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Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 3759186, 16 pages
https://doi.org/10.1155/2017/3759186
Review Article

Functional, Cellular, and Molecular Remodeling of the Heart under Influence of Oxidative Cigarette Tobacco Smoke

1Department of Pharmacology and Toxicology, American University of Beirut Faculty of Medicine, Beirut, Lebanon
2Department of Pharmacology and Toxicology, University of Mississippi Medical Center School of Medicine, Jackson, MS, USA
3Department of Biochemistry and Molecular Genetics, American University of Beirut Faculty of Medicine, Beirut, Lebanon

Correspondence should be addressed to Firas Kobeissy and Fouad A. Zouein

Received 30 March 2017; Accepted 1 June 2017; Published 20 July 2017

Academic Editor: Victor M. Victor

Copyright © 2017 Abdullah Kaplan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General, Atlanta, GA, 2014.
  2. Centers for Disease, C, “The surgeon general’s 1989 report on reducing the health consequences of smoking: 25 years of progress,” MMWR Supplements, vol. 38, no. 2, pp. 1–32, 1989. View at Google Scholar
  3. B. P. Rafacho, P. S. Azevedo, B. F. Polegato et al., “Tobacco smoke induces ventricular remodeling associated with an increase in NADPH oxidase activity,” Cellular Physiology and Biochemistry, vol. 27, no. 3-4, pp. 305–312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Yao, I. Edirisinghe, S. R. Yang et al., “Genetic ablation of NADPH oxidase enhances susceptibility to cigarette smoke-induced lung inflammation and emphysema in mice,” The American Journal of Pathology, vol. 172, no. 5, pp. 1222–1237, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. A. Ambrose and R. S. Barua, “The pathophysiology of cigarette smoking and cardiovascular disease: an update,” Journal of the American College of Cardiology, vol. 43, no. 10, pp. 1731–1737, 2004. View at Google Scholar
  6. S. S. Barbieri, E. Zacchi, P. Amadio et al., “Cytokines present in smokers’ serum interact with smoke components to enhance endothelial dysfunction,” Cardiovascular Research, vol. 90, no. 3, pp. 475–483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Bernhard and X. L. Wang, “Smoking, oxidative stress and cardiovascular diseases—do anti-oxidative therapies fail?” Current Medicinal Chemistry, vol. 14, no. 16, pp. 1703–1712, 2007. View at Google Scholar
  8. A. Csordas, G. Wick, G. Laufer, and D. Bernhard, “An evaluation of the clinical evidence on the role of inflammation and oxidative stress in smoking-mediated cardiovascular disease,” Biomarker Insights, vol. 3, pp. 127–139, 2008. View at Google Scholar
  9. A. Das, N. Dey, A. Ghosh, S. Das, D. J. Chattopadhyay, and I. B. Chatterjee, “Molecular and cellular mechanisms of cigarette smoke-induced myocardial injury: prevention by vitamin C,” PloS One, vol. 7, no. 9, article e44151, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Gvozdjak, A. Gvozdjáková, J. Kucharská, and V. Bada, “The effect of smoking on myocardial metabolism,” Czechoslovak Medicine, vol. 10, no. 1, pp. 47–53, 1987. View at Google Scholar
  11. A. Gvozdjakova, V. Bada, L. Sány et al., “Smoke cardiomyopathy: disturbance of oxidative processes in myocardial mitochondria,” Cardiovascular Research, vol. 18, no. 4, pp. 229–232, 1984. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Alam, J. Wardell, E. Andersson, C. Höglund, and R. Nordlander, “Acute effects of smoking on diastolic function in healthy participants: studies by conventional doppler echocardiography and doppler tissue imaging,” Journal of the American Society of Echocardiography, vol. 15, no. 10, Part 2, pp. 1232–1237, 2002. View at Google Scholar
  13. I. Barutcu, A. M. Esen, D. Kaya et al., “Effect of acute cigarette smoking on left and right ventricle filling parameters: a conventional and tissue Doppler echocardiographic study in healthy participants,” Angiology, vol. 59, no. 3, pp. 312–316, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. O. Ciftci, M. Calişkan, H. Güllü, A. Yildirir, and H. Müderrisoğlu, “Mentholated cigarette smoking induced alterations in left and right ventricular functions in chronic smokers,” Anadolu Kardiyoloji Dergisi, vol. 8, no. 2, pp. 116–122, 2008. View at Google Scholar
