Nicotine potentiates proatherogenic effects of oxLDL by stimulating and upregulating macrophage CD36 signaling

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 4, 2013, Pages

  Zhou, Ming Sheng ^a,b   Chadipiralla, Kiranmai ^b   Mendez, Armando J ^b   Jaimes, Edgar A ^c   Silverstein, Roy L ^d   Webster, Keith ^b   Raij, Leopoldo ^b  

^a JINZHOU MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

CD36; Foam cell; Inflammatory cytokine; Macrophage; Nicotine

Indexed keywords

APOLIPOPROTEIN E; CD14 ANTIGEN; CD36 ANTIGEN; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINE; OXIDIZED LOW DENSITY LIPOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE C DELTA; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR RISK; CELL POPULATION; CELL STIMULATION; CONTROLLED STUDY; FOAM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIPID STORAGE; LIPID TRANSPORT; MACROPHAGE; MACROPHAGE ACTIVATION; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

CD36; FOAM CELL; INFLAMMATORY CYTOKINE; MACROPHAGE; NICOTINE;

ANIMALS; ANTIGENS, CD14; ANTIGENS, CD36; ANTIOXIDANTS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL LINE; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FOAM CELLS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MICE, KNOCKOUT; NICOTINE; PLAQUE, ATHEROSCLEROTIC; PPAR GAMMA; PROTEIN KINASE C-DELTA; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84881625230     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00042.2013     Document Type: Article

References (59)

