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Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 6709742, 9 pages
https://doi.org/10.1155/2018/6709742
Research Article

Role of Exercise-Induced Cardiac Remodeling in Ovariectomized Female Rats

1Department of Physiology, Anatomy and Neuroscience, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary
2Department of Orthopaedics, University of Debrecen, Debrecen, Hungary
3Department of Pharmacology and Pharmacotherapy, University of Debrecen, Debrecen, Hungary

Correspondence should be addressed to Anikó Pósa; uh.degezs-u.oib@okinap

Received 25 August 2017; Revised 21 November 2017; Accepted 8 January 2018; Published 13 February 2018

Academic Editor: Undurti N. Das

Copyright © 2018 Renáta Szabó 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. A. Pósa, K. Kupai, R. Ménesi et al., “Sexual dimorphism of cardiovascular ischemia susceptibility is mediated by heme oxygenase,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 521563, 11 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. Z. Jouyandeh, F. Nayebzadeh, M. Qorbani, and M. Asadi, “Metabolic syndrome and menopause,” Journal of Diabetes & Metabolic Disorders, vol. 12, no. 1, p. 1, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. W. Kosmala, R. Plaksej, M. Przewlocka-Kosmala, J. Kuliczkowska-Plaksej, G. Bednarek-Tupikowska, and W. Mazurek, “Matrix metalloproteinases 2 and 9 and their tissue inhibitors 1 and 2 in premenopausal obese women: relationship to cardiac function,” International Journal of Obesity, vol. 32, no. 5, pp. 763–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Pedram, M. Razandi, F. O'Mahony, D. Lubahn, and E. R. Levin, “Estrogen receptor-β prevents cardiac fibrosis,” Molecular Endocrinology, vol. 24, no. 11, pp. 2152–2165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. M. A. Düzenli, K. Ozdemir, A. Sokmen et al., “Effects of menopause on the myocardial velocities and myocardial performance index,” Circulation Journal, vol. 71, no. 11, pp. 1728–1733, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Rienks, A. P. Papageorgiou, N. G. Frangogiannis, and S. Heymans, “Myocardial extracellular matrix: an ever-changing and diverse entity,” Circulation Research, vol. 114, no. 5, pp. 872–888, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. S. L. Bowers and T. A. Baudino, “Cardiac myocyte-fibroblast interactions and the coronary vasculature,” Journal of Cardiovascular Translational Research, vol. 5, no. 6, pp. 783–793, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. C. A. Souders, S. L. Bowers, and T. A. Baudino, “Cardiac fibroblast: the renaissance cell,” Circulation Research, vol. 105, no. 12, pp. 1164–1176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. K. E. Porter and N. A. Turner, “Cardiac fibroblasts: at the heart of myocardial remodeling,” Pharmacology & Therapeutics, vol. 123, no. 2, pp. 255–278, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Fan, A. Takawale, J. Lee, and Z. Kassiri, “Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease,” Fibrogenesis & Tissue Repair, vol. 5, no. 1, p. 15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. D. T. Nguyen, C. Ding, E. Wilson, G. M. Marcus, and J. E. Olgin, “Pirfenidone mitigates left ventricular fibrosis and dysfunction after myocardial infarction and reduces arrhythmias,” Heart Rhythm, vol. 7, no. 10, pp. 1438–1445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Sawicki, “Intracellular regulation of matrix metalloproteinase-2 activity: new strategies in treatment and protection of heart subjected to oxidative stress,” Scientifica, vol. 2013, Article ID 130451, 12 pages, 2013. View at Publisher · View at Google Scholar
  13. S. Loffek, O. Schilling, and C. W. Franzke, “Series “matrix metalloproteinases in lung health and disease”: biological role of matrix metalloproteinases: a critical balance,” The European Respiratory Journal, vol. 38, no. 1, pp. 191–208, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. M. M. Benjamin and R. A. Khalil, “Matrix metalloproteinase inhibitors as investigative tools in the pathogenesis and management of vascular disease,” Experientia Supplementum, vol. 103, pp. 209–279, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. H. B. Kwak, J.h. Kim, K. Joshi, A. Yeh, D. A. Martinez, and J. M. Lawler, “Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart,” The FASEB Journal, vol. 25, no. 3, pp. 1106–1117, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. C. M. Marques, F. A. M. Nascimento, C. A. Mandarim-de-Lacerda, and M. B. Aguila, “Exercise training attenuates cardiovascular adverse remodeling in adult ovariectomized spontaneously hypertensive rats,” Menopause, vol. 13, no. 1, pp. 87–95, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. C. Campos, K. M. Gomes, and J. C. Ferreira, “Impact of exercise training on redox signaling in cardiovascular diseases,” Food and Chemical Toxicology, vol. 62, pp. 107–119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Pósa, R. Szabó, K. Kupai et al., “Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 787063, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Pósa, R. Szabó, A. Csonka et al., “Endogenous estrogen-mediated heme oxygenase regulation in experimental menopause,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 429713, 7 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Pósa, R. Szabó, K. Kupai et al., “Cardioprotective effects of voluntary exercise in a rat model: role of matrix metalloproteinase-2,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 876805, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Kong, P. Christia, and N. G. Frangogiannis, “The pathogenesis of cardiac fibrosis,” Cellular and Molecular Life Sciences, vol. 71, no. 4, pp. 549–574, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. M. A. Horn