Cigarette smoke exposure promotes arterial thrombosis and vessel remodeling after vascular injury in apolipoprotein E-deficient mice

Journal of Vascular Research

Volumn 45, Issue 6, 2008, Pages 480-492

  Schroeter, Marco R ^a   Sawalich, Matthias ^a   Humboldt, Tim ^a   Leifheit, Maren ^a   Meurrens, Kris ^c   Berges, An ^c   Xu, Haiyan ^c   Lebrun, Stefan ^d   Wallerath, Thomas ^b   Konstantinides, Stavros ^a   Schleef, Raymond ^e   Schaefer, Katrin ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Philip Morris Research Laboratories GmbH   (Germany)

^c Philip Morris Research Laboratories   (Belgium)

^d PHILIP MORRIS PRODUCTS S A   (Switzerland)

^e Philip Morris USA   (United States)

Author keywords

ApoE knockout mice; Arterial thrombosis; Neointima formation; Smoking; Smooth muscle cells

Indexed keywords

APOLIPOPROTEIN E; FERRIC CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTERY THROMBOSIS; ARTICLE; BLOOD VESSEL INJURY; CELL PROLIFERATION; CELL VIABILITY; CIGARETTE SMOKING; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTIMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER;

ACTINS; ANIMALS; APOLIPOPROTEINS E; APOPTOSIS; CAROTID ARTERY DISEASES; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FERRIC COMPOUNDS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; SMOKE; SMOKING; THROMBOSIS; TIME FACTORS; VASCULAR PATENCY;

EID: 54249141420     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000127439     Document Type: Article

References (47)