1. Abe T, Shimamura M, Jackman K, Kurinami H, Anrather J, Zhou P, Iadecola C. Key role of CD36 in Toll-like receptor 2 signaling in cerebral ischemia. Stroke 41: 898-904, 2010.
2. Chelland Campbell S, Moffatt RJ, Stamford BA. Smoking and smoking cessation-the relationship between cardiovascular disease and lipoprotein metabolism: a review. Atherosclerosis 201: 225-235, 2008.
3. Collot-Teixeira S, Martin J, McDermott-Roe C, Poston R, McGregor JL. CD36 and macrophages in atherosclerosis. Cardiovasc Res 75: 468-477, 2007.
4. Cornhill JF, Barrett WA, Herderick EE, Mahley RW, Fry DL. Topographic study of sudanophilic lesions in cholesterol-fed minipigs by image analysis. Atherosclerosis 5: 415-426, 1985.
5. de Winther MP, van Dijk KW, Havekes LM, Hofker MH. Macrophage scavenger receptor class A: a multifunctional receptor in atherosclerosis. Atheroscler Thromb Vasc Biol 20: 290-297, 2000.
6. Dressman J, Kincer J, Matveev SV, Guo L, Greenberg RN, Guerin T, Meade D, Li XA, Zhu W, Uittenbogaard A, Wilson ME, Smart EJ. HIV protease inhibitors promote atherosclerotic lesion formation independent of dyslipidemia by increasing CD36-dependent cholesteryl ester accumulation in macrophages. J Clin Invest 111: 389-397, 2003.
7. Erhardt L. Cigarette smoking: an undertreated risk factor for cardiovascular diseases. Atherosclerosis 205: 23-32 2009.
8. Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 108: 785-791, 2001.
9. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF, Sharma K, Silverstein RL. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 105: 1049-1056, 2000.
10. Feng J, Han J, Pearce SF, Silverstein RL, Gotto AM Jr, Hajjar DP, Nicholson AC. Induction of CD36 expression by oxidized LDL and IL-4 by a common signaling pathway dependent on protein kinase C and PPAR-gamma. J Lipid Res 41: 688-696, 2000.
11. Fuhrman B, Volkova N, Aviram M. Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis 161: 307-316, 2002.
12. Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, Kobayashi M, Tobe K. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 58: 2574-2582, 2009.
13. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661, 2010.
14. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964, 2005.
15. Han J, Hajjar DP, Febbraio M, Nicholson AC. Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J Biol Chem 272: 21654-21659, 1997.
16. Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, Tsao PS, Johnson FL, Cooke JP. Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 7: 833-839, 2001.
17. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zèahringer U, Beutler B. CD36 is a sensor of diacylglycerides. Nature 433: 523-527, 2005.
18. Jaimes EA, DeMaster EG, Tian RX, Raij L. Stable compounds of cigarette smoke induce endothelial superoxide anion production via NADPH oxidase activation. Arterioscler Thromb Vasc Biol 24: 1031-1036, 2004.
19. Jaimes EA, Tian RX, Raij L. Nicotine: the link between cigarette smoking and the progression of renal injury? Am J Physiol Heart Circ Physiol 292: H76-H82, 2007.
20. Jefferis BJ, Lowe GD, Welsh P, Rumley A, Lawlor DA, Ebrahim S, Carson C, Doig M, Feyerabend C, McMeekin L, Wannamethee SG, Cook DG, Whincup PH. Secondhand smoke (SHS) exposure is associated with circulating markers of inflammation and endothelial function in adult men and women. Atherosclerosis 208: 550-556, 2010.
21. Keidar S, Heinrich R, Kaplan M, Hayek T, Aviram M. Angiotensin II administration to atherosclerotic mice increases macrophage uptake of oxidized ldl: a possible role for interleukin-6. Arterioscler Thromb Vasc Biol 21: 1464-1469, 2001.
22. Kennedy DJ, Kuchibhotla S, Westfall KM, Silverstein RL, Morton RE, Febbraio M. A CD36-dependent pathway enhances macrophage and adipose tissue inflammation and impairs insulin signaling. Cardiovasc Res 89: 604-613, 2011.
23. 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 277: 49982-49988, 2002.
24. Lau PP, Li L, Merched AJ, Zhang AL, Ko KW, Chan L. Nicotine induces proinflammatory responses in macrophages and the aorta leading to acceleration of atherosclerosis in low-density lipoprotein receptor(-/-) mice. Arterioscler Thromb Vasc Biol 26: 143-149, 2006.
25. Lee J, Cooke JP. The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis 215: 281-283, 2011.
26. Lewis S, Surbramanian G, Pandey S, Udupa N. Pharmacokinetic evaluation of a developed nicotine transdermal system. Indian J Pharm Sci 69: 309-312, 2007.
27. Ley K, Miller YI, Hedric CC. Monocyte and macrophage dynamics during atherosclerosis. Arterioscler Thromb Vasc Biol 31: 1506-1516, 2011.
28. Libby P, Pidker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 473: 317-325, 2011.
29. Lin CS, Lin FY, Ho LJ, Tsai CS, Cheng SM, Wu WL, Huang CY, Lian CH, Yang SP, Lai JH. PKCd signalling regulates SR-A and CD36 expression and foam cell formation. Cardiovasc Res 95: 346-355, 2012.
30. Manning-Tobin JJ, Moore KJ, Seimon TA, Bell SA, Sharuk M, Alvarez-Leite JI, de Winther MP, Tabas I, Freeman MW. Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice. Arterioscler Thromb Vasc Biol 29: 19-26, 2009.
