Using bioinformatics and systems genetics to dissect HDL-cholesterol genetics in an MRL/MpJ x SM/J intercross

Journal of Lipid Research

Volumn 53, Issue 6, 2012, Pages 1163-1175

  Leduc, Magalie S ^a,b   Blair, Rachael Hageman ^a,c   Verdugo, Ricardo A ^a   Tsaih, Shirng Wern ^d   Walsh, Kenneth ^a   Churchill, Gary A ^a   Paigen, Beverly ^a  

^a JACKSON LABORATORY   (United States)

^b SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Gene suppression; Genomics; High density lipoprotein cholesterol

Indexed keywords

APOLIPOPROTEIN A2; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL LIPASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOA2 GENE; ARTICLE; BIOINFORMATICS; CHROMOSOME 1; CHROMOSOME 10; CHROMOSOME 11; CHROMOSOME 13; CHROMOSOME 18; CHROMOSOME 3; CHROMOSOME 4; CHROMOSOME 7; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCUS; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC TRAIT; GENETICS; LIPG GENE; LIVER PARENCHYMA; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; SYSTEMS GENETICS;

AMINO ACID SEQUENCE; ANIMALS; CHOLESTEROL, HDL; CHROMOSOMES, MAMMALIAN; DOGS; FEMALE; GENOMICS; HUMANS; HYBRIDIZATION, GENETIC; LIPASE; MALE; MICE; MOLECULAR SEQUENCE DATA; QUANTITATIVE TRAIT LOCI; RATS; SYSTEMS BIOLOGY;

EID: 84861437612     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M025833     Document Type: Article

References (53)