  15. E. Giacomin, E. Palmerini, P. Ballo, V. Zacà, G. Bova, and S. Mondillo, “Acute effects of caffeine and cigarette smoking on ventricular long-axis function in healthy subjects,” Cardiovascular Ultrasound, vol. 6, p. 9, 2008. View at Google Scholar
  16. O. Gulel, K. Soylu, M. Yazici, S. Demircan, K. Durna, and M. Sahin, “Longitudinal diastolic myocardial functions are affected by chronic smoking in young healthy people: a study of color tissue Doppler imaging,” Echocardiography, vol. 24, no. 5, pp. 494–498, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. T. F. Ilgenli and O. Akpinar, “Acute effects of smoking on right ventricular function. A tissue Doppler imaging study on healthy subjects,” Swiss Medical Weekly, vol. 137, no. 5-6, pp. 91–96, 2007. View at Publisher · View at Google Scholar
  18. O. Karakaya, I. Barutcu, A. M. Esen et al., “Acute smoking-induced alterations in Doppler echocardiographic measurements in chronic smokers,” Texas Heart Institute Journal, vol. 33, no. 2, pp. 134–138, 2006. View at Google Scholar
  19. A. Leone, “Biochemical markers of cardiovascular damage from tobacco smoke,” Current Pharmaceutical Design, vol. 11, no. 17, pp. 2199–2208, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Narkiewicz, P. J. van de Borne, M. Hausberg et al., “Cigarette smoking increases sympathetic outflow in humans,” Circulation, vol. 98, no. 6, pp. 528–534, 1998. View at Publisher · View at Google Scholar
  21. H. M. Mertens, H. Mannebach, and U. Gleichmann, “Non-invasive effects of cigarette smoking on left ventricular function at rest and with exercise in normal individuals (author’s transl),” Zeitschrift für Kardiologie, vol. 68, no. 6, pp. 374–381, 1979. View at Google Scholar
  22. M. A. Talukder, W. M. Johnson, S. Varadharaj et al., “Chronic cigarette smoking causes hypertension, increased oxidative stress, impaired NO bioavailability, endothelial dysfunction, and cardiac remodeling in mice,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 300, no. 1, pp. H388–H396, 2011. View at Google Scholar
  23. L. Gu, V. Pandey, D. L. Geenen, S. A. Chowdhury, and M. R. Piano, “Cigarette smoke-induced left ventricular remodelling is associated with activation of mitogen-activated protein kinases,” European Journal of Heart Failure, vol. 10, no. 11, pp. 1057–1064, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. P. P. Santos, F. Oliveira, V. C. Ferreira et al., “The role of lipotoxicity in smoke cardiomyopathy,” PloS One, vol. 9, no. 12, article e113739, 2014. View at Google Scholar
  25. D. R. Duarte, M. F. Minicucci, P. S. Azevedo et al., “The role of oxidative stress and lipid peroxidation in ventricular remodeling induced by tobacco smoke exposure after myocardial infarction,” Clinics (São Paulo, Brazil), vol. 64, no. 7, pp. 691–7, 2009. View at Google Scholar
  26. A. Gvozdjakova, F. Simko, J. Kucharská, Z. Braunová, P. Psenek, and J. Kyselovic, “Captopril increased mitochondrial coenzyme Q10 level, improved respiratory chain function and energy production in the left ventricle in rabbits with smoke mitochondrial cardiomyopathy,” BioFactors, vol. 10, no. 1, pp. 61–65, 1999. View at Publisher · View at Google Scholar
  27. R. Novo, C. M. Freire, S. Felisbino et al., “Smoking is associated with remodeling of gap junction in the rat heart: smoker’s paradox explanation?” Arquivos Brasileiros de Cardiologia, vol. 100, no. 3, pp. 274–280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. D. R. Duarte, M. F. Minicucci, P. S. Azevedo et al., “Influence of lisinopril on cardiac remodeling induced by tobacco smoke exposure,” Medical Science Monitor, vol. 16, no. 8, pp. BR255–BR259, 2010. View at Google Scholar
  29. J. M. Bradley, J. B. Nguyen, A. C. Fournett, and J. D. Gardner, “Cigarette smoke exacerbates ventricular remodeling and dysfunction in the volume overloaded heart,” Microscopy and Microanalysis, vol. 18, no. 1, pp. 91–98, 2012. View at Google Scholar
  30. X. Zhou, G. An, and J. Chen, “Hydrogen sulfide improves left ventricular function in smoking rats via regulation of apoptosis and autophagy,” Apoptosis, vol. 19, no. 6, pp. 998–1005, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. W. H. Herbert, “Cigarette smoking and arteriographically demonstrable coronary artery disease,” Chest, vol. 67, no. 1, pp. 49–52, 1975. View at Publisher · View at Google Scholar
