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Cigarette Smoke Exacerbates Ventricular Remodeling and Dysfunction in the Volume Overloaded Heart

Published online by Cambridge University Press:  08 December 2011

Jessica M. Bradley
Affiliation:
Department of Physiology, Louisiana State University Health Sciences Center, 1901 Perdido Street, New Orleans, LA 70112, USA
Jonathan B. Nguyen
Affiliation:
Department of Physiology, Louisiana State University Health Sciences Center, 1901 Perdido Street, New Orleans, LA 70112, USA
Alyssa C. Fournett
Affiliation:
Department of Physiology, Louisiana State University Health Sciences Center, 1901 Perdido Street, New Orleans, LA 70112, USA
Jason D. Gardner*
Affiliation:
Department of Physiology, Louisiana State University Health Sciences Center, 1901 Perdido Street, New Orleans, LA 70112, USA
*
Corresponding author. E-mail: [email protected]
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Abstract

Cigarette smoking is an independent risk factor for heart disease and is linked to sudden cardiac death. In this study, we examined the effects of cigarette smoke (CS) on the volume overload stressed heart. Our hypothesis was that CS exacerbates volume overload (VO)–induced cardiac dysfunction by accelerating ventricular remodeling. VO stress was surgically induced in male Sprague-Dawley rats by abdominal aortocaval fistula (ACF). Rats, with and without ACF, were exposed to either room air or CS (6 cigarettes/day) for 6 weeks. Temporal echocardiogram measurements indicated that CS significantly increased VO-induced left ventricular dilatation, prevented compensatory wall thickening, and depressed fractional shortening. Morphological analysis of ventricular collagen revealed that CS blunted compensatory collagen expression (45% decrease versus ACF alone). CS exacerbated the VO-induced increase of MMP-9 and TIMP-1 expression in the heart. CS also blocked the compensatory increases of HIF-1α, VEGF, and TGF-β in the VO-stressed heart. These data indicate that CS worsens VO remodeling by disrupting compensatory mechanisms, thereby promoting eccentric dilation and dysfunction.

