Retinol-binding protein-dependent cholesterol uptake regulates macrophage foam cell formation and promotes atherosclerosis

Circulation

Volumn 135, Issue 14, 2017, Pages 1339-1354

  Liu, Yan ^a,b   Zhong, Yuan ^a   Chen, Hongen ^a   Wang, Duan ^a   Wang, Min ^a   Ou, Jing Song ^a   Xia, Min ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

atherosclerosis; CD36; cholesterol uptake; RBP4

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOTENSIN RECEPTOR ANTAGONIST; APOLIPOPROTEIN E; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CD36 ANTIGEN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PROTEIN KINASE C; PROTEIN KINASE P60; RETINOIC ACID; RETINOL BINDING PROTEIN 4; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 4; CARRIER PROTEIN; CHOLESTEROL-BINDING PROTEIN; PANCREATIC ELASTASE; PLASMA RETINOL BINDING PROTEIN; RBP4 PROTEIN, MOUSE;

ADVERSE OUTCOME; AGE; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL STIMULATION; CHOLESTEROL TRANSPORT; DIABETES MELLITUS; DISEASE COURSE; FOAM CELL; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYPERTENSION; MACROPHAGE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PREDICTIVE VALUE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; UPREGULATION; ANIMAL; C57BL MOUSE; COHORT ANALYSIS; DEFICIENCY; HUMAN; MALE; METABOLISM; PATHOLOGY; PROSPECTIVE STUDY;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CARRIER PROTEINS; COHORT STUDIES; FOAM CELLS; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PANCREATIC ELASTASE; PROSPECTIVE STUDIES; RETINOL-BINDING PROTEINS, PLASMA;

EID: 85011277367     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.116.024503     Document Type: Article

References (43)