1. Willett WC, Green A, Stampfer MJ, Speizer FE, Colditz GA, Rosner B, Monson RR, Stason W, Hennekens CH: Relative and absolute excess risks of coronary heart disease among women who smoke cigarettes. N Engl J Med 1987;317:1303-1309.
2. Wolf PA, D'Agostino RB, Kannel WB, Bonita R, Belanger AJ: Cigarette smoking as a risk factor for stroke. The Framingham Study. JAMA 1988;259:1025-1029.
3. Ezzati M, Henley S, Thun MJ, Lopez AD: Role of smoking in global and regional cardiovascular mortality. Circulation 2005;112:489-497.
4. Burke AP, Farb A, Malcom GT, Liang YH, Smialek J, Virmani R: Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med 1997;336:1276-1282.
5. Howard G, Wagenknecht LE, Burke GL, Diez-Roux A, Evans GW, McGovern P, Nieto FJ, Tell GS: Cigarette smoking and progression of atherosclerosis: the Atherosclerosis Risk in Communities (ARIC) Study. JAMA 1998;279:119-124.
6. Dagenais GR, Yi Q, Lonn E, Sleight P, Ostergren J, Yusuf S;HOPE Trial Investigators: Impact of cigarette smoking in high-risk patients participating in a clinical trial. A substudy from the Heart Outcomes Prevention Evaluation (HOPE) trial. Eur J Cardiovasc Prev Rehabil 2005;12:75-81.
7. Thun MJ, Day-Lally CA, Calle EE, Flanders WD, Heath CW: Excess mortality among cigarette smokers: changes in a 20-year interval. Am J Public Health 1995;85:1223-1230.
8. Galan KM, Deligonul U, Kern MJ, Chaitman BR, Vandormael MG: Increased frequency of restenosis in patients continuing to smoke cigarettes after percutaneous transluminal coronary angioplasty. Am J Cardiol 1988;61:260-263.
9. Hasdai D, Garratt KN, Grill DE, Lerman A, Holmes DR Jr: Effect of smoking status on the long-term outcome after successful percutaneous coronary revascularization. N Engl J Med 1997;336:755-761.
10. Macdonald RG, Henderson MA, Hirshfeld JW Jr, Goldberg SH, Bass T, Vetrovec G, Cowley M, Taussig A, Whitworth H, Margolis JR, et al: Patient-related variables and restenosis after percutaneous transluminal coronary angioplasty: a report from the M-HEART Group. Am J Cardiol 1990;66:926-931.
11. Anazawa T, Dimayuga PC, Li H, Tani S, Bradfield J, Chyu KY, Kaul S, Shah PK, Cercek B: Effect of exposure to cigarette smoke on carotid artery intimal thickening: the role of inducible NO synthase. Arterioscler Thromb Vasc Biol 2004;24:1652-1658.
12. Davis JA, Brown AT, Chen H, Wang Y, Poirier LA, Eidt JF, Cruz CP, Moursi MM: Cigarette smoke increases intimal hyperplasia and homocysteine in a rat carotid endarterectomy. J Surg Res 2004;121:69-75.
13. Petrik PV, Gelabert HA, Moore WS, Quinones-Baldrich W, Law MM: Cigarette smoking accelerates carotid artery intimal hyperplasia in a dose-dependent manner. Stroke 1995;26:1409-1414.
14. Tani S, Dimayuga PC, Anazawa T, Chyu KY, Li H, Shah PK, Cercek B: Aberrant antibody responses to oxidized LDL and increased intimal thickening in apoE-/- mice exposed to cigarette smoke. Atherosclerosis 2004;175:7-14.
15. Ruengsakulrach P, Sinclair R, Komeda M, Raman J, Gordon I, Buxton B: Comparative histopathology of radial artery versus internal thoracic artery and risk factors for development of intimal hyperplasia and atherosclerosis. Circulation 1999;100(19 Suppl):II139-II144.
16. International Organization for Standardization: Tobacco and tobacco products - Atmosphere for conditioning and testing, 3rd ed (ISO 3402). Geneva, International Organization for Standardization, 1999.
17. International Organization for Standardization: Routine analytical cigarette-smoking machine - Definitions and standard conditions, 3rd ed (ISO 3308). Geneva, International Organization for Standardization, 2000.
18. Vanscheeuwijck PM, Teredesai A, Terpstra PM, Verbeeck J, Kuhl P, Gerstenberg B, Gebel S, Carmines EL: Evaluation of the potential effects of ingredients added to cigarettes. Part 4: subchronic inhalation toxicity. Food Chem Toxicol 2002;40:113-131.
19. Haussmann HJ, Anskeit E, Becker D, Kuhl P, Stinn W, Teredesai A, Voncken P, Walk RA: Comparison of fresh and room-aged cigarette sidestream smoke in a subchronic inhalation study on rats. Toxicol Sci 1998;41:100-116.
20. Rustemeier K, Stabbert R, Haussmann HJ, Roemer E, Carmines EL: Evaluation of the potential effects of ingredients added to cigarettes. Part 2: chemical composition of mainstream smoke. Food Chem Toxicol 2002;40:93-104.
21. Roemer E, Stabbert R, Rustemeier K, Veltel DJ, Meisgen TJ, Reininghaus W, Carchman RA, Gaworski CL, Podraza KF: Chemical composition, cytotoxicity and mutagenicity of smoke from US commercial and reference cigarettes smoked under two sets of machine smoking conditions. Toxicology 2004;195:31-52.
22. Konstantinides S, Schäfer K, Thinnes T, Loskutoff DJ: Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation 2001;103:576-583.