  32. D. R. Ramsdale, E. B. Faragher, C. L. Bray, D. H. Bennett, C. Ward, and D. C. Beton, “Smoking and coronary artery disease assessed by routine coronary arteriography,” British Medical Journal (Clinical Research Ed.), vol. 290, no. 6463, pp. 197–200, 1985. View at Google Scholar
  33. X. L. Wang, C. Tam, R. M. McCredie, and D. E. Wilcken, “Determinants of severity of coronary artery disease in Australian men and women,” Circulation, vol. 89, no. 5, pp. 1974–1981, 1994. View at Publisher · View at Google Scholar
  34. D. Waters, J. Lespérance, P. Gladstone et al., “Effects of cigarette smoking on the angiographic evolution of coronary atherosclerosis. A Canadian Coronary Atherosclerosis Intervention Trial (CCAIT) Substudy. CCAIT Study Group,” Circulation, vol. 94, no. 4, pp. 614–621, 1996. View at Publisher · View at Google Scholar
  35. R. S. Barua, J. A. Ambrose, L. J. Eales-Reynolds, M. C. DeVoe, J. G. Zervas, and D. C. Saha, “Dysfunctional endothelial nitric oxide biosynthesis in healthy smokers with impaired endothelium-dependent vasodilatation,” Circulation, vol. 104, no. 16, pp. 1905–1910, 2001. View at Publisher · View at Google Scholar
  36. R. S. Barua, J. A. Ambrose, S. Srivastava, M. C. DeVoe, and L. J. Eales-Reynolds, “Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase: an in vitro demonstration in human coronary artery endothelial cells,” Circulation, vol. 107, no. 18, pp. 2342–2347, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. D. S. Celermajer, M. R. Adams, P. Clarkson et al., “Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults,” The New England Journal of Medicine, vol. 334, no. 3, pp. 150–154, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. D. S. Celermajer, K. E. Sorensen, D. Georgakopoulos et al., “Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults,” Circulation, vol. 88, no. 5, Part 1, pp. 2149–2155, 1993. View at Google Scholar
  39. R. G. Ijzerman, E. H. Serne, M. M. van Weissenbruch, R. T. de Jongh, and C. D. Stehouwer, “Cigarette smoking is associated with an acute impairment of microvascular function in humans,” Clinical Science (London, England), vol. 104, no. 3, pp. 247–252, 2003. View at Publisher · View at Google Scholar
  40. W. G. Mayhan and G. M. Sharpe, “Effect of cigarette smoke extract on arteriolar dilatation in vivo,” Journal of Applied Physiology (1985), vol. 81, no. 5, pp. 1996–2003, 1996. View at Google Scholar
  41. Y. Ota, K. Kugiyama, S. Sugiyama et al., “Impairment of endothelium-dependent relaxation of rabbit aortas by cigarette smoke extract—role of free radicals and attenuation by captopril,” Atherosclerosis, vol. 131, no. 2, pp. 195–202, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Sumida, H. Watanabe, K. Kugiyama, M. Ohgushi, T. Matsumura, and H. Yasue, “Does passive smoking impair endothelium-dependent coronary artery dilation in women?” Journal of the American College of Cardiology, vol. 31, no. 4, pp. 811–815, 1998. View at Google Scholar
  43. W. Y. Craig, G. E. Palomaki, and J. E. Haddow, “Cigarette smoking and serum lipid and lipoprotein concentrations: an analysis of published data,” BMJ, vol. 298, no. 6676, pp. 784–788, 1989. View at Publisher · View at Google Scholar
  44. B. Frei, T. M. Forte, B. N. Ames, and C. E. Cross, “Gas phase oxidants of cigarette smoke induce lipid peroxidation and changes in lipoprotein properties in human blood plasma. Protective effects of ascorbic acid,” The Biochemical Journal, vol. 277, Part 1, pp. 133–138, 1991. View at Google Scholar
  45. T. Heitzer, S. Ylä-Herttuala, J. Luoma et al., “Cigarette smoking potentiates endothelial dysfunction of forearm resistance vessels in patients with hypercholesterolemia. Role of oxidized LDL,” Circulation, vol. 93, no. 7, pp. 1346–1353, 1996. View at Publisher · View at Google Scholar
  46. Y. Yamaguchi, S. Kagota, J. Haginaka, and M. Kunitomo, “Evidence of modified LDL in the plasma of hypercholesterolemic WHHL rabbits injected with aqueous extracts of cigarette smoke,” Environmental Toxicology and Pharmacology, vol. 8, no. 4, pp. 255–260, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. E. A. Bermudez, N. Rifai, J. E. Buring, J. E. Manson, and P. M. Ridker, “Relation between markers of systemic vascular inflammation and smoking in women,” The American Journal of Cardiology, vol. 89, no. 9, pp. 1117–9, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. C. J. Smith and T. H. Fischer, “Particulate and vapor phase constituents of cigarette mainstream smoke and risk of myocardial infarction,” Atherosclerosis, vol. 158, no. 2, pp. 257–267, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. P. S. Tappia, K. L. Troughton, S. C. Langley-Evans, and R. F. Grimble, “Cigarette smoking influences cytokine production and antioxidant defences,” Clinical Science (London, England), vol. 88, no. 4, pp. 485–489, 1995. View at Publisher · View at Google Scholar
