Obesity favors apolipoprotein E- and C-III-containing high density lipoprotein subfractions associated with risk of heart disease

Journal of Lipid Research

Volumn 55, Issue 10, 2014, Pages 2167-2177

  Talayero, Beatriz ^a   Wang, Liyun ^a   Furtado, Jeremy ^a   Carey, Vincent J ^b   Bray, George A ^c   Sacks, Frank M ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b CHANNING LABORATORY   (United States)

^c PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Apolipoprotein A I; Coronary heart disease; High density lipoprotein size

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN C3; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL;

ADULT; AGED; ARTICLE; BODY MASS; CARDIOVASCULAR RISK; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; FEMALE; GENOTYPE; HEART PROTECTION; HIGH RISK POPULATION; HUMAN; IMMUNOAFFINITY CHROMATOGRAPHY; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; LIPOPROTEIN BLOOD LEVEL; MALE; MOLECULAR WEIGHT; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OBESITY; PHENOTYPE; PREDICTIVE VALUE; PREVALENCE; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN LOCALIZATION; BLOOD; CLINICAL TRIAL; HEART DISEASE; MIDDLE AGED; MULTICENTER STUDY;

ADULT; AGED; APOLIPOPROTEIN C-III; APOLIPOPROTEINS E; FEMALE; HEART DISEASES; HUMANS; LIPOPROTEINS, HDL; MALE; MIDDLE AGED; OBESITY;

EID: 84907495541     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M042333     Document Type: Article

References (52)