Type
Feature Article
Copyright
Copyright © Microscopy Society of America 2012

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References

REFERENCES

Adachi, C., Naruse, M., Ishihara, Y., Tanabe, A., Takagi, S., Yoshimoto, T., Naruse, K., Kagawa, J. & Takano, K. (2000). Effects of acute and chronic cigarette smoking on the expression of endothelin-1 mRNA of the cardiovascular tissue in rats. J Cardiovasc Pharm 36, S198S200.CrossRefGoogle ScholarPubMed
Ambrose, J.A. & Barua, R.S. (2004). The pathophysiology of cigarette smoking and cardiovascular disease. J Am Coll Cardiol 43(10), 17311737.CrossRefGoogle ScholarPubMed
Azzalini, L., Ferrer, E., Ramalho, L.N., Moreno, M., Domínguez, M., Colmenero, J., Peinado, V.I., Barberà, J.A., Arroyo, V., Ginès, P., Caballería, J. & Bataller, R. (2010). Cigarette smoking exacerbates nonalcoholic fatty liver disease in obese rats. Hepatology 51(5), 15671576.CrossRefGoogle ScholarPubMed
Brown, L.A., Nunez, D.J., Brookes, C.I.O. & Wilkins, M.R. (1995). Selective increase in endothelin-1 and endothelin A receptor subtype in the hypertrophied myocardium of the aotro-venacaval fistula rat. Cardiovasc Res 29(6), 768774.CrossRefGoogle ScholarPubMed
Castardeli, E., Duarte, D.R., Minicucci, M.F., Azevedo, P.S., Matsubara, B.B., Matsubara, L.S., Campana, A.O., Paiva, S.A.R. & Zornoff, L.A.M. (2007). Tobacco smoke-induced left ventricular remodeling is not associated with metalloporteinase-2 of -9 activation. Eur J Heart Fail 9, 10811085.CrossRefGoogle Scholar
Castardeli, E., Paiva, S.A.R., Matsubara, B.B., Matsubara, L.S., Minicucci, M.F., Azevedo, P.S., Campana, A.O. & Zornoff, L.A.M. (2005). Chronic cigarette smoke exposure results in cardiac remodeling and impaired ventricular function in rats. Arq Bras Cardiol 84(4), 320324.CrossRefGoogle ScholarPubMed
Chen, L.-J., Zhao, Y., Gao, S., Chou, I.-N., Toselli, P., Stone, P. & Li, W. (2004). Downregulation of lysyl oxidase and upregulation of cellular thiols in rat fetal lung fibroblasts treated with cigarette smoke condensate. Toxicol Sci 83, 372379.CrossRefGoogle ScholarPubMed
Edirisinghe, I., Arunachalam, G., Wong, C., Yao, H., Rahman, A., Phipps, R.P., Jin, Z.-G. & Rahman, I. (2010). Cigarette smoke-induced oxidative/nitrosative stress impairs VEGF- and fluid shear stress-mediated signaling in endothelial cells. Andioxid Redox Signal 12(12), 13551369.CrossRefGoogle ScholarPubMed
Edirisinghe, I. & Rahman, I. (2010). Cigarette smoke-mediated oxidative stress, shear stress, and endothelial dysfunction: Role of VEGFR 2. Ann NY Acad Sci 1203, 6672.CrossRefGoogle Scholar
Frantz, S., Hu, K., Adamek, A., Wolf, J., Sallam, A., Kg Maier, S., Lonning, S., Ling, H., Ertl, G. & Bauersachs, J. (2008). Transforming growth factor beta inhibition increases mortality and left ventricular dilatation after myocardial infarction. Basic Res Cardiol 103(5), 485492.CrossRefGoogle ScholarPubMed
Gao, S., Chen, K., Zhao, Y., Rich, C.B., Chen, L., Li, S.J., Toselli, P., Stone, P. & Li, W. (2005). Transcriptional and posttranscriptional inhibition of lysyl oxidase expression by cigarette smoke condensate in cultured rat fetal lung fibroblasts. Toxicol Sci 87(1), 197203.CrossRefGoogle ScholarPubMed
Gardner, J.D., Brower, G.L. & Janicki, J.S. (2005). Effects of dietary phytoestrogens on cardiac remodeling secondary to chronic volume overload in femal rats. J Appl Physiol 99, 13781383.CrossRefGoogle Scholar
Griffith, R. & Standafer, S. (1985). Simultaneous mainstream-sidestream smoke exposure systems II. The rat exposure system. Toxicology 35(1), 1324.CrossRefGoogle ScholarPubMed
Gu, L., Pandey, V., Greenen, D.L., Chowdhury, S.A.K. & Piano, M.R. (2008). Cigarette smoke-induced left ventricular remodeling is associated with activation of mitrogen-activated protein kinases. Eur J Heart Fail 10, 10571064.CrossRefGoogle Scholar