31. Martâin-Fuentes P, Civeira F, Recalde D, Garcâia-Otâin AL, Jarauta E, Marzo I, Cenarro A. Individual variation of scavenger receptor expression in human macrophages with oxidized low-density lipoprotein is associated with a differential inflammatory response. J Immunol 179: 3242-3248, 2007.
32. Moore KJ, Freeman MW. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol 26: 1702-1711, 2006.
33. Moore KJ, Kunjathoor VV, Koehn SL, Manning JJ, Tseng AA, Silver JM, McKee M, Freeman MW. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest 115: 2192-2201, 2005.
34. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969, 2008.
35. Ockene IS, Miller NH. Cigarette smoking, cardiovascular disease, and stroke: a statement for healthcare professionals from the American Heart Association. American Heart Association Task Force on Risk Reduction. Circulation 96: 3243-3247, 1997.
36. Pamukcu B, Lip GY, Devitt A, Griffiths H, Shantsila E. The role of monocytes in atherosclerotic coronary artery disease. Ann Med 42: 394-403, 2010.
37. Park YM, Febbraio M, Silverstein RL. CD36 modulates migration of mouse and human macrophages in response to oxidized LDL and may contribute to macrophage trapping in the arterial intima. J Clin Invest 119: 136-145, 2009.
38. Podrez EA, Byzova TV, Febbraio M, Salomon RG, Ma Y, Valiyaveettil M, Poliakov E, Sun M, Finton PJ, Curtis BR, Chen J, Zhang R, Silverstein RL, Hazen SL. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med 13: 1086-1095, 2007.
39. Podrez EA, Febbraio M, Sheibani N, Schmitt D, Silverstein RL, Hajjar DP, Cohen PA, Frazier WA, Hoff HF, Hazen SL. Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J Clin Invest 105: 1095-1108, 2000.
40. Rahaman SO, Lennon DJ, Febbraio M, Podrez EA, Hazen SL, Silverstein RL. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab 4: 211-221, 2006.
41. Rahaman SO, Zhou G, Silverstein RL. Vav protein guanine nucleotide exchange factor regulates CD36 protein-mediated macrophage foam cell formation via calcium and dynamin-dependent processes. J Biol Chem 286: 36011-36019, 2011.
42. Robinet P, Wang Z, Hazen SL, Smith JD. A simple and sensitive enzymatic method for cholesterol quantification in macrophages and foam cells. J Lipid Res 51: 3364-3369, 2010.
43. Silverstein RL. Inflammation, atherosclerosis, and arterial thrombosis: role of the scavenger receptor CD36. Cleve Clin J Med 76, Suppl 2: S27-30, 2009.
44. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11: 155-161, 2010.
45. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 117: 195-205, 2007.
46. Swirski FK, Wildgruber M, Ueno T, Figueiredo JL, Panizzi P, Iwamoto Y, Zhang E, Stone JR, Rodriguez E, Chen JW, Pittet MJ, Weissleder R, Nahrendorf M. Myeloperoxidase-rich Ly-6C+ myeloid cells infiltrate allografts and contribute to an imaging signature of organ rejection in mice. J Clin Invest 120: 2627-2634, 2010.
47. Tabas I, Williams KJ, Borâen J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116: 1832-1844, 2007.
48. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117: 185-194, 2007.
49. Thorne RF, Mhaidat NM, Ralston KJ, Burns GF. CD36 is a receptor for oxidized high density lipoprotein: implications for the development of atherosclerosis. FEBS Lett 581: 1227-1232, 2007.
50. Thun MJ, Carter B, Frskanich D, Prentice R, Lopez AD, Hartqe P, Gapstur SM. 50-year trends in smoking-related mortality in the United States. N Engl J Med 368: 351-364, 2013.
51. Tsoyi K, Jang HJ, Kim JW, Chang HK, Lee YS, Pae HO, Kim HJ, Seo HG, Lee JH, Chung HT, Chang KC. Stimulation of alpha7 nicotinic acetylcholine receptor by nicotine attenuates inflammatory response in macrophages and improves survival in experimental model of sepsis through heme oxygenase-1 induction. Antioxid Redox Signal 14: 2057-2070, 2011.
52. Urakawa N, Nagata T, Kudo K, Kimura K, Imamura T. Simultaneous determination of nicotine and cotinine in various human tissues using capillary gas chromatography/mass spectrometry. Int J Legal Med 106: 232-236, 1994.
53. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 17: 1410-1422, 2011.
54. Wilson HM. Macrophages heterogeneity in atherosclerosis-implications for therapy. J Cell Mol Med 14: 2055-2065, 2010.
55. Winkelmann BR, von Holt K, Unverdorben M. Smoking and atherosclerotic cardiovascular disease: Part I: atherosclerotic disease process. Biomarkers Med 3: 411-428, 2009.
56. Woollard KJ, Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat Rev Cardiol 7: 77-86, 2010.
57. Yu H, Shao H, Yan J, Tsoukias NM, Zhou MS. Bone marrow transplantation improves endothelial function in hypertensive Dahl salt-sensitive rats. J Am Soc Hypertens 6: 331-337, 2012.
58. Yvan-Charvet L, Ranalletta M, Wang N, Han S, Terasaka N, Li R, Welch C, Tall AR. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest 117: 3900-3908, 2007.
59. Zhou MS, Schulman IH, Raij L. Vascular inflammation, insulin resistance, and endothelial dysfunction in salt-sensitive hypertension: role of nuclear factor kappa B activation. J Hypertens 28: 527-535, 2010.