  50. R. P. Tracy, B. M. Psaty, E. Macy et al., “Lifetime smoking exposure affects the association of C-reactive protein with cardiovascular disease risk factors and subclinical disease in healthy elderly subjects,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 10, pp. 2167–2176, 1997. View at Publisher · View at Google Scholar
  51. D. Blache, “Involvement of hydrogen and lipid peroxides in acute tobacco smoking-induced platelet hyperactivity,” The American Journal of Physiology, vol. 268, no. 2, Part 2, pp. H679–H685, 1995. View at Google Scholar
  52. Y. Fusegawa, S. Goto, S. Handa, T. Kawada, and Y. Ando, “Platelet spontaneous aggregation in platelet-rich plasma is increased in habitual smokers,” Thrombosis Research, vol. 93, no. 6, pp. 271–278, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Rival, J. M. Riddle, and P. D. Stein, “Effects of chronic smoking on platelet function,” Thrombosis Research, vol. 45, no. 1, pp. 75–85, 1987. View at Publisher · View at Google Scholar · View at Scopus
  54. R. S. Barua, J. A. Ambrose, D. C. Saha, and L. J. Eales-Reynolds, “Smoking is associated with altered endothelial-derived fibrinolytic and antithrombotic factors: an in vitro demonstration,” Circulation, vol. 106, no. 8, pp. 905–8, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Matetzky, S. Tani, S. Kangavari et al., “Smoking increases tissue factor expression in atherosclerotic plaques: implications for plaque thrombogenicity,” Circulation, vol. 102, no. 6, pp. 602–604, 2000. View at Publisher · View at Google Scholar
  56. D. E. Newby, R. A. Wright, C. Labinjoh et al., “Endothelial dysfunction, impaired endogenous fibrinolysis, and cigarette smoking: a mechanism for arterial thrombosis and myocardial infarction,” Circulation, vol. 99, no. 11, pp. 1411–1415, 1999. View at Publisher · View at Google Scholar
  57. M. Pretorius, D. A. Rosenbaum, J. Lefebvre, D. E. Vaughan, and N. J. Brown, “Smoking impairs bradykinin-stimulated t-PA release,” Hypertension, vol. 39, no. 3, pp. 767–771, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. T. P. Devasagayam, J. C. Tilak, K. K. Boloor, K. S. Sane, S. S. Ghaskadbi, and R. D. Lele, “Free radicals and antioxidants in human health: current status and future prospects,” The Journal of the Association of Physicians of India, vol. 52, pp. 794–804, 2004. View at Google Scholar
  59. K. M. Holmstrom and T. Finkel, “Cellular mechanisms and physiological consequences of redox-dependent signalling,” Nature Reviews. Molecular Cell Biology, vol. 15, no. 6, pp. 411–421, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. X. Zhou, C. Li, W. Xu, and J. Chen, “Trimetazidine protects against smoking-induced left ventricular remodeling via attenuating oxidative stress, apoptosis, and inflammation,” PloS One, vol. 7, no. 7, article e40424, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. B. Bozkurt, S. B. Kribbs, F. J. Clubb Jr. et al., “Pathophysiologically relevant concentrations of tumor necrosis factor-alpha promote progressive left ventricular dysfunction and remodeling in rats,” Circulation, vol. 97, no. 14, pp. 1382–1391, 1998. View at Publisher · View at Google Scholar
  62. M. Bujak, M. Dobaczewski, K. Chatila et al., “Interleukin-1 receptor type I signaling critically regulates infarct healing and cardiac remodeling,” The American Journal of Pathology, vol. 173, no. 1, pp. 57–67, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Hasper, M. Hummel, F. X. Kleber, I. Reindl, and H. D. Volk, “Systemic inflammation in patients with heart failure,” European Heart Journal, vol. 19, no. 5, pp. 761–5, 1998. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Matsumoto, T. Tsujino, M. Lee-Kawabata et al., “Serum interleukin-6 and C-reactive protein are markedly elevated in acute decompensated heart failure patients with left ventricular systolic dysfunction,” Cytokine, vol. 49, no. 3, pp. 264–268, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Ono, A. Matsumori, T. Shioi, Y. Furukawa, and S. Sasayama, “Cytokine gene expression after myocardial infarction in rat hearts: possible implication in left ventricular remodeling,” Circulation, vol. 98, no. 2, pp. 149–156, 1998. View at Publisher · View at Google Scholar
