The American journal of cardiology. 1997; 79(3):350-4. PMID: 9036757
48. Wang L, Gill R, Pedersen TL, Higgins LJ, Newman JW, Rutledge JC. Triglyceride-rich lipoprotein lipolysis releases neutral and oxidized FFAs that induce endothelial cell inflammation. Journal of lipid research. 2009; 50(2):204-13. doi: 10.1194/jlr.M700505-JLR200 PMID: 18812596
49. Lee HS, Moon KC, Song CY, Kim BC, Wang S, Hong HK. Glycated albumin activates PAI-1 transcription through Smad DNA binding sites in mesangial cells. American journal of physiology Renal physiology. 2004; 287(4):F665-72. PMID: 15198928
50. Kim YS, Kim BC, Song CY, Hong HK, Moon KC, Lee HS. Advanced glycosylation end products stimulate collagen mRNA synthesis in mesangial cells mediated by protein kinase C and transforming growth factor-beta. The Journal of laboratory and clinical medicine. 2001; 138(1):59-68. PMID: 11433229
51. Li MC, He SH. IL-10 and its related cytokines for treatment of inflammatory bowel disease. World journal of gastroenterology: WJG. 2004; 10(5):620-5. PMID: 14991925
52. Li WD, Dong C, Li D, Garrigan C, Price RA. A genome scan for serum triglyceride in obese nuclear families. Journal of lipid research. 2005; 46(3):432-8. PMID: 15604520
53. Wang K, Li WD, Glessner JT, Grant SF, Hakonarson H, Price RA. Large copy-number variations are enriched in cases with moderate to extreme obesity. Diabetes2010. p. 2690-4. doi: 10.2337/db10-0192 PMID: 20622171
54. Lahiri DK, Nurnberger JI Jr. A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic acids research. 1991; 19(19):5444. PMID: 1681511
55. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. American journal of human genetics. 2007; 81(3):559-75. PMID: 17701901
56. Zhang K, Cui S, Chang S, Zhang L, Wang J. i-GSEA4GWAS: a web server for identification of pathways/gene sets associated with traits by applying an improved gene set enrichment analysis to genome-wide association study. Nucleic acids research. 2010; 38(Web Server):W90-W5. doi: 10.1093/nar/gkq324 PMID: 20435672