1. Hopkins, P. N., and R. R. Williams. 1981. A survey of 246 suggested coronary risk factors. Atherosclerosis. 40: 1-52. (Pubitemid 11040301)
2. Castelli, W. P., J. T. Doyle, T. Gordon, C. G. Hames, M. C. Hjortland, S. B. Hulley, A. Kagan, and W. J. Zukel. 1977. HDL cholesterol and other lipids in coronary heart disease. The cooperative lipoprotein phenotyping study. Circulation. 55: 767-772. (Pubitemid 8090093)
3. Barter, P. J., M. Caulfield, M. Eriksson, S. M. Grundy, J. J. Kastelein, M. Komajda, J. Lopez-Sendon, L. Mosca, J. C. Tardif, D. D. Waters, et al. 2007. Effects of torcetrapib in patients at high risk for coronary events. N. Engl. J. Med. 357: 2109-2122. (Pubitemid 350146106)
4. Melnikova, I. 2005. Raising HDL cholesterol. Nat. Rev. Drug Discov. 4: 185-186. (Pubitemid 40372547)
5. Williams, P. T. 1997. Interactive effects of exercise, alcohol, and vegetarian diet on coronary artery disease risk factors in 9242 runners: the National Runners' Health Study. Am. J. Clin. Nutr. 66: 1197-1206. (Pubitemid 27473345)
6. Teslovich, T. M., K. Musunuru, A. V. Smith, A. C. Edmondson, I. M. Stylianou, M. Koseki, J. P. Pirruccello, S. Ripatti, D. I. Chasman, C. J. Willer, et al. 2010. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 466: 707-713.
7. Wang, X., and B. Paigen. 2005. Genetics of variation in HDL cholesterol in humans and mice. Circ. Res. 96: 27-42. (Pubitemid 40095752)
8. Leduc, M. S., M. Lyons, K. Darvishi, K. Walsh, S. Sheehan, S. Amend, A. Cox, M. Orho-Melander, S. Kathiresan, B. Paigen, et al. 2011. The mouse QTL map helps interpret human genome-wide association studies for HDL cholesterol. J. Lipid Res. 52: 1139-1149.
9. Burgess-Herbert, S. L., A. Cox, S. W. Tsaih, and B. Paigen. 2008. Practical applications of the bioinformatics toolbox for narrowing quantitative trait loci. Genetics. 180: 2227-2235.
10. DiPetrillo, K., X. Wang, I. M. Stylianou, and B. Paigen. 2005. Bioinformatics toolbox for narrowing rodent quantitative trait loci. Trends Genet. 21: 683-692. (Pubitemid 41608691)
11. Langfelder, P., L. W. Castellani, Z. Zhou, E. Paul, R. Davis, E. E. Schadt, A. J. Lusis, S. Horvath, and M. Mehrabian. 2012. A systems genetic analysis of high density lipoprotein metabolism and network preservation across mouse models. Biochim. Biophys. Acta. 1821: 435-447.
12. Langfelder, P., and S. Horvath. 2008. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 9: 559.
13. Leduc, M. S., R. S. Hageman, R. A. Verdugo, S. W. Tsaih, K. Walsh, G. A. Churchill, and B. Paigen. 2011. Integration of QTL and bioinformatic tools to identify candidate genes for triglycerides in mice. J. Lipid Res. 52: 1672-1682.
14. Leduc, M. S., R. S. Hageman, Q. Meng, R. A. Verdugo, S. W. Tsaih, G. A. Churchill, B. Paigen, and R. Yuan. 2010. Identification of genetic determinants of IGF-1 levels and longevity among mouse inbred strains. Aging Cell. 9: 823-836.
15. Cox, A., C. L. Ackert-Bicknell, B. L. Dumont, Y. Ding, J. T. Bell, G. A. Brockmann, J. E. Wergedal, C. Bult, B. Paigen, J. Flint, et al. 2009. A new standard genetic map for the laboratory mouse. Genetics. 182: 1335-1344.
16. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 19: 185-193. (Pubitemid 36181903)
17. Dai, M., P. Wang, A. D. Boyd, G. Kostov, B. Athey, E. G. Jones, W. E. Bunney, R. M. Myers, T. P. Speed, H. Akil, et al. 2005. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33: e175.
18. Broman, K. W., H. Wu, S. Sen, and G. A. Churchill. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 19: 889-890. (Pubitemid 36582406)
19. Broman, K. W., S. Sen, S. E. Owens, A. Manichaikul, E. M. Southard- Smith, and G. A. Churchill. 2006. The X chromosome in quantitative trait locus mapping. Genetics. 174: 2151-2158. (Pubitemid 46011602)
20. Ng, P. C., and S. Henikoff. 2001. Predicting deleterious amino acid substitutions. Genome Res. 11: 863-874. (Pubitemid 32447869)