  66. G. Torre-Amione, S. Kapadia, C. Benedict, H. Oral, J. B. Young, and D. L. Mann, “Proinflammatory cytokine levels in patients with depressed left ventricular ejection fraction: a report from the studies of left ventricular dysfunction (SOLVD),” Journal of the American College of Cardiology, vol. 27, no. 5, pp. 1201–1206, 1996. View at Google Scholar
  67. M. F. Huang, W. L. Lin, and Y. C. Ma, “A study of reactive oxygen species in mainstream of cigarette,” Indoor Air, vol. 15, no. 2, pp. 135–140, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. A. L. Bluhm, J. Weinstein, and J. A. Sousa, “Free radicals in tobacco smoke,” Nature, vol. 229, no. 5285, p. 500, 1971. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Witschi, “Carcinogenic activity of cigarette smoke gas phase and its modulation by beta-carotene and N-acetylcysteine,” Toxicological Sciences, vol. 84, no. 1, pp. 81–87, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. K. F. Chung, “Inflammatory mediators in chronic obstructive pulmonary disease,” Current Drug Targets. Inflammation and Allergy, vol. 4, no. 6, pp. 619–625, 2005. View at Google Scholar
  71. A. Churg, J. Dai, H. Tai, C. Xie, and J. L. Wright, “Tumor necrosis factor-alpha is central to acute cigarette smoke-induced inflammation and connective tissue breakdown,” American Journal of Respiratory and Critical Care Medicine, vol. 166, no. 6, pp. 849–854, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. B. T. Mossman, K. M. Lounsbury, and S. P. Reddy, “Oxidants and signaling by mitogen-activated protein kinases in lung epithelium,” American Journal of Respiratory Cell and Molecular Biology, vol. 34, no. 6, pp. 666–669, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. M. J. Walters, M. J. Paul-Clark, M. M. SK, K. Ito, I. M. Adcock, and J. A. Mitchell, “Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance,” Molecular Pharmacology, vol. 68, no. 5, pp. 1343–1353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. S. V. Culpitt, D. F. Rogers, P. Shah et al., “Impaired inhibition by dexamethasone of cytokine release by alveolar macrophages from patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 167, no. 1, pp. 24–31, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Altara, M. Manca, R. Sabra, A. A. Eid, G. W. Booz, and F. A. Zouein, “Temporal cardiac remodeling post-myocardial infarction: dynamics and prognostic implications in personalized medicine,” Heart Failure Reviews, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. X. Zhou, C. Li, W. Xu, and J. Chen, “Protective effects of valsartan against cigarette smoke-induced left ventricular systolic dysfunction in rats,” International Journal of Cardiology, vol. 167, no. 3, pp. 677–680, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Arnson, Y. Shoenfeld, and H. Amital, “Effects of tobacco smoke on immunity, inflammation and autoimmunity,” Journal of Autoimmunity, vol. 34, no. 3, pp. J258–J265, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. A. K. Khanna, J. Xu, and M. R. Mehra, “Antioxidant N-acetyl cysteine reverses cigarette smoke-induced myocardial infarction by inhibiting inflammation and oxidative stress in a rat model,” Laboratory Investigation, vol. 92, no. 2, pp. 224–235, 2012. View at Google Scholar
  79. P. P. dos Santos, B. F. Nogueira, B. P. Rafacho et al., “Aldosterone is not involved in the ventricular remodeling process induced by tobacco smoke exposure,” Cellular Physiology and Biochemistry, vol. 30, no. 5, pp. 1191–1201, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. R. J. Mailloux, S. L. McBride, and M. E. Harper, “Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics,” Trends in Biochemical Sciences, vol. 38, no. 12, pp. 592–602, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. I. Rahman and W. MacNee, “Antioxidant pharmacological therapies for COPD,” Current Opinion in Pharmacology, vol. 12, no. 3, pp. 256–265, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. B. Aravamudan, M. A. Thompson, C. M. Pabelick, and Y. S. Prakash, “Mitochondria in lung diseases,” Expert Review of Respiratory Medicine, vol. 7, no. 6, pp. 631–646, 2013. View at Google Scholar