1. Blaner WS. Retinol-binding protein: the serum transport protein for vitamin A. Endocr Rev. 1989; 10: 308-316. doi: 10.1210/edrv-10-3-308.
2. Newcomer ME, Ong DE. Plasma retinol binding protein: structure and function of the prototypic lipocalin. Biochim Biophys Acta. 2000; 1482: 57-64.
3. Graham TE, Yang Q, Blüher M, Hammarstedt A, Ciaraldi TP, Henry RR, Wason CJ, Oberbach A, Jansson PA, Smith U, Kahn BB. Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med. 2006; 354: 2552-2563. doi: 10.1056/NEJMoa054862.
4. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L, Kahn BB. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature. 2005; 436: 356-362. doi: 10.1038/nature03711.
5. Farjo KM, Farjo RA, Halsey S, Moiseyev G, Ma JX. Retinol-binding protein 4 induces inflammation in human endothelial cells by an NADPH oxidase- And nuclear factor kappa B-dependent and retinol-independent mechanism. Mol Cell Biol. 2012; 32: 5103-5115. doi: 10.1128/MCB.00820-12.
6. Wang J, Chen H, Liu Y, Zhou W, Sun R, Xia M. Retinol binding protein 4 induces mitochondrial dysfunction and vascular oxidative damage. Atherosclerosis. 2015; 240: 335-344. doi: 10.1016/j.atherosclerosis.2015.03.036.
7. Solini A, Santini E, Madec S, Rossi C, Muscelli E. Retinol-binding protein-4 in women with untreated essential hypertension. Am J Hypertens. 2009; 22: 1001-1006. doi: 10.1038/ajh.2009.116.
8. Sasaki M, Otani T, Kawakami M, Ishikawa SE. Elevation of plasma retinol-binding protein 4 and reduction of plasma adiponectin in subjects with cerebral infarction. Metabolism. 2010; 59: 527-532. doi: 10.1016/j.metabol.2009.08.015.
9. Sun Q, Kiernan UA, Shi L, Phillips DA, Kahn BB, Hu FB, Manson JE, Albert CM, Rexrode KM. Plasma retinol-binding protein 4 (RBP4) levels and risk of coronary heart disease: a prospective analysis among women in the nurses? health study. Circulation. 2013; 127: 1938-1947. doi: 10.1161/CIRCULATIONAHA. 113.002073.
10. Lusis AJ. Atherosclerosis. Nature. 2000; 407: 233-241. doi: 10.1038/35025203.
11. Yu XH, Fu YC, Zhang DW, Yin K, Tang CK. Foam cells in atherosclerosis. Clin Chim Acta. 2013; 424: 245-252. doi: 10.1016/j.cca.2013.06.006.
12. Kunjathoor VV, Febbraio M, Podrez EA, Moore KJ, Andersson L, Koehn S, Rhee JS, Silverstein R, Hoff HF, Freeman MW. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem. 2002; 277: 49982-49988. doi: 10.1074/jbc.M209649200.
13. Ghosh S, Zhao B, Bie J, Song J. Macrophage cholesteryl ester mobilization and atherosclerosis. Vascul Pharmacol. 2010; 52: 1-10. doi: 10.1016/j.vph.2009.10.002.
14. Westerterp M, Bochem AE, Yvan-Charvet L, Murphy AJ, Wang N, Tall AR. ATP-binding cassette transporters, atherosclerosis, and inflammation. Circ Res. 2014; 114: 157-170. doi: 10.1161/CIRCRESAHA. 114.300738.
15. Li AC, Glass CK. The macrophage foam cell as a target for therapeutic intervention. Nat Med. 2002; 8: 1235-1242. doi: 10.1038/nm1102-1235.
16. Liu Y, Mu D, Chen H, Li D, Song J, Zhong Y, Xia M. Retinol-binding protein 4 induces hepatic mitochondrial dysfunction and promotes hepatic steatosis. J Clin Endocrinol Metab. 2016; 101: 4338-4348. doi: 10.1210/jc.2016-1320.
17. Kotla S, Singh NK, Traylor JG Jr, Orr AW, Rao GN. ROS-dependent Syk and Pyk2-mediated STAT1 activation is required for 15(S)-hydroxyeicosatetraenoic acid-induced CD36 expression and foam cell formation. Free Radic Biol Med. 2014; 76: 147-162. doi: 10.1016/j.freeradbiomed.2014.08.007.
18. Wei ZZ, Yu SP, Lee JH, Chen D, Taylor TM, Deveau TC, Yu AC, Wei L. Regulatory role of the JNK-STAT1/3 signaling in neuronal differentiation of cultured mouse embryonic stem cells. Cell Mol Neurobiol. 2014; 34: 881-893. doi: 10.1007/s10571-014-0067-4.
19. Sumara G, Belwal M, Ricci R. "Jnking" atherosclerosis. Cell Mol Life Sci. 2005; 62: 2487-2494. doi: 10.1007/s00018-005-5253-6.
20. Wang Y, Botvinick EL, Zhao Y, Berns MW, Usami S, Tsien RY, Chien S. Visualizing the mechanical activation of Src. Nature. 2005; 434: 1040-1045. doi: 10.1038/nature03469.
21. Xia M, Ling W, Zhu H, Wang Q, Ma J, Hou M, Tang Z, Li L, Ye Q. Anthocyanin prevents CD40-Activated proinflammatory signaling in endothelial cells by regulating cholesterol distribution. Arterioscler Thromb Vasc Biol. 2007; 27: 519-524. doi: 10.1161/01. ATV.0000254672.04573.2d.
22. Isken A, Golczak M, Oberhauser V, Hunzelmann S, Driever W, Imanishi Y, Palczewski K, von Lintig J. RBP4 disrupts vitamin A uptake homeostasis in a STRA6-deficient animal model for Matthew-Wood syndrome. Cell Metab. 2008; 7: 258-268. doi: 10.1016/j.cmet.2008.01.009.