1. Gordon, T., W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber. 1977. High density lipoprotein as a protective factor against coronary heart disease: the Framingham Study. Am. J. Med. 62: 707-714.
2. Sharrett, A. R., C. M. Ballantyne, S. A. Coady, G. Heiss, P. D. Sorlie, D. Catellier, and W. Patsch; Atherosclerosis Risk in Communities Study Group. 2001. Coronary heart disease protection from lipoprotein cholesterol levels, triglycerides, lipoprotein(a), apolipoproteins A-I and B, and HDL density subfractions: the Atherosclerosis Risk in Communities (ARIC) Study. Circulation. 104: 1108-1113.
3. Assmann, G., H. Schulte, A. von Eckardstein, and Y. Huang. 1996. High-density lipoprotein cholesterol as a predictor of coronary heart disease risk. The PROCAM experience and pathophysiological implications for reverse cholesterol transport. Atherosclerosis. 124 (Suppl.): S11-S20.
4. Di Angelantonio, E., N. Sarwar, P. Perry, S. Kaptoge, K. K. Ray, A. Thompson, A. M. Wood, S. Lewington, N. Sattar, C. J. Packard, et al. 2009. Major lipids, apolipoproteins, and risk of vascular disease. J. Am. Med. Assoc. 302: 1993-2000.
5. McQueen, M. J., S. Hawken, X. Wang, S. Ounpuu, A. Sniderman, J. Probstfield, K. Steyn, J. E. Sanderson, M. Hasani, E. Volkova, et al. 2008. Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study): a case-control study. Lancet. 372: 224-233.
6. Nissen, S. E., J. C. Tardif, S. J. Nicholls, J. H. Revkin, C. L. Shear, W. T. Duggan, W. Ruzyllo, W. B. Bachinsky, G. P. Lasala, and E. M. Tuzcu. 2007. Effect of torcetrapib on the progression of coronary atherosclerosis. N. Engl. J. Med. 356: 1304-1316. [Erratum. 2007. N. Engl. J. Med. 357: 835.]
7. 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.
8. Schwartz, G. G., A. G. Olsson, M. Abt, C. M. Ballantyne, P. J. Barter, J. Brumm, B. R. Chaitman, I. M. Holme, D. Kallend, L. A. Leiter, et al.; dal-OUTCOMES Investigators. 2012. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N. Engl. J. Med. 367: 2089-2099.
9. Anderson, G. L., M. Limacher, A. R. Assaf, T. Bassford, S. A. Beresford, H. Black, D. Bonds, R. Brunner, R. Brzyski, B. Caan, et al.; Women's Health Initiative Steering Committee. 2004. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. J. Am. Med. Assoc. 291: 1701-1712.
10. Hulley, S., D. Grady, T. Bush, C. Furberg, D. Herrington, B. Riggs, and E. Vittinghoff. 1998. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. J. Am. Med. Assoc. 280: 605-613.
11. Hodis, H. N., W. J. Mack, S. P. Azen, R. A. Lobo, D. Shoupe, P. R. Mahrer, D. P. Faxon, L. Cashin-Hemphill, M. E. Sanmarco, W. J. French, et al.; Women's Estrogen-Progestin Lipid-Lowering Hormone Atherosclerosis Regression Trial Research Group. 2003. Hormone therapy and the progression of coronary-artery atherosclerosis in postmenopausal women. N. Engl. J. Med. 349: 535-545.
12. AIM-HIGH Investigators. 2011. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N. Engl. J. Med. 365: 2255-2267. [Erratum. 2012. N. Engl. J. Med. 367: 189.]
13. HPS2-THRIVE Collaborative Group. 2014. Effects of extended-release niacin with laropiprant in high-risk patients. N. Engl. J. Med. 371: 203-217.
14. Voight, B. F., G. M. Peloso, M. Orho-Melander, R. Frikke-Schmidt, M. Barbalic, M. K. Jensen, G. Hindy, H. Hólm, E. L. Ding, T. Johnson, et al. 2012. Plasma HDL cholesterol and risk of myocardial infarction: a Mendelian randomisation study. Lancet. 380: 572-580.
15. Sacks, F. M., P. Alaupovic, L. E. Moye, T. G. Cole, B. Sussex, M. J. Stampfer, M. A. Pfeffer, and E. Braunwald. 2000. VLDL, apoliproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) Trial. Circulation. 102: 1886-1892.
16. Vaisar, T., P. Mayer, E. Nilsson, X. Q. Zhao, R. Knopp, and B. J. Prazen. 2010. HDL in humans with cardiovascular disease exhibits a proteomic signature. Clin. Chim. Acta. 411: 972-979.