  83. S. W. Ballinger, C. Patterson, C. N. Yan et al., “Hydrogen peroxide- and peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells,” Circulation Research, vol. 86, no. 9, pp. 960–966, 2000. View at Publisher · View at Google Scholar
  84. C. A. Knight-Lozano, C. G. Young, D. L. Burow et al., “Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues,” Circulation, vol. 105, no. 7, pp. 849–854, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Lough, “Cardiomyopathy produced by cigarette smoke. Ultrastructural observations in guinea pigs,” Archives of Pathology & Laboratory Medicine, vol. 102, no. 7, pp. 377–380, 1978. View at Google Scholar
  86. H. K. Thomsen and K. Kjeldsen, “Threshold limit for carbon monoxide-induced myocardial damage: an electron microscopic study in rabbits,” Archives of Environmental Health, vol. 29, no. 2, pp. 73–78, 1974. View at Google Scholar
  87. T. S. Tippetts, D. R. Winden, A. C. Swensen et al., “Cigarette smoke increases cardiomyocyte ceramide accumulation and inhibits mitochondrial respiration,” BMC Cardiovascular Disorders, vol. 14, p. 165, 2014. View at Google Scholar
  88. A. P. Wong, A. Niedzwiecki, and M. Rath, “Myocardial energetics and the role of micronutrients in heart failure: a critical review,” American Journal of Cardiovascular Disease, vol. 6, no. 3, pp. 81–92, 2016. View at Google Scholar
  89. S. Yamada, X. Q. Zhang, T. Kadono et al., “Direct toxic effects of aqueous extract of cigarette smoke on cardiac myocytes at clinically relevant concentrations,” Toxicology and Applied Pharmacology, vol. 236, no. 1, pp. 71–77, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Minicucci, F. Oliveira, P. Santos et al., “Pentoxifylline attenuates cardiac remodeling induced by tobacco smoke exposure,” Arquivos Brasileiros de Cardiologia, vol. 106, no. 5, pp. 396–403, 2016. View at Publisher · View at Google Scholar · View at Scopus
  91. G. Pearson, F. Robinson, T. Beers Gibson et al., “Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions,” Endocrine Reviews, vol. 22, no. 2, pp. 153–183, 2001. View at Publisher · View at Google Scholar
  92. J. R. Testa and P. N. Tsichlis, “AKT signaling in normal and malignant cells,” Oncogene, vol. 24, no. 50, pp. 7391–7393, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. X. Zhou, C. Li, and X. Lu, “The pathogenic role of autophagy in smoking-induced left ventricular systolic dysfunction in rats,” International Journal of Cardiology, vol. 168, no. 4, pp. 4302-4303, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. J. W. Stephens and S. E. Humphries, “The molecular genetics of cardiovascular disease: clinical implications,” Journal of Internal Medicine, vol. 253, no. 2, pp. 120–127, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. P. J. Talmud, J. W. Stephens, E. Hawe et al., “The significant increase in cardiovascular disease risk in APOEepsilon4 carriers is evident only in men who smoke: potential relationship between reduced antioxidant status and ApoE4,” Annals of Human Genetics, vol. 69, Part 6, pp. 613–622, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Chen, P. T. Dawes, J. C. Packham, and D. L. Mattey, “Interaction between smoking and functional polymorphism in the TGFB1 gene is associated with ischaemic heart disease and myocardial infarction in patients with rheumatoid arthritis: a cross-sectional study,” Arthritis Research & Therapy, vol. 14, no. 2, p. R81, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. P. de Moerloose and F. Boehlen, “Inherited thrombophilia in arterial disease: a selective review,” Seminars in Hematology, vol. 44, no. 2, pp. 106–113, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. M. L. Grisoni, C. Proust, M. Alanne et al., “Haplotypic analysis of tag SNPs of the interleukin-18 gene in relation to cardiovascular disease events: the MORGAM project,” European Journal of Human Genetics, vol. 16, no. 12, pp. 1512–1520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. L. P. Breitling, R. Yang, B. Korn, B. Burwinkel, and H. Brenner, “Tobacco-smoking-related differential DNA methylation: 27K discovery and replication,” American Journal of Human Genetics, vol. 88, no. 4, pp. 450–457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. E. S. Wan, W. Qiu, A. Baccarelli et al., “Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome,” Human Molecular Genetics, vol. 