23. Schäfer K, Konstantinides S, Riedel C, Thinnes T, Müller K, Dellas C, Hasenfuss G, Loskutoff DJ: Different mechanisms of increased luminal stenosis after arterial injury in mice deficient for urokinase- or tissue-type plasminogen activator. Circulation 2002;106:1847-1852.
24. Schäfer K, Schroeter MR, Dellas C, Puls M, Nitsche M, Weiss E, Hasenfuss G, Konstantinides SV: Plasminogen activator inhibitor-1 from bone marrow-derived cells suppresses neointimal formation after vascular injury in mice. Arterioscler Thromb Vasc Biol 2006;26:1254-1259.
25. Raupach T, Schäfer K, Konstantinides S, Andreas S: Secondhand smoke as an acute threat for the cardiovascular system: a change in paradigm. Eur Heart J 2006;27:386-392.
26. Gairola CG, Drawdy ML, Block AE, Daugherty A: Sidestream cigarette smoke accelerates atherogenesis in apolipoprotein E-/-mice. Atherosclerosis 2001;156:49-55.
27. 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 2001;7:833-839.
28. 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 2006;26:143-149.
29. Yamaguchi Y, Matsuno S, Kagota S, Haginaka J, Kunitomo M: Oxidants in cigarette smoke extract modify low-density lipoprotein in the plasma and facilitate atherogenesis in the aorta of Watanabe heritable hyperlipidemic rabbits. Atherosclerosis 2001;156:109-117.
30. Gurlek A, Dagalp Z, Oral D, Omurlu K, Erol C, Akyol T, Tutar E: Restenosis after transluminal coronary angioplasty: a risk factor analysis. J Cardiovasc Risk 1995;2:51-55.
31. Kotamaki M, Laustiola K, Syvanne M, Heikkila J: Influence of continued smoking and some biological risk factors on restenosis after percutaneous transluminal coronary angioplasty. J Intern Med 1996;240:293-301.
32. Cohen DJ, Doucet M, Cutlip DE, Ho KK, Popma JJ, Kuntz RE: Impact of smoking on clinical and angiographic restenosis after percutaneous coronary intervention: another smoker's paradox? Circulation 2001;104:773-778.
33. Violaris AG, Thury A, Regar E, Melkert R, Serruys PW: Influence of a history of smoking on short term (six month) clinical and angiographic outcome after successful coronary angioplasty. Heart 2000;84:299-306.
34. Cutlip DE, Chauhan MS, Baim DS, Ho KK, Popma JJ, Carrozza JP, Cohen DJ, Kuntz RE: Clinical restenosis after coronary stenting: perspectives from multicenter clinical trials. J Am Coll Cardiol 2002;40:2082-2089.
35. Schillinger M, Exner M, Mlekusch W, Haumer M, Sabeti S, Ahmadi R, Wagner O, Minar E: Effect of smoking on restenosis during the 1st year after lower-limb endovascular interventions. Radiology 2004;231:831-838.
36. Carty CS, Soloway PD, Kayastha S, Bauer J, Marsan B, Ricotta JJ, Dryjski M: Nicotine and cotinine stimulate secretion of basic fibroblast growth factor and affect expression of matrix metalloproteinases in cultured human smooth muscle cells. J Vasc Surg 1996;24:927-934.
37. Cucina A, Sapienza P, Corvino V, Borrelli V, Mariani V, Randone B, Santoro DL, Cavallaro A: Nicotine-induced smooth muscle cell proliferation is mediated through bFGF and TGF-beta 1. Surgery 2000;127:316-322.
38. Villablanca AC: Nicotine stimulates DNA synthesis and proliferation in vascular endothelial cells in vitro. J Appl Physiol 1998;84:2089-2098.
39. Mundal HH, Hjemdahl P, Gjesdal K: Acute effects of cigarette smoking on platelet function and plasma catecholamines in hypertensive and normotensive men. Am J Hypertens 1998;11:677-681.
40. Rubenstein D, Jesty J, Bluestein, D: Differences between mainstream and sidestream cigarette smoke extracts and nicotine in the activation of platelets under static and flow conditions. Circulation 2004;109:78-83.
41. Fusegawa Y, Goto S, Handa S, Kawada T, Ando Y: Platelet spontaneous aggregation in platelet-rich plasma is increased in habitual smokers. Thromb Res 1999;93:271-278.
42. Hung J, Lam JY, Lacoste L, Letchacovski, G: Cigarette smoking acutely increases platelet thrombus formation in patients with coronary artery disease taking aspirin. Circulation 1995;92:2432-2436.
43. Meade TW, Imeson J, Stirling Y: Effects of changes in smoking and other characteristics on clotting factors and the risk of ischaemic heart disease. Lancet 1987;2:986-988.
44. Miller GJ, Bauer KA, Cooper JA, Rosenberg RD: Activation of the coagulant pathway in cigarette smokers. Thromb Haemost 1998;79:549-553.
45. Matetzky S, Tani S, Kangavari S, Dimayuga P, Yano J, Xu H, Chyu KY, Fishbein MC, Shah PK, Cercek B: Smoking increases tissue factor expression in atherosclerotic plaques: implications for plaque thrombogenicity. Circulation 2000;102:602-604.
46. Simpson AJ, Gray RS, Moore NR, Booth NA: The effects of chronic smoking on the fibrinolytic potential of plasma and platelets. Br J Haematol 1997;97:208-213.
47. Geng YJ, Libby P: Progression of atheroma: a struggle between death and procreation. Arterioscler Thromb Vasc Biol 2002;22:1370-1380.