Identification of pathways for atherosclerosis in mice: Integration of quantitative trait locus analysis and global gene expression data

Circulation Research

Volumn 101, Issue 3, 2007, Pages

  Wang, Susanna S ^a   Schadt, Eric E ^c   Wang, Hui ^b   Wang, Xuping ^b   Ingram Drake, Leslie ^a   Shi, Weibin ^b,d   Drake, Thomas A ^a   Lusis, Aldons J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROSETTA INPHARMATICS   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Atherosclerosis; C3H HeJ; Expression arrays; Quantitative trait locus; Sex

Indexed keywords

GLUCOSE; INSULIN; TRIACYLGLYCEROL;

ADIPOSE TISSUE; ARTICLE; ATHEROSCLEROTIC CARDIOVASCULAR DISEASE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA MICROARRAY; FEMALE; GENE EXPRESSION; GENE INTERACTION; GENE LOCUS; GENETIC CODE; GENETIC REGULATION; GENOME ANALYSIS; GENOTYPE; GLUCOSE BLOOD LEVEL; INFLAMMATION; LIVER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE TRAIT LOCUS; RISK FACTOR; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL;

ADIPOSE TISSUE; ANIMALS; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CHOLESTEROL; CROSSES, GENETIC; DIET, ATHEROGENIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HYPERLIPIDEMIAS; INFLAMMATION; LIVER; LOD SCORE; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MODELS, GENETIC; OXIDATIVE PHOSPHORYLATION; QUANTITATIVE TRAIT LOCI; RISK FACTORS; RNA, MESSENGER; SEX CHARACTERISTICS;

EID: 34548364227     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.152975     Document Type: Article

References (58)

