Enhanced atheroprotection and lesion remodelling by targeting the foam cell and increasing plasma cholesterol acceptors

Cardiovascular Research

Volumn 109, Issue 2, 2016, Pages 294-304

  Son, Se Hee ^a   Goo, Young Hwa ^a   Choi, Mihyun ^a   Saha, Pradip K ^b   Oka, Kazuhiro ^b   Chan, Lawrence C B ^b   Paul, Antoni ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Apolipoprotein A I; Atherosclerosis; Foam cell; Lipid droplet; Perilipin 2; Reverse cholesterol transport

Indexed keywords

APOLIPOPROTEIN A1; CHOLESTEROL; COLLAGEN; FAT DROPLET; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PERILIPIN; PERILIPIN 2; UNCLASSIFIED DRUG; ADIPOPHILIN; APOLIPOPROTEIN E; CHOLESTEROL ESTER; PLIN2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROMA; ATHEROSCLEROSIS; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; FEMALE; FOAM CELL; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOLIPOPROTEIN A-I; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BIOLOGICAL TRANSPORT; CHOLESTEROL; CHOLESTEROL ESTERS; FOAM CELLS; LIPOPROTEINS, HDL; MACROPHAGES; MICE, KNOCKOUT; PERILIPIN-2;

EID: 84959887295     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv241     Document Type: Article

References (42)