23. Norseen J, Hosooka T, Hammarstedt A, Yore MM, Kant S, Aryal P, Kiernan UA, Phillips DA, Maruyama H, Kraus BJ, Usheva A, Davis RJ, Smith U, Kahn BB. Retinol-binding protein 4 inhibits insulin signaling in adipocytes by inducing proinflammatory cytokines in macrophages through a c-Jun N-Terminal kinase- And toll-like receptor 4-dependent and retinol-independent mechanism. Mol Cell Biol. 2012; 32: 2010-2019. doi: 10.1128/MCB.06193-11.
24. Kläting N, Graham TE, Berndt J, Kralisch S, Kovacs P, Wason CJ, Fasshauer M, Schän MR, Stumvoll M, Blüher M, Kahn BB. Serum retinol-binding protein is more highly expressed in visceral than in subcutaneous adipose tissue and is a marker of intra-Abdominal fat mass. Cell Metab. 2007; 6: 79-87. doi: 10.1016/j.cmet.2007.06.002.
25. Bobbert T, Raila J, Schwarz F, Mai K, Henze A, Pfeiffer AF, Schweigert FJ, Spranger J. Relation between retinol, retinol-binding protein 4, transthyretin and carotid intima media thickness. Atherosclerosis. 2010; 213: 549-551. doi: 10.1016/j.atherosclerosis. 2010.07.063.
26. Ingelsson E, Sundsträm J, Melhus H, Michaëlsson K, Berne C, Vasan RS, Risérus U, Blomhoff R, Lind L, Arnläv J. Circulating retinolbinding protein 4, cardiovascular risk factors and prevalent cardiovascular disease in elderly. Atherosclerosis. 2009; 206: 239-244. doi: 10.1016/j.atherosclerosis.2009.02.029.
27. Feng S, Zhu Y, Yan C, Wang Y, Zhang Z. Retinol binding protein 4 correlates with and is an early predictor of carotid atherosclerosis in type 2 diabetes mellitus patients. J Biomed Res. 2015; 29: 451-455. doi: 10.7555/JBR.29.20140087.
28. Liu Y, Wang D, Chen H, Xia M. Circulating retinol binding protein 4 is associated with coronary lesion severity of patients with coronary artery disease. Atherosclerosis. 2015; 238: 45-51. doi: 10.1016/j.atherosclerosis.2014.11.016.
29. Fuster JJ, Ouchi N, Gokce N, Walsh K. Obesity-induced changes in adipose tissue microenvironment and their impact on cardiovascular disease. Circ Res. 2016; 118: 1786-1807. doi: 10.1161/CIRCRESAHA.115.306885.
30. Linton MF, Atkinson JB, Fazio S. Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science. 1995; 267: 1034-1037.
31. Chistiakov DA, Bobryshev YV, Orekhov AN. Macrophage-mediated cholesterol handling in atherosclerosis. J Cell Mol Med. 2016; 20: 17-28. doi: 10.1111/jcmm.12689.
32. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell. 2001; 104: 503-516.
33. Abroun S, Saki N, Ahmadvand M, Asghari F, Salari F, Rahim F. STATs: an old story, yet mesmerizing. Cell J. 2015; 17: 395-411.
34. Sehgal PB. Paradigm shifts in the cell biology of STAT signaling. Semin Cell Dev Biol. 2008; 19: 329-340. doi: 10.1016/j.semcdb.2008.07.003.
35. Schneider JG, Finck BN, Ren J, Standley KN, Takagi M, Maclean KH, Bernal-Mizrachi C, Muslin AJ, Kastan MB, Semenkovich CF. ATM-dependent suppression of stress signaling reduces vascular disease in metabolic syndrome. Cell Metab. 2006; 4: 377-389. doi: 10.1016/j.cmet.2006.10.002.
36. Martin GS. The hunting of the Src. Nat Rev Mol Cell Biol. 2001; 2: 467-475. doi: 10.1038/35073094.
37. Mukherjee A, Arnaud L, Cooper JA. Lipid-dependent recruitment of neuronal Src to lipid rafts in the brain. J Biol Chem. 2003; 278: 40806-40814. doi: 10.1074/jbc.M306440200.
38. Holzer RG, Park EJ, Li N, Tran H, Chen M, Choi C, Solinas G, Karin M. Saturated fatty acids induce c-Src clustering within membrane subdomains, leading to JNK activation. Cell. 2011; 147: 173-184. doi: 10.1016/j.cell.2011.08.034.
39. Blomhoff R, Blomhoff HK. Overview of retinoid metabolism and function. J Neurobiol. 2006; 66: 606-630. doi: 10.1002/neu.20242.
40. Kawaguchi R, Yu J, Honda J, Hu J, Whitelegge J, Ping P, Wiita P, Bok D, Sun H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science. 2007; 315: 820-825. doi: 10.1126/science.1136244.
41. Berry DC, Jin H, Majumdar A, Noy N. Signaling by vitamin A and retinol-binding protein regulates gene expression to inhibit insulin responses. Proc Natl Acad Sci U S A. 2011; 108: 4340-4345. doi: 10.1073/pnas.1011115108.
42. Moore KJ, Sheedy FJ, Fisher EA. Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol. 2013; 13: 709-721. doi: 10.1038/nri3520.
43. Higashimori M, Tatro JB, Moore KJ, Mendelsohn ME, Galper JB, Beasley D. Role of toll-like receptor 4 in intimal foam cell accumulation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2011; 31: 50-57. doi: 10.1161/ATVBAHA.110.210971.