1. Lusis AJ, Mar R, Pajukanta P. Genetics of atherosclerosis. Annu Rev Genomics Hum Genet. 2004;5:189-218.
2. Allayee H, Ghazalpour A, Lusis AJ. Using mice to dissect genetic factors in atherosclerosis. Arterioscler Thromb Vasc Biol. 2003;23:1501-1509.
3. Wang X, Ishimori N, Korstanje R, Rollins J, Paigen B. Identifying novel genes for atherosclerosis through mouse-human comparative genetics. Am J Hum Genet. 2005;77:1-15.
4. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, Colinayo V, Ruff TG, Milligan SB, Lamb JR, Cavet G, Linsley PS, Mao M, Stoughton RB, Friend SH. Genetics of gene expression surveyed in maize, mouse and man. Nature. 2003;422:297-302.
5. Chesler EJ, Lu L, Shou S, Qu Y, Gu J, Wang J, Hsu HC, Mountz JD, Baldwin NE, Langston MA, Threadgill DW, Manly KF, Williams RW. Complex trait analysis of gene expression uncovers polygenic and pleiotropic networks that modulate nervous system function. Nat Genet. 2005;37:233-242.
6. Bystrykh L, Weersing E, Dontje B, Sutton S, Pletcher MT, Wiltshire T, Su AI, Vellenga E, Wang J, Manly KF, Lu L, Chesler EJ, Alberts R, Jansen RC, Williams RW, Cooke MP, de Haan G. Uncovering regulatory pathways that affect hematopoietic stem cell function using 'genetical genomics'. Nat Genet. 2005;37:225-232.
7. Hubner N, Wallace CA, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Muller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ. Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet. 2005;37:243-253.
8. Doss S, Schadt EE, Drake TA, Lusis AJ. Cis-acting expression quantitative trait loci in mice. Genome Res. 2005;15:681-691.
9. Yaguchi H, Togawa K, Moritani M, Itakura M. Identification of candidate genes in the type 2 diabetes modifier locus using expression QTL. Genomics. 2005;85:591-599.
10. Yamashita S, Wakazono K, Nomoto T, Tsujino Y, Kuramoto T, Ushijima T. Expression quantitative trait loci analysis of 13 genes in the rat prostate. Genetics. 2005;171:1231-1238.
11. Palmer AA, Verbitsky M, Suresh R, Kamens HM, Reed CL, Li N, Burkhart-Kasch S, McKinnon CS, Belknap JK, Gilliam TC, Phillips TJ. Gene expression differences in mice divergently selected for methamphetamine sensitivity. Mamm Genome. 2005;16:291-305.
12. MacLaren EJ, Sikela JM. Cerebellar gene expression profiling and eQTL analysis in inbred mouse strains selected for ethanol sensitivity. Alcohol Clin Exp Res. 2005;29:1568-1579.
13. Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, Guhathakurta D, Sieberts SK, Monks S, Reitman M, Zhang C, Lum PY, Leonardson A, Thieringer R, Metzger JM, Yang L, Castle J, Zhu H, Kash SF, Drake TA, Sachs A, Lusis AJ. An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet. 2005;37:710-717.
14. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
15. Paigen B, Mitchell D, Reue K, Morrow A, Lusis AJ, LeBoeuf RC. Ath-1, a gene determining atherosclerosis susceptibility and high density lipoprotein levels in mice. Proc Natl Acad Sci U S A. 1987;84:3763-3767.
16. Su Z, Li Y, James JC, McDuffie M, Matsumoto AH, Helm GA, Weber JL, Lusis AJ, Shi W. Quantitative trait locus analysis of atherosclerosis in an intercross between C57BL/6 and C3H mice carrying the mutant apolipoprotein E gene. Genetics. 2006;172:1799-1807.
17. Shi W, Wang NJ, Shih DM, Sun VZ, Wang X, Lusis AJ. Determinants of atherosclerosis susceptibility in the C3H and C57BL/6 mouse model: evidence for involvement of endothelial cells but not blood cells or cholesterol metabolism. Circ Res. 2000;86:1078-1084.
18. Wang S, Yehya N, Schadt EE, Wang H, Drake TA, Lusis AJ. Genetic and genomic analysis of a fat mass trait with complex inheritance reveals marked sex specificity. PLoS Genet. 2006;2:e15.
19. Ghazalpour A, Doss S, Zhang B, Wang S, Plaisier C, Castellanos R, Brozell A, Schadt EE, Drake TA, Lusis AJ, Horvath S. Integrating genetic and network analysis to characterize genes related to mouse weight. PLoS Genet. 2006;2:e130.
20. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 2006;16:995-1004.