Gunja-Smith, Z., Morales, A.R., Romanelli, R. & Woessner, J.F.W. Jr. (1996). Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy: Role of metalloproteinases and pyridinoline cross-links. Am J Pathol 148(5), 16391648.Google ScholarPubMed
Haak, T., Jungmann, E., Raab, C. & Usadel, K.H. (1994). Elevated endothelin-1 levels after cigarette smoking. Metabolism 43(3), 267269.CrossRefGoogle ScholarPubMed
Hansson, J., Vasan, R.S., Arnlov, J., Ingelsson, E., Lind, L., Larsson, A., Michaelsson, K. & Sundstrom, J. (2011). Biomarkers of extracellular matrix metabolism (MMP-9 and TIMP-1) and risk of stroke, myocardial infarction, and cause-specific mortality: Cohort study. PLoS One 6(1), e16185.CrossRefGoogle ScholarPubMed
Higgins, D.F., Biju, M.P., Akai, Y., Wutz, A., Johnson, R.S. & Haase, V.H. (2004). Hypoxic induction of Ctgf is directly mediated by Hif-1. Am J Physiol-Renal 287(6), F1223F1232.CrossRefGoogle ScholarPubMed
Hutchinson, K.R., Stewart, J.A. Jr. & Lucchesi, P.A. (2010). Extracellular matrix remodeling during the progression of volume overload-induced heart failure. J Molec Cell Cardiol 48, 564569.CrossRefGoogle ScholarPubMed
Izumiya, Y., Shiojima, I., Sato, K., Sawyer, D., Colucci, W. & Walsh, K. (2006). Vascular endothelin growth factor blockade promotes the transition from compensatory cardiac hypertrophy to failure in response to pressure overload. Hypertension 47, 887893.CrossRefGoogle Scholar
Jorgensen, L.N., Kallehave, F., Christensen, E., Siana, J.E. & Gottrup, F. (1998). Less collagen production in smokers. Surgery 123(4), 450455.CrossRefGoogle ScholarPubMed
Jourdan-LeSaux, C., Zhang, J. & Lindsey, M.L. (2010). Extracellular matrix roles during cardiac repair. Life Sci 87, 391400.CrossRefGoogle ScholarPubMed
Knuutinen, A., Kokkonen, N., Risteli, J., Vahakangas, K., Kallioinen, M., Salo, T., Sorsa, T. & Oikarinen, A. (2002). Smoking affects collagen synthesis and extracellular matrix turnover in human skin British. J Dermatol 146, 588594.Google Scholar
Lim, H. & Zhu, Y.Z. (2006). Role of transforming growth factor-B in the progression of heart failure. Cell Mol Life Sci 63, 25842596.CrossRefGoogle Scholar
Lu, Y., Azad, N., Wang, L., Iyer, A.K.V., Castranova, V., Jiang, B.-H. & Rojanasakul, Y. (2010). Phosphatidylinositol-3-kinase/Akt regulates bleomycin-induced fibroblast proliferation and collagen production. Am J Respir Cell Mol Biol 42, 432441.CrossRefGoogle ScholarPubMed
Lucas, J.A., Zhang, Y., Li, P., Gong, K., Miller, A.P., Hassan, E., Hage, F., Xing, D., Wells, B., Oparil, S. & Chen, Y.-F. (2010). Inhibition of transforming growth factor-B signaling induces left ventricular dilation and dysfunction in the pressure overload heart. Am J Physiol Heart Circ Physiol 298, H424H432.CrossRefGoogle Scholar
Margulies, K., Hildebrand, F., Lerman, A., Perrella, M. & Burnett, J. Jr. (1990). Increased endothelin in experimental heart failure. Circulation 82, 22262230.CrossRefGoogle ScholarPubMed
McMurray, J., Ray, S., Abdullah, I., Dargie, H. & Morton, J. (1992). Plasma endothelin in chronic heart failure. Circulation 85, 13741379.CrossRefGoogle ScholarPubMed
Michaud, S.E., Ménard, C., Guy, L.G., Gennaro, G. & Rivard, A. (2003). Inhibition of hypoxia-induced angiogenesis by cigarette smoke exposure: Impairment of the HIF-1alpha/VEGF pathway. FASEB J 17(9), 11501152.CrossRefGoogle ScholarPubMed
Morimoto, Y., Tsuda, T., Nakamura, H., Hori, H., Yamato, H., Nagata, N., Higashi, T., Kido, M. & Tanaka, I. (1997). Expression of matrix metalloproteinases, tissue inhibitiors of metalloproteinases, and extracellular matrix mRNA following exposure to mineral fibers and cigarette smoke in vivo. Exp Health Persp 105, 12471251.Google Scholar