17. Jensen, M. K., E. B. Rimm, J. D. Furtado, and F. M. Sacks. 2012. Apolipoprotein C-III as a potential modulator of the association between HDL-cholesterol and incident coronary heart disease. J. Am. Heart Assoc. 1: jah3-e000232.
18. Campos, H., D. Perlov, C. Khoo, and F. M. Sacks. 2001. Distinct patterns of lipoproteins with apoB defined by presence of apoE or apo C-III in hypercholesterolemia and hypertriglyceridemia. J. Lipid Res. 42: 1239-1249.
19. Alaupovic, P. 1996. Significance of apolipoproteins for structure, function, and classification of plasma lipoproteins. Methods Enzymol. 263: 32-60.
20. Shah, A. S., L. Tan, J. L. Long, and W. S. Davidson. 2013. Proteomic diversity of high-density lipoproteins: our emerging understanding of its importance in lipid transport and beyond. J. Lipid Res. 54: 2575-2585.
21. Davidson, W. S., R. A. G. D. Silva, S. Chantepie, W. R. Lagor, M. J. Chapman, and A. Kontush. 2009. Proteomic analysis of defined HDL subpopulations reveals particle-specific protein clusters: relevance to antioxidative function. Arterioscler. Thromb. Vasc. Biol. 29: 870-876.
22. Gordon, S. M., J. Deng, L. J. Lu, and W. S. Davidson. 2010. Proteomic characterization of human plasma high density lipoprotein fractionated by gel filtration chromatography. J. Proteome Res. 9: 5239-5249.
23. Orsoni, A., S. Saheb, J. Levels, G. Dallinga-Thie, M. Atassi, R. Bittar, P. Robillard, E. Bruckert, A. Kontush, A. Carrie, et al. 2011. LDL-apheresis depletes apoE-HDL and pre-b1-HDL in familial hypercholesterolemia: relevance to atheroprotection. J. Lipid Res. 52: 2304-2313.
24. Zheng, C., C. Khoo, J. Furtado, and F. M. Sacks. 2010. Apolipoprotein C-III and the metabolic basis for hypertriglyceridemia and the dense low-density lipoprotein phenotype. Circulation. 121: 1722-1734.
25. Mendivil, C. O., E. B. Rimm, J. Furtado, and F. M. Sacks. 2013. Apolipoprotein E in VLDL and LDL with apolipoprotein C-III is associated with a lower risk of coronary heart disease. J. Am. Heart Assoc. 2: e000130 10.1161/JAHA.113.000130.
26. Hennessy, L. K., S. T. Kunitake, M. Jarvis, R. L. Hamilton, G. Endeman, A. Protter, and J. P. Kane. 1997. Isolation of subpopulations of high density lipoproteins: three particle species containing apoE and two species devoid of apoE that have affinity for heparin. J. Lipid Res. 38: 1859-1868.
27. Asztalos, B. F., E. J. Schaefer, K.V. Horvath, S. Yamashita, M. Miller, G. Franceschini, and L. Calabresi. 2007. Role of LCAT in HDL remodeling: investigation of LCAT deficiency states. J. Lipid Res. 48: 592-599.
28. Krimbou, L., M. Marcil, H. Chiba, and J. Genest, Jr. 2003. Structural and functional properties of human plasma high density-sized lipoprotein containing only apoE particles. J. Lipid Res. 44: 884-892.
29. Rye, K. A., R. Bright, M. Psaltis, and P. J. Barter. 2006. Regulation of reconstituted high density lipoprotein structure and remodeling by apolipoprotein E. J. Lipid Res. 47: 1025-1036.
30. Weisgraber, K. H., and R. W. Mahley. 1980. Subfractionation of human high density lipoproteins by heparin-Sepharose affinity chromatography. J. Lipid Res. 21: 316-325.
31. Hannuksela, M. L., M. E. Brousseau, S. M. Meyn, H. Nazih, G. Bader, R. D. Shamburek, P. Alaupovic, and H. B. Brewer, Jr. 2002. In vivo metabolism of apolipoprotein E within the HDL subpopulations LpE, LpE:A-I, LpE:A-II and LpE:A-I:A-II. Atherosclerosis. 165: 205-220.
32. Castro, G. R., and C. J. Fielding. 1984. Evidence for the distribution of apolipoprotein E between lipoprotein classes in human normocholesterolemic plasma and for the origin of unassociated apolipoprotein E (Lp-E). J. Lipid Res. 25: 58-67.
33. Bekaert, E. D., P. Alaupovic, C. Knight-Gibson, P. Blackett, and M. Ayrault-Jarrier. 1991. Composition of plasma ApoA-I-containing lipoprotein particles in children and adults. Pediatr. Res. 29: 315-321.
34. Chan, D. C., M. N. Nguyen, G. F. Watts, and P. H. Barrett. 2008. Apolipoprotein C-III transport in centrally obese men: associations with very low-density lipoprotein apolipoprotein B and high-density lipoprotein apolipoprotein A-I metabolism. J. Clin. Endocrinol. Metab. 93: 557-564.