21. Mehrabian M, Qiao JH, Hyman R, Ruddle D, Laughton C, Lusis AJ. Influence of the apoA-II gene locus on HDL levels and fatty streak development in mice. Arterioscler Thromb. 1993;13:1-10.
22. Hardenbol P, Baner J, Jain M, Nilsson M, Namsaraev EA, Karlin-Neumann GA, Fakhrai-Rad H, Ronaghi M, Willis TD, Landegren U, Davis RW. Multiplexed genotyping with sequence-tagged molecular inversion probes. Nat Biotechnol. 2003;21:673-678.
23. Lander E, Kruglyak L. Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet. 1995;11:241-247.
24. Wang S, Basten CJ, Zeng ZB. Windows QTL Cartographer, version 2.5. Raleigh, NC: Department of Statistics, North Carolina State University; 2006 Available at http://statgen.ncsu.edu/qtlcart/WQTLCart.htm.
25. He YD, Dai H, Schadt EE, Cavet G, Edwards SW, Stepaniants SB, Duenwald S, Kleinhanz R, Jones AR, Shoemaker DD, Stoughton RB. Microarray standard data set and figures of merit for comparing data processing methods and experiment designs. Bioinformatics. 2003;19:956-965.
26. Welch CL, Bretschger S, Latib N, Bezouevski M, Guo Y, Pleskac N, Liang CP, Barlow C, Dansky H, Breslow JL, Tall AR. Localization of atherosclerosis susceptibility loci to chromosomes 4 and 6 using the Ldlr knockout mouse model. Proc Natl Acad Sci U S A. 2001;98:7946-7951.
27. Ishimori N, Li R, Kelmenson PM, Korstanje R, Walsh KA, Churchill GA, Forsman-Semb K, Paigen B. Quantitative trait loci analysis for plasma HDL-cholesterol concentrations and atherosclerosis susceptibility between inbred mouse strains C57BL/6J and 129S1/SvImJ. Arterioscler Thromb Vasc Biol. 2004;24:161-166.
28. Smith JD, Bhasin JM, Baglione J, Settle M, Xu Y, Barnard J. Atherosclerosis susceptibility loci identified from a strain intercross of apolipoprotein E-deficient mice via a high-density genome scan. Arterioscler Thromb Vasc Biol. 2006;26:597-603.
29. Flint J, Valdar W, Shifman S, Mott R. Strategies for mapping and cloning quantitative trait genes in rodents. Nat Rev Genet. 2005;6:271-286.
30. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Soc. 1995;57:289-300.
31. Wang X, Ria M, Kelmenson PM, Eriksson P, Higgins DC, Samnegard A, Petros C, Rollins J, Bennet AM, Wiman B, de Faire U, Wennberg C, Olsson PG, Ishii N, Sugamura K, Hamsten A, Forsman-Semb K, Lagercrantz J, Paigen B. Positional identification of TNFSF4, encoding OX40 ligand, as a gene that influences atherosclerosis susceptibility. Nat Genet. 2005;37:365-372.
32. Korstanje R, Li R, Howard T, Kelmenson P, Marshall J, Paigen B, Churchill G. 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. 2004;45:881-888.
33. Avery CL, Freedman BI, Kraja AT, Borecki IB, Miller MB, Pankow JS, Arnett D, Lewis CE, Myers RH, Hunt SC, North KE. Genotype-by-sex interaction in the aetiology of type 2 diabetes mellitus: support for sex-specific quantitative trait loci in Hypertension Genetic Epidemiology Network participants. Diabetologia. 2006;49:2329-2336.
34. Franceschini N, MacCluer JW, Goring HH, Cole SA, Rose KM, Almasy L, Diego V, Laston S, Lee ET, Howard BV, Best LG, Fabsitz RR, Roman MJ, North KE. A quantitative trait loci-specific gene-by-sex interaction on systolic blood pressure among American Indians: the Strong Heart Family Study. Hypertension. 2006;48:266-270.
35. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoEdeficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994;14:133-140.
36. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler Thromb. 1994;14:141-147.
37. Bogue MA, Grubb SC, Maddatu TP, Bult CJ. Mouse Phenome Database (MPD). Nucleic Acids Res. 2007;35:D643-D649.
38. Wright SD, Burton C, Hernandez M, Hassing H, Montenegro J, Mundt S, Patel S, Card DJ, Hermanowski-Vosatka A, Bergstrom JD, Sparrow CP, Detmers PA, Chao YS. Infectious agents are not necessary for murine atherogenesis. J Exp Med. 2000;191:1437-1442.
39. Merat S, Casanada F, Sutphin M, Palinski W, Reaven PD. Western-type diets induce insulin resistance and hyperinsulinemia in LDL receptor-deficient mice but do not increase aortic atherosclerosis compared with normoinsulinemic mice in which similar plasma cholesterol levels are achieved by a fructose-rich diet. Arterioscler Thromb Vasc Biol. 1999;19:1223-1230.