21, no. 13, pp. 3073–3082, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. L. P. Breitling, K. Salzmann, D. Rothenbacher, B. Burwinkel, and H. Brenner, “Smoking, F2RL3 methylation, and prognosis in stable coronary heart disease,” European Heart Journal, vol. 33, no. 22, pp. 2841–2848, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. J. J. McDougall, C. Zhang, L. Cellars, E. Joubert, C. M. Dixon, and N. Vergnolle, “Triggering of proteinase-activated receptor 4 leads to joint pain and inflammation in mice,” Arthritis and Rheumatism, vol. 60, no. 3, pp. 728–737, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. J. D. Muehlschlegel, T. E. Perry, K. Y. Liu et al., “Polymorphism in the protease-activated receptor-4 gene region associates with platelet activation and perioperative myocardial injury,” American Journal of Hematology, vol. 87, no. 2, pp. 161–166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. C. C. Wu, S. Y. Wu, C. Y. Liao, C. M. Teng, Y. C. Wu, and S. C. Kuo, “The roles and mechanisms of PAR4 and P2Y12/phosphatidylinositol 3-kinase pathway in maintaining thrombin-induced platelet aggregation,” British Journal of Pharmacology, vol. 161, no. 3, pp. 643–658, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. E. L. Marczylo, A. A. Amoako, J. C. Konje, T. W. Gant, and T. H. Marczylo, “Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern?” Epigenetics, vol. 7, no. 5, pp. 432–439, 2012. View at Google Scholar
  106. M. J. Maenner, L. C. Denlinger, A. Langton, K. J. Meyers, C. D. Engelman, and H. G. Skinner, “Detecting gene-by-smoking interactions in a genome-wide association study of early-onset coronary heart disease using random forests,” BMC Proceedings, vol. 3, Supplement 7, p. S88, 2009. View at Google Scholar
  107. S. F. Ali, E. E. Smith, D. L. Bhatt, G. C. Fonarow, and L. H. Schwamm, “Paradoxical association of smoking with in-hospital mortality among patients admitted with acute ischemic stroke,” Journal of the American Heart Association, vol. 2, no. 3, article e000171, 2013. View at Google Scholar
  108. G. I. Barbash, J. Reiner, H. D. White et al., “Evaluation of paradoxic beneficial effects of smoking in patients receiving thrombolytic therapy for acute myocardial infarction: mechanism of the “smoker’s paradox” from the GUSTO-I trial, with angiographic insights. Global Utilization of Streptokinase and Tissue-Plasminogen Activator for Occluded Coronary Arteries,” Journal of the American College of Cardiology, vol. 26, no. 5, pp. 1222–1229, 1995. View at Google Scholar
  109. A. H. Kitchin and S. J. Pocock, “Prognosis of patients with acute myocardial infarction admitted to a coronary care unit. I: survival in hospital,” British Heart Journal, vol. 39, no. 11, pp. 1163–1166, 1977. View at Publisher · View at Google Scholar · View at Scopus
  110. J. S. Pollock, R. D. Hollenbeck, L. Wang, D. R. Janz, T. W. Rice, and J. A. McPherson, “A history of smoking is associated with improved survival in patients treated with mild therapeutic hypothermia following cardiac arrest,” Resuscitation, vol. 85, no. 1, pp. 99–103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Gupta, D. Kolte, S. Khera et al., “Smoker’s paradox in patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention,” Journal of the American Heart Association, vol. 5, no. 4, 2016. View at Publisher · View at Google Scholar · View at Scopus
  112. S. A. Paiva, R. Novo, B. B. Matsubara et al., “Beta-carotene attenuates the paradoxical effect of tobacco smoke on the mortality of rats after experimental myocardial infarction,” The Journal of Nutrition, vol. 135, no. 9, pp. 2109–2113, 2005. View at Google Scholar
  113. Y. J. Zhang, J. Iqbal, D. van Klaveren et al., “Smoking is associated with adverse clinical outcomes in patients undergoing revascularization with PCI or CABG: the SYNTAX trial at 5-year follow-up,” Journal of the American College of Cardiology, vol. 65, no. 11, pp. 1107–1115, 2015. View at Google Scholar
  114. B. Acar, O. Ozeke, S. Unal et al., “Change in left ventricular systolic function in patients with ST elevation myocardial infarction: evidence for smoker’s paradox or pseudo-paradox?” Indian Heart Journal, vol. 68, no. 6, pp. 816–820, 2016. View at Publisher · View at Google Scholar · View at Scopus