21. Li, R., S. W. Tsaih, K. Shockley, I. M. Stylianou, J. Wergedal, B. Paigen, and G. A. Churchill. 2006. Structural model analysis of multiple quantitative traits. PLoS Genet. 2: e114.
22. Neto, E., M. Keller, A. Attie, and B. Yandell. 2010. Causal graphical models in systems genetics: a unified framework for joint inference of causal network and genetic architecture for correlated phenotypes. Ann. Appl. Stat. 4: 320-339.
23. Langfelder, P., and S. Horvath. 2007. Eigengene networks for studying the relationships between co-expression modules. BMC Syst. Biol. 1: 54.
24. Lehmann, E. 1975. Nonparametrics: Statistical Methods Based on Ranks. Holden-Day, San Francisco.
25. Wang, X., R. Korstanje, D. Higgins, and B. Paigen. 2004. Haplotype analysis in multiple crosses to identify a QTL gene. Genome Res. 14: 1767-1772. (Pubitemid 39276435)
26. Su, Z., N. Ishimori, Y. Chen, E. H. Leiter, G. A. Churchill, B. Paigen, and I. M. Stylianou. 2009. Four additional mouse crosses improve the lipid QTL landscape and identify Lipg as a QTL gene. J. Lipid Res. 50: 2083-2094.
27. Su, Z., S. W. Tsaih, J. Szatkiewicz, Y. Shen, and B. Paigen. 2008. Candidate genes for plasma triglyceride, FFA, and glucose revealed from an intercross between inbred mouse strains NZB/B1NJ and NZW/LacJ. J. Lipid Res. 49: 1500-1510.
28. Lelliott, C. J., G. Medina-Gomez, N. Petrovic, A. Kis, H. M. Feldmann, M. Bjursell, N. Parker, K. Curtis, M. Campbell, P. Hu, et al. 2006. Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 4: e369.
29. Lawson, H. A., A. Lee, G. L. Fawcett, B. Wang, L. S. Pletscher, T. J. Maxwell, T. H. Ehrich, J. P. Kenney-Hunt, J. B. Wolf, C. F. Semenkovich, et al. 2011. The importance of context to the genetic architecture of diabetes-related traits is revealed in a genome-wide scan of a LG/J x SM/J murine model. Mamm. Genome. 22: 197-208.
30. Lawson, H. A., K. M. Zelle, G. L. Fawcett, B. Wang, L. S. Pletscher, T. J. Maxwell, T. H. Ehrich, J. P. Kenney-Hunt, J. B. Wolf, C. F. Semenkovich, et al. 2010. Genetic, epigenetic, and gene-by-diet interaction effects underlie variation in serum lipids in a LG/JxSM/J murine model. J. Lipid Res. 51: 2976-2984.
31. Stylianou, I. M., J. P. Affourtit, K. R. Shockley, R. Y. Wilpan, F. A. Abdi, S. Bhardwaj, J. Rollins, G. A. Churchill, and B. Paigen. 2008. Applying gene expression, proteomics and single-nucleotide polymorphism analysis for complex trait gene identification. Genetics. 178: 1795-1805.
32. Suto, J. 2005. Apolipoprotein gene polymorphisms as cause of cholesterol QTLs in mice. J. Vet. Med. Sci. 67: 583-589. (Pubitemid 41373915)
33. Rainwater, D. L., L. A. Cox, J. Rogers, J. L. VandeBerg, and M. C. Mahaney. 2009. Localization of multiple pleiotropic genes for lipoprotein metabolism in baboons. J. Lipid Res. 50: 1420-1428.
34. Kullo, I. J., S. T. Turner, E. Boerwinkle, S. L. Kardia, and M. de Andrade. 2005. A novel quantitative trait locus on chromosome 1 with pleiotropic effects on HDL-cholesterol and LDL particle size in hypertensive sibships. Am. J. Hypertens. 18: 1084-1090. (Pubitemid 41139907)
35. Korstanje, R., R. Li, T. Howard, P. Kelmenson, J. Marshall, B. Paigen, and G. Churchill. 2004. Influence of sex and diet on quantitative trait loci for HDL cholesterol levels in an SM/J by NZB/ BlNJ intercross population. J. Lipid Res. 45: 881-888. (Pubitemid 38552858)
36. Shockley, K. R., D. Witmer, S. L. Burgess-Herbert, B. Paigen, and G. A. Churchill. 2009. Effects of atherogenic diet on hepatic gene expression across mouse strains. Physiol. Genomics. 39: 172-182.
37. Rockman, M. V. 2008. Reverse engineering the genotype-phenotype map with natural genetic variation. Nature. 456: 738-744.
38. Vaisar, T., S. Pennathur, P. S. Green, S. A. Gharib, A. N. Hoofnagle, M. C. Cheung, J. Byun, S. Vuletic, S. Kassim, P. Singh, et al. 2007. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J. Clin. Invest. 117: 746-756. (Pubitemid 46348533)