40. Teupser D, Persky AD, Breslow JL. Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler Thromb Vasc Biol. 2003;23:1907-1913.
41. Davenport P, Tipping PG. The role of interleukin-4 and interleukin-12 in the progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol. 2003;163:1117-1125.
42. Teupser D, Tan M, Persky AD, Breslow JL. Atherosclerosis quantitative trait loci are sex- and lineage-dependent in an intercross of C57BL/6 and FVB/N low-density lipoprotein receptor-/- mice. Proc Natl Acad Sci U S A. 2006;103:123-128.
43. Weiss LA, Pan L, Abney M, Ober C. The sex-specific genetic architecture of quantitative traits in humans. Nat Genet. 2006;38:218-222.
44. Tamura Y, Adachi H, Osuga J, Ohashi K, Yahagi N, Sekiya M, Okazaki H, Tomita S, Iizuka Y, Shimano H, Nagai R, Kimura S, Tsujimoto M, Ishibashi S. FEEL-1 and FEEL-2 are endocytic receptors for advanced glycation end products. J Biol Chem. 2003;278:12613-12617.
45. Kzhyshkowska J, Gratchev A, Brundiers H, Mamidi S, Krusell L, Goerdt S. Phosphatidylinositide 3-kinase activity is required for stabilin-1-mediated endosomal transport of acLDL. Immunobiology. 2005;210:161-173.
46. Hansen B, Longati P, Elvevold K, Nedredal GI, Schledzewski K, Olsen R, Falkowski M, Kzhyshkowska J, Carlsson F, Johansson S, Smedsrod B, Goerdt S, McCourt P. Stabilin-1 and stabilin-2 are both directed into the early endocytic pathway in hepatic sinusoidal endothelium via interactions with clathrin/AP-2, independent of ligand binding. Exp Cell Res. 2005;303:160-173.
47. Elhage R, Jawien J, Rudling M, Ljunggren HG, Takeda K, Akira S, Bayard F, Hansson GK. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc Res. 2003;59:234-240.
48. Aizawa Y, Akita K, Taniai M, Torigoe K, Mori T, Nishida Y, Ushio S, Nukada Y, Tanimoto T, Ikegami H, Ikeda M, Kurimoto M. Cloning and expression of interleukin-18 binding protein. FEBS Lett. 1999;445:338-342.
49. Mallat Z, Corbaz A, Scoazec A, Graber P, Alouani S, Esposito B, Humbert Y, Chvatchko Y, Tedgui A. Interleukin-18/interleukin-18 binding protein signaling modulates atherosclerotic lesion development and stability. Circ Res. 2001;89:e41-e45.
50. Tiret L, Godefroy T, Lubos E, Nicaud V, Tregouet DA, Barbaux S, Schnabel R, Bickel C, Espinola-Klein C, Poirier O, Perret C, Munzel T, Rupprecht HJ, Lackner K, Cambien F, Blankenberg S. Genetic analysis of the interleukin-18 system highlights the role of the interleukin-18 gene in cardiovascular disease. Circulation. 2005;112:643-650.
51. Lutgens E, Faber B, Schapira K, Evelo CT, van Haaften R, Heeneman S, Cleutjens KB, Bijnens AP, Beckers L, Porter JG, Mackay CR, Rennert P, Bailly V, Jarpe M, Dolinski B, Koteliansky V, de Fougerolles T, Daemen MJ. Gene profiling in atherosclerosis reveals a key role for small inducible cytokines: validation using a novel monocyte chemoattractant protein monoclonal antibody. Circulation. 2005;111:3443-3452.
52. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112:1796-1808.
53. George J, Mulkins M, Shaish A, Casey S, Schatzman R, Sigal E, Harats D. Interleukin (IL)-4 deficiency does not influence fatty streak formation in C57BL/6 mice. Atherosclerosis. 2000;153:403-411.
54. Lee YW, Kuhn H, Hennig B, Neish AS, Toborek M. IL-4-induced oxidative stress upregulates VCAM-1 gene expression in human endothelial cells. J Mol Cell Cardiol. 2001;33:83-94.
55. Walch L, Massade L, Dufilho M, Brunet A, Rendu F. Pro-atherogenic effect of interleukin-4 in endothelial cells: modulation of oxidative stress, nitric oxide and monocyte chemoattractant protein-1 expression. Atherosclerosis. 2006;187:285-291.
56. Saleh MC, Wheeler MB, Chan CB. Uncoupling protein-2: evidence for its function as a metabolic regulator. Diabetologia. 2002;45:174-187.
57. Ballinger SW. Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med. 2005;38:1278-1295.
58. Blanc J, Alves-Guerra MC, Esposito B, Rousset S, Gourdy P, Ricquier D, Tedgui A, Miroux B, Mallat Z. Protective role of uncoupling protein 2 in atherosclerosis. Circulation. 2003;107:388-390.