  115. G. Gennaro, S. J. Brener, B. Redfors et al., “Effect of smoking on infarct size and major adverse cardiac events in patients with large anterior ST-elevation myocardial infarction (from the INFUSE-AMI trial),” The American Journal of Cardiology, vol. 118, no. 8, pp. 1097–1104, 2016. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Saad, G. Fuernau, S. Desch et al., ““Smoker’s paradox” in patients with cardiogenic shock complicating myocardial infarction - a substudy of the IABP-SHOCK II-trial and registry,” International Journal of Cardiology, vol. 222, pp. 775–779, 2016. View at Publisher · View at Google Scholar · View at Scopus
  117. M. P. Ryan and J. J. Hinojosa, “Conceptual obstacles to making use of four smoking-cessation strategies: what reasons do light smokers give for rejecting strategies?” Health Psychology Open, vol. 2, no. 2, article 2055102915624928, 2015. View at Publisher · View at Google Scholar
  118. L. F. Stead, R. Perera, C. Bullen et al., “Nicotine replacement therapy for smoking cessation,” Cochrane Database of Systematic Reviews, vol. 11, article CD000146, 2012. View at Google Scholar
  119. P. M. Cinciripini, D. W. Wetter, and J. B. McClure, “Scheduled reduced smoking: effects on smoking abstinence and potential mechanisms of action,” Addictive Behaviors, vol. 22, no. 6, pp. 759–767, 1997. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Shapiro, G. E. Schwartz, B. Tursky, and S. R. Shnidman, “Smoking on cue: a behavioral approach to smoking reduction,” Journal of Health and Social Behavior, vol. 12, no. 2, pp. 108–113, 1971. View at Publisher · View at Google Scholar
  121. K. Morphett, B. Partridge, C. Gartner, A. Carter, and W. Hall, “Why don’t smokers want help to quit? A qualitative study of smokers’ attitudes towards assisted vs. unassisted quitting,” International Journal of Environmental Research and Public Health, vol. 12, no. 6, pp. 6591–6607, 2015. View at Publisher · View at Google Scholar · View at Scopus
  122. A. Black, E. Beard, J. Brown, J. Fidler, and R. West, “Beliefs about the harms of long-term use of nicotine replacement therapy: perceptions of smokers in England,” Addiction, vol. 107, no. 11, pp. 2037–2042, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. B. P. Rafacho, P. Santos, H. B. Assalin et al., “Role of vitamin D in the cardiac remodeling induced by tobacco smoke exposure,” International Journal of Cardiology, vol. 155, no. 3, pp. 472–3, 2012. View at Publisher · View at Google Scholar · View at Scopus
  124. S. I. Bibli, I. Andreadou, C. Glynos et al., “Exposure to cigarette smoke abrogates the beneficial effect of ischemic postconditioning,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 311, no. 5, pp. H1321–H1332, 2016. View at Publisher · View at Google Scholar · View at Scopus
  125. X. Zhou, L. Zhao, J. Mao, J. Huang, and J. Chen, “Antioxidant effects of hydrogen sulfide on left ventricular remodeling in smoking rats are mediated via PI3K/Akt-dependent activation of Nrf2,” Toxicological Sciences, vol. 144, no. 1, pp. 197–203, 2015. View at Publisher · View at Google Scholar · View at Scopus
  126. D. Reis Junior, E. L. Antonio, M. F. de Franco, H. A. de Oliveira, P. J. Tucci, and A. J. Serra, “Association of exercise training with tobacco smoking prevents fibrosis but has adverse impact on myocardial mechanics,” Nicotine & Tobacco Research, vol. 18, no. 12, pp. 2268–2272, 2016. View at Publisher · View at Google Scholar
  127. L. A. Zornoff, D. R. Duarte, M. F. Minicucci et al., “Effects of beta-carotene and smoking on heart remodeling after myocardial infarction,” Arquivos Brasileiros de Cardiologia, vol. 89, no. 3, pp. 135–141, 2007, 151-7. View at Google Scholar
  128. D. R. Duarte, L. C. Oliveira, M. F. Minicucci et al., “Effects of the administration of beta-blockers on ventricular remodeling induced by cigarette smoking in rats,” Arquivos Brasileiros de Cardiologia, vol. 92, no. 6, pp. 443–447, 2009, 462-6, 479-83. View at Google Scholar
  129. F. Denipote, L. P. Ardisson, P. S. Azevedo et al., “Influence of taurine on cardiac remodeling induced by tobacco smoke exposure,” Cellular Physiology and Biochemistry, vol. 27, no. 3-4, pp. 291–298, 2011. View at Publisher · View at Google Scholar · View at Scopus
  130. B. Zhu, Y. Sun, R. E. Sievers et al., “L-arginine decreases infarct size in rats exposed to environmental tobacco smoke,” American Heart Journal, vol. 132, no. 1, Part 1, pp. 91–100, 1996. View at Google Scholar