35. Onat, A., G. Hergenc¸, E. Ayhan, M. U ur, H. Kaya, M. Tuncer, and G. Can. 2009. Serum apolipoprotein C-III in high-density lipoprotein: a key diabetogenic risk factor in Turks. Diabet. Med. 26: 981-988.
36. Cohn, J. S., M. Tremblay, R. Batal, H. Jacques, C. Rodriguez, G. Steiner, O. Mamer, and J. Davignon. 2004. Increased apoC-III production is a characteristic feature of patients with hypertriglyceridemia. Atherosclerosis. 177: 137-145.
37. Sacks, F. M., G. A. Bray, V. J. Carey, S. R. Smith, D. H. Ryan, S. D. Anton, K. McManus, C. M. Champagne, L. M. Bishop, N. Laranjo, et al. 2009. Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N. Engl. J. Med. 360: 859-873.
38. Khoo, C., H. Judge, and F. M. Sacks. 1999. Effects of estrogenic oral contraceptives on the lipoprotein B particle system defined by apolipoproteins E and C-III content. J. Lipid Res. 40: 202-212.
39. Cohn, J. S., C. Rodriguez, H. Jacques, M. Tremblay, and J. Davignon. 2004. Storage of human plasma samples leads to alterations in the lipoprotein distribution of apoC-III and apoE. J. Lipid Res. 45: 1572-1579.
40. Rosenson, R. S., H. B. Brewer, Jr., M. J. Chapman, S. Fazio, M. M. Hussain, A. Kontush, R. M. Krauss, J. D. Otvos, A. T. Remaley, and E. J. Schaefer. 2011. HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin. Chem. 57: 392-410.
41. Warnick, G. R., J. R. McNamara, C. N. Boggess, F. Clendenen, P. T. Williams, and C. C. Landolt. 2006. Polyacrylamide gradient gel electrophoresis of lipoprotein subclasses. Clin. Lab. Med. 26: 803-846.
42. Kawakami, A., M. Aikawa, P. Libby, P. Alcaide, F. W. Luscinskas, and F. M. Sacks. 2006. Apolipoprotein CIII in apolipoprotein B lipoproteins enhances the adhesion of human monocytic cells to endothelial cells. Circulation. 113: 691-700.
43. Tian, L., J. Jia, F. Mingde, Y. Tian, Y. Xu, H. Tian, and Y. Yang. 2006. Alterations of high density lipoprotein subclasses in obese subjects. Lipids. 41: 789-796.
44. Després, J. P., S. Moorjani, P. J. Lupien, A. Tremblay, A. Nadeau, and C. Bouchard. 1990. Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease. Arteriosclerosis. 10: 497-511.
45. Williams, P. T., W. L. Haskell, K. M. Vranizan, and R. M. Krauss. 1995. The associations of high-density lipoprotein subclasses with insulin and glucose levels, physical activity, resting heart rate, and regional adiposity in men with coronary artery disease: the Stanford Coronary Risk Intervention Project baseline survey. Metabolism. 44: 106-114.
46. Sasahara, T., T. Yamashita, D. Sviridov, N. Fidge, and P. Nestel. 1997. Altered properties of high density lipoprotein subfractions in obese subjects. J. Lipid Res. 38: 600-611.
47. Bertière, M. C., F. Fumeron, D. Rigaud, D. Malon, M. Apfelbaum, and A. Girard-Globa. 1988. Low high density lipoprotein-2 concentrations in obese male subjects. Atherosclerosis. 73: 57-61.
48. Miida, T., Y. Nakamura, K. Inano, T. Matsuto, T. Yamaguchi, T. Tsuda, and M. Okada. 1996. Pre beta 1-high-density lipoprotein increases in coronary artery disease. Clin. Chem. 42: 1992-1995.
49. Wilson, H. M., J. C. Patel, D. Russell, and E. R. Skinner. 1993. Alterations in the concentration of an apolipoprotein E-containing subfraction of plasma high-density lipoprotein in coronary heart disease. Clin. Chim. Acta. 220: 175-187.
50. Mahley, R. W. 1988. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science. 240: 622-630.
51. Ji, Z. S., S. Fazio, Y. L. Lee, and R. W. Mahley. 1994. Secretion-capture role for apolipoprotein E in remnant lipoprotein metabolism involving cell surface heparan sulfate proteoglycans. J. Biol. Chem. 269: 2764-2772.
52. Matthews, D. R., J. P. Hosker, A. S. Rudenski, B. A. Naylor, D. F. Treacher, and R. C. Turner. 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 28: 412-419.