1. Glass CK, Witztum JL. Atherosclerosis: The road ahead. Cell 2001;104:503-516.
2. Paul A, Chang BH, Li L, Yechoor VK, Chan L. Deficiency of adipose differentiationrelated protein impairs foam cell formation and protects against atherosclerosis. Circ Res 2008;102:1492-1501.
3. Kimmel AR, Brasaemle DL, Andrews-Hill M, Sztalryd C, Londos C. Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J Lipid Res 2010;51:468-471.
4. Xu G, Sztalryd C, Lu X, Tansey JT, Gan J, Dorward H, Kimmel AR, Londos C. Posttranslational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway. J Biol Chem 2005;280:42841-42847.
5. Straub BK, Gyoengyoesi B, Koenig M, Hashani M, Pawella LM, Herpel E, Mueller W, Macher-Goeppinger S, Heid H, Schirmacher P. Adipophilin/perilipin-2 as a lipid droplet-specific marker for metabolically active cells and diseases associated with metabolic dysregulation. Histopathology 2013;62:617-631.
6. Chang BH-J, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiationrelated protein. Mol Cell Biol 2006;26:1063-1076.
7. Bosma M, Hesselink MKC, Sparks LM, Timmers S, Ferraz MJ, Mattijssen F, van Beurden D, Schaart G, de Baets MH, Verheyen FK, Kersten S, Schrauwen P. Perilipin 2 improves insulin sensitivity in skeletal muscle despite elevated intramuscular lipid levels. Diabetes 2012;61:2679-2690.
8. Imanishi Y, Sun W, Maeda T, Maeda A, Palczewski K. Retinyl ester homeostasis in the adipose differentiation-related protein-deficient retina. J Biol Chem 2008;283: 25091-25102.
9. Dahlhoff M, Camera E, Picardo M, Zouboulis CC, Chan L, Chang BH-J, Schneider MR. PLIN2, the major perilipin regulated during sebocyte differentiation, controls sebaceous lipid accumulation in vitro and sebaceous gland size in vivo. Bioch Biophys Acta-Gen Subj 2013;1830:4642-4649.
10. Larigauderie G, Furman C, Jaye M, Lasselin C, Copin C, Fruchart JC, Castro G, Rouis M. Adipophilin enhances lipid accumulation and prevents lipid efflux from THP-1 macrophages: potential role in atherogenesis. Arterioscler Thromb Vasc Biol 2004;24:504-510.
11. Son SH, Goo YH, Chang BH, Paul A. Perilipin 2 (PLIN2)-deficiency does not increase cholesterol-induced toxicity in macrophages. PLoS ONE 2012;7:e33063.
12. Cuchel M, Rader DJ. Macrophage reverse cholesterol transport: key to the regression of atherosclerosis? Circulation 2006;113:2548-2555.
13. Tall AR. Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J Intern Med 2008;263:256-273.
14. Gordon DJ, Rifkind BM. High-density lipoprotein-The clinical implications of recent studies. N Engl J Med 1989;321:1311-1316.
15. Plump AS, Scott CJ, Breslow JL. Human apolipoprotein A-I gene expression increases high density lipoprotein and suppresses atherosclerosis in the apolipoprotein E-deficient mouse. Proc Natl Acad Sci USA 1994;91:9607-9611.
16. Pászty C, Maeda N, Verstuyft J, Rubin EM. Apolipoprotein AI transgene corrects apolipoprotein E deficiency-induced atherosclerosis in mice. J Clin Invest 1994;94:899-903.
17. Tangirala RK, Tsukamoto K, Chun SH, Usher D, Puré E, Rader DJ. Regression of atherosclerosis induced by liver-directed gene transfer of apolipoprotein A-I in mice. Circulation 1999;100:1816-1822.
18. Rong JX, Li J, Reis ED, Choudhury RP, Dansky HM, Elmalem VI, Fallon JT, Breslow JL, Fisher EA. Elevating high-density lipoprotein cholesterol in apolipoprotein E-deficient mice remodels advanced atherosclerotic lesions by decreasing macrophage and increasing smooth muscle cell content. Circulation 2001;104:2447-2452.
19. Pastore L, Belalcazar LM, Oka K, Cela R, Lee B, Chan L, Beaudet AL. Helper-dependent adenoviral vector-mediated long-Term expression of human apolipoprotein A-I reduces atherosclerosis in apo E-deficient mice. Gene 2004;327:153-160.
20. Belalcazar LM, Merched A, Carr B, Oka K, Chen KH, Pastore L, Beaudet A, Chan L. Long-Term stable expression of human apolipoprotein A-I mediated by helperdependent adenovirus gene transfer inhibits atherosclerosis progression and remodels atherosclerotic plaques in a mouse model of familial hypercholesterolemia. Circulation 2003;107:2726-2732.
21. Oka K, Belalcazar LM, Dieker C, Nour EA, Nuno-Gonzalez P, Paul A, Cormier S, Shin JK, Finegold M, Chan L. Sustained phenotypic correction in a mouse model of hypoalphalipoproteinemia with a helper-dependent adenovirus vector. Gene Ther 2007; 14:191-202.
22. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 1987;68:231-240.
23. Goo Y-H, Son S-H, Kreienberg PB, Paul A. Novel lipid droplet-Associated serine hydrolase regulates macrophage cholesterol mobilization. Arterioscler Thromb Vasc Biol 2014;34:386-396.
24. Zhang Y, Da Silva JR, Reilly M, Billheimer JT, Rothblat GH, Rader DJ. Hepatic expression of scavenger receptor class B type I (SR-BI) is a positive regulator of macrophage reverse cholesterol transport in vivo. J Clin Invest 2005;115:2870-2874.
25. Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, Parathath S, van Gils JM, Rayner AJ, Chang AN, Suarez Y, Fernandez-Hernando C, Fisher EA, Moore KJ. Antagonismof miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 2011;121:2921-2931.
26. Schaefer EJ, Lamon-Fava S, Ordovas JM, Cohn SD, Schaefer MM, Castelli WP, Wilson PW. Factors associated with low and elevated plasma high density lipoprotein cholesterol and apolipoprotein A-I levels in the Framingham Offspring Study. J Lipid Res 1994;35:871-882.
27. Van Craeyveld E, Gordts S, Nefyodova E, Jacobs F, De Geest B. Regression and stabilization of advanced murine atherosclerotic lesions: A comparison of LDL lowering and HDL raising gene transfer strategies. J Mol Med 2011;89:555-567.
28. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler Thromb 1994;14:141-147.
29. Ouimet M, Marcel YL. Regulation of lipid droplet cholesterol efflux from macrophage foam cells. Arterioscler Thromb Vasc Biol 2012;32:575-581.
30. Gordon DJ, Probstfield JL, Garrison RJ, Neaton JD, Castelli WP, Knoke JD, Jacobs DR, Bangdiwala S, Tyroler HA. High-density lipoprotein cholesterol and cardiovascular disease. Four Prospective American Studies. Circulation 1989;79:8-15.
31. Tuteja S, Rader DJ. High-density lipoproteins in the prevention of cardiovascular disease: changing the paradigm. Clin Pharmacol Ther 2014;96:48-56.
32. Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ. Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 2011;364:127-135.
33. Carr RM, Peralta G, Yin X, Ahima RS. Absence of perilipin 2 prevents hepatic steatosis, glucose intolerance and ceramide accumulation in alcohol-fed mice. PLoS ONE. 2014;9: e97118.
34. Chang BH-J, Li L, Saha P, Chan L. Absence of adipose differentiation related protein upregulates hepatic VLDL secretion, relieves hepatosteatosis, and improves whole body insulin resistance in leptin-deficient mice. J Lipid Res 2010;51:2132-2142.
35. McManaman JL, Bales ES, Orlicky DJ, Jackman M, MacLean PS, Cain S, Crunk AE, Mansur A, Graham CE, Bowman TA, Greenberg AS. Perilipin-2-null mice are protected against diet-induced obesity, adipose inflammation, and fatty liver disease. J Lipid Res 2013;54:1346-1359.
36. Carr SC, Farb A, Pearce WH, Virmani R, Yao JST. Activated inflammatory cells are associated with plaque rupture in carotid artery stenosis. Surgery 1997;122:757-763.
37. Rekhter MD. Collagen synthesis in atherosclerosis: Too much and not enough. Cardiovasc Res 1999;41:376-384.
38. Choudhury RP, Rong JX, Trogan E, Elmalem VI, Dansky HM, Breslow JL, Witztum JL, Fallon JT, Fisher EA. High-density lipoproteins retard the progression of atherosclerosis and favorably remodel lesions without suppressing indices of inflammation or oxidation. Arterioscler Thromb Vasc Biol 2004;24:1904-1909.
39. Reimers GJ, Jackson CL, Rickards J, Chan PY, Cohn JS, Rye K-A, Barter PJ, Rodgers KJ. Inhibition of rupture of established atherosclerotic plaques by treatment with apolipoprotein A-I. Cardiovasc Res 2011;91:37-44.
40. Out R, HoekstraM, Habets K, Meurs I, deWaard V, Hildebrand RB, Wang Y, Chimini G, Kuiper J, Van Berkel TJ, Van Eck M. Combined deletion of macrophage ABCA1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels. Arterioscler Thromb Vasc Biol 2008; 28:258-264.
41. Van Eck M, Singaraja RR, Ye D, Hildebrand RB, James ER, Hayden MR, Van Berkel TJC. Macrophage ATP-binding cassette transporter A1 overexpression inhibits atherosclerotic lesion progression in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2006;26:929-934.
42. Fu Y, Mukhamedova N, Ip S, DSouza W, Henley Katya J, DiTommaso T, Kesani R, Ditiatkovski M, Jones L, Lane Rachael M, Jennings G, Smyth Ian M, Kile Benjamin T, Sviridov D. ABCA12 regulates ABCA1-dependent cholesterol efflux from macrophages and the development of atherosclerosis. Cell Metab 2013;18:225-238.