Pauschinger, M., Knof, D., Petschauer, S., Doerner, A., Poller, W., Schwimmbeck, P.L., Kuhl, U. & Schultheiss, H.-P. (1999). Dilated cardiomyopathy is associated with significant changes in collagen type I/III. Circulation 99, 27502756.CrossRefGoogle ScholarPubMed
Raveendran, M., Senthil, D., Utama, B., Shen, Y., Dudley, D., Wang, J., Zhang, Y. & Wang, X.L. (2004). Cigarette suppresses the expression of P4Ha and vascular collagen production. BBRC 323, 592598.Google Scholar
Rudnicki, M., Perco, P., Enrich, J., Eder, S., Heininger, D., Bernthaler, A., Wiesinger, M., Sarkozi, R., Noppert, S.-J., Schramek, H., Mayer, B., Oberbauer, R. & Mayer, G. (2009). Hypoxia response and VEGF—A expression in human proximal tubular epithelial cells in stable and progressive renal disease. Lab Invest 89(3), 337346.CrossRefGoogle ScholarPubMed
Shiojima, I., Sato, K., Izumiya, Y., Schiekofer, S., Ito, M., Liao, R. & Colucci, W. (2005). Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failuer. J Clin Invest 58, 2637.Google Scholar
Spain, D.M. & Bradess, V.A. (1970). Sudden death from coronary heart disease: Survival time, frequency of thrombi, and cigarette smoking. Chest 58, 107110.CrossRefGoogle ScholarPubMed
Spinale, F.G., Coker, M.L., Thomas, C.V., Walker, J.D., Mukherjee, R. & Hebbar, L. (1998). Time-dependent changes in matrix metalloproteinase activity and expression during the progression of congesitve heart failure: Relation to ventricular and myocyte function. Circ Res 82, 482495.CrossRefGoogle ScholarPubMed
Spinella, F., Rosano, L., Castro, V.D., Natalis, P.G. & Bagnato, A. (2002). Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1a in ovarian carcinoma cells. J Biol Chem 277, 2785027855.CrossRefGoogle Scholar
Thackaberry, E.A., Gabaldon, D.M., Walker, M.K. & Smith, S.M. (2002). Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1 a in the absence of cardiac hypoxia. Cardiovasc Toxicol 2, 263273.CrossRefGoogle ScholarPubMed
Villarreal, F.J. & Dillmann, W.H. (1992). Cardiac hypertrophy-induced changes in mRNA levles for TGF-B1, fibronectin, and collagen. Am J Physiol Heart Circ Physiol 262, H1861H1866.CrossRefGoogle Scholar
Villarreal, F.J., Hong, D. & Omens, J. (1999). Nicotine-modified postinfarction left ventricular remodeling. Am J Physiol Heart Circ Physiol 276, H1103H1106.CrossRefGoogle ScholarPubMed
Voloshenyuk, T.G. & Gardner, J.D. (2010). Estrogen improves TIMP-MMP balance and collagen distribution in volume-overloaded hearts of ovariectomized females. Am J Physiol Regul Integr Comp Physiol 299, R686R693.CrossRefGoogle ScholarPubMed
Voloshenyuk, T.G., Landesman, E.S., Khoutorova, E., Hart, A.D. & Gardner, J.D. (2011). Induction of cardiac fibroblast lysyl oxidase by TGF-[beta]1 requires PI3K/Akt, Smad3, and MAPK signaling. Cytokine 55(1), 9097.CrossRefGoogle Scholar
Weber, K.T. (1997). Extracellular matrix remodeling in heart failure. Circulation 96, 40654082.CrossRefGoogle ScholarPubMed
Zentilin, L., Puligadda, U., Lionetti, V., Zacchigna, S., Collesi, C., Pattarini, L., Ruozi, G., Camporesi, S., Sinagra, G., Pepe, M., Recchia, F.A. & Giacca, M. (2010). Cardiomyocyte VEGFR-1 activation by VEGF-B induces compensatory hypertrophy and preserves cardiac function after myocardial infarction FASEB J 24(5), 14671478.CrossRefGoogle ScholarPubMed
Zhu, B., Sun, Y., Sievers, R., Glantz, S., Parmley, W. & Wolfe, C. (1994). Exposure to environmental tobacco smoke increased myocardial infarct size in rats. Circulation 89, 12821290.CrossRefGoogle ScholarPubMed
Zornoff, L.A., Matsubara, B.B., Matsubara, L.S., Mincucci, M.F., Azevedo, P.S., Campanha, A.O. & Paiva, S.A.R. (2006). Cigarette smoke exposure intensifies ventricular remodeling process following myocardial infarction. Arq Bras Cardiol 86(4), 276281.Google ScholarPubMed