39. Barter, P. J., S. Nicholls, K. A. Rye, G. M. Anantharamaiah, M. Navab, and A. M. Fogelman. 2004. Antiinflammatory properties of HDL. Circ. Res. 95: 764-772. (Pubitemid 39390578)
40. Yvan-Charvet, L., J. Kling, T. Pagler, H. Li, B. Hubbard, T. Fisher, C. P. Sparrow, A. K. Taggart, and A. R. Tall. 2010. Cholesterol efflux potential and antiinflammatory properties of high-density lipoprotein after treatment with niacin or anacetrapib. Arterioscler. Thromb. Vasc. Biol. 30: 1430-1438.
41. Arora, P., B. Garcia-Bailo, Z. Dastani, D. Brenner, A. Villegas, S. Malik, T. D. Spector, B. Richards, A. El-Sohemy, M. Karmali, et al. 2011. Genetic polymorphisms of innate immunity-related inflammatory pathways and their association with factors related to type 2 diabetes. BMC Med. Genet. 12: 95.
42. Park, S. H., J. H. Park, J. S. Kang, and Y. H. Kang. 2003. Involvement of transcription factors in plasma HDL protection against TNF-alpha- induced vascular cell adhesion molecule-1 expression. Int. J. Biochem. Cell Biol. 35: 168-182.
43. Buch, S., C. Schafmayer, H. Volzke, C. Becker, A. Franke, H. von Eller-Eberstein, C. Kluck, I. Bassmann, M. Brosch, F. Lammert, et al. 2007. A genome-wide association scan identifies the hepatic cholesterol transporter ABCG8 as a susceptibility factor for human gallstone disease. Nat. Genet. 39: 995-999. (Pubitemid 47185186)
44. Martinez, L. O., S. Jacquet, J. P. Esteve, C. Rolland, E. Cabezon, E. Champagne, T. Pineau, V. Georgeaud, J. E. Walker, F. Terce, et al. 2003. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature. 421: 75-79. (Pubitemid 36077087)
45. Brunham, L. R., J. K. Kruit, J. Iqbal, C. Fievet, J. M. Timmins, T. D. Pape, B. A. Coburn, N. Bissada, B. Staels, A. K. Groen, et al. 2006. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 116: 1052-1062.
46. Lyons, M. A., H. Wittenburg, R. Li, K. A. Walsh, G. A. Churchill, M. C. Carey, and B. Paigen. 2003. Quantitative trait loci that determine lipoprotein cholesterol levels in DBA/2J and CAST/Ei inbred mice. J. Lipid Res. 44: 953-967. (Pubitemid 37279655)
47. Lyons, M. A., H. Wittenburg, R. Li, K. A. Walsh, R. Korstanje, G. A. Churchill, M. C. Carey, and B. Paigen. 2004. Quantitative trait loci that determine lipoprotein cholesterol levels in an intercross of 129S1/ SvImJ and CAST/Ei inbred mice. Physiol. Genomics. 17: 60-68. (Pubitemid 38924151)
48. Su, Z., X. Wang, S. W. Tsaih, A. Zhang, A. Cox, S. Sheehan, and B. Paigen. 2009. Genetic basis of HDL variation in 129/SvImJ and C57BL/6J mice: importance of testing candidate genes in targeted mutant mice. J. Lipid Res. 50: 116-125.
49. Welch, C. L., S. Bretschger, P. Z. Wen, M. Mehrabian, N. Latib, J. Fruchart-Najib, J. C. Fruchart, C. Myrick, and A. J. Lusis. 2004. Novel QTLs for HDL levels identified in mice by controlling for Apoa2 allelic effects: confirmation of a chromosome 6 locus in a congenic strain. Physiol. Genomics. 17: 48-59. (Pubitemid 38924150)
50. Anunciado, R. V., M. Nishimura, M. Mori, A. Ishikawa, S. Tanaka, F. Horio, T. Ohno, and T. Namikawa. 2003. Quantitative trait locus analysis of serum insulin, triglyceride, total cholesterol and phospholipid levels in the (SM/J x A/J)F2 mice. Exp. Anim. 52: 37-42. (Pubitemid 41349989)
51. Su, Z., A. Cox, Y. Shen, I. M. Stylianou, and B. Paigen. 2009. Farp2 and Stk25 are candidate genes for the HDL cholesterol locus on mouse chromosome 1. Arterioscler. Thromb. Vasc. Biol. 29: 107-113.
52. Mehrabian, M., L. W. Castellani, P. Z. Wen, J. Wong, T. Rithaporn, S. Y. Hama, G. P. Hough, D. Johnson, J. J. Albers, G. A. Mottino, et al. 2000. Genetic control of HDL levels and composition in an interspecific mouse cross (CAST/Ei x C57BL/6J). J. Lipid Res. 41: 1936-1946. (Pubitemid 32038988)
53. Maltais, L. J., J. A. Blake, T. Chu, C. M. Lutz, J. T. Eppig, and I. Jackson. 2002. Rules and guidelines for mouse gene, allele, and mutation nomenclature: a condensed version. Genomics. 79: 471-474. (Pubitemid 34274284)