and A. W. Trafford, “Aging and the cardiac collagen matrix: novel mediators of fibrotic remodelling,” Journal of Molecular and Cellular Cardiology, vol. 93, pp. 175–185, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. G. L. Brower, J. D. Gardner, M. F. Forman et al., “The relationship between myocardial extracellular matrix remodeling and ventricular function,” European Journal of Cardio-Thoracic Surgery, vol. 30, no. 4, pp. 604–610, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Kania, P. Blyszczuk, and U. Eriksson, “Mechanisms of cardiac fibrosis in inflammatory heart disease,” Trends in Cardiovascular Medicine, vol. 19, no. 8, pp. 247–252, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Russo and N. G. Frangogiannis, “Diabetes-associated cardiac fibrosis: cellular effectors, molecular mechanisms and therapeutic opportunities,” Journal of Molecular and Cellular Cardiology, vol. 90, pp. 84–93, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. C. J. Li, L. Lv, H. Li, and D. M. Yu, “Cardiac fibrosis and dysfunction in experimental diabetic cardiomyopathy are ameliorated by alpha-lipoic acid,” Cardiovascular Diabetology, vol. 11, no. 1, p. 73, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Bhupathy, C. D. Haines, and L. A. Leinwand, “Influence of sex hormones and phytoestrogens on heart disease in men and women,” Women’s Health, vol. 6, no. 1, pp. 77–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Posa, I. Pavo, and C. Varga, “Heme oxygenase contributes to estradiol and raloxifene-induced vasorelaxation in estrogen deficiency,” International Journal of Cardiology, vol. 189, pp. 252–254, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Lee, P. Cheng, S. Hong et al., “Oxidative stress induces vascular heme oxygenase-1 expression in ovariectomized rats,” Free Radical Biology & Medicine, vol. 39, no. 1, pp. 108–117, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. S. S. Signorelli, S. Neri, S. Sciacchitano et al., “Duration of menopause and behavior of malondialdehyde, lipids, lipoproteins and carotid wall artery intima-media thickness,” Maturitas, vol. 39, no. 1, pp. 39–42, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. S. A. Almeida, E. R. G. Claudio, V. F. Mengal et al., “Exercise training reduces cardiac dysfunction and remodeling in ovariectomized rats submitted to myocardial infarction,” PLoS One, vol. 9, no. 12, article e115970, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Cavalera, J. Wang, and N. G. Frangogiannis, “Obesity, metabolic dysfunction, and cardiac fibrosis: pathophysiological pathways, molecular mechanisms, and therapeutic opportunities,” Translational Research, vol. 164, no. 4, pp. 323–335, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. H. B. Kwak, “Aging, exercise, and extracellular matrix in the heart,” Journal of Exercise Rehabilitation, vol. 9, no. 3, pp. 338–347, 2013. View at Publisher · View at Google Scholar
  34. A. C. Felix, S. G. Dutra, G. C. Tezini, M. V. Simões, and H. C. de Souza, “Aerobic physical training increases contractile response and reduces cardiac fibrosis in rats subjected to early ovarian hormone deprivation,” Journal of Applied Physiology, vol. 118, no. 10, pp. 1276–1285, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. L. M. Yung, W. T. Wong, X. Y. Tian et al., “Inhibition of renin-angiotensin system reverses endothelial dysfunction and oxidative stress in estrogen deficient rats,” PLoS One, vol. 6, no. 3, article e17437, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Lejsková, S. Alušík, Z. Valenta, S. Adámková, and J. Piťha, “Natural postmenopause is associated with an increase in combined cardiovascular risk factors,” Physiological Research, vol. 61, no. 6, pp. 587–596, 2012. View at Google Scholar
  37. V. A. Braga, G. K. Couto, M. C. Lazzarin, L. V. Rossoni, and A. Medeiros, “Aerobic exercise training prevents the onset of endothelial dysfunction via increased nitric oxide bioavailability and reduced reactive oxygen species in an experimental model of menopause,” PLoS One, vol. 10, no. 4, article e0125388, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. J. H. Park, M. Iemitsu, S. Maeda, A. Kitajima, T. Nosaka, and N. Omi, “Voluntary running exercise attenuates the progression of endothelial dysfunction and arterial calcification in ovariectomized rats,” Acta Physiologica, vol. 193, no. 1, pp. 47–55, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. A. L. Jacob-Ferreira, M. Y. Kondo, P. K. Baral et al., “Phosphorylation status of 72 kDa MMP-2 determines its structure and activity in response to peroxynitrite,” PLoS One, vol. 8, no. 8, article e71794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Kupai, C. Csonka, V. Fekete et al., “Cholesterol diet-induced hyperlipidemia impairs the cardioprotective effect of postconditioning: role of peroxynitrite,” American Journal of Physiology Heart and Circulatory Physiology, vol. 297, no. 5, pp. H1729–H1735, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. M. W. Owens, S. A. Milligan, D. Jourd'heuil, and M. B. Grisham, “Effects of reactive metabolites of oxygen and nitrogen on gelatinase A activity,” The American Journal of Physiology, vol. 273, no. 2, pp. L445–L450, 1997. View at Publisher · View at Google Scholar
  42. S. Rajagopalan, X. P. Meng, S. Ramasamy, D. G. Harrison, and Z. S. Galis, “Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability,” The Journal of Clinical Investigation, vol. 98, no. 11, pp. 2572–2579, 1996. View at Publisher · View at Google Scholar
  43. R. Schulz, “Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches,” Annual Review of Pharmacology and Toxicology, vol. 47, no. 1, pp. 211–242, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. S. R. Emami, M. Jafari, R. Haghshenas, and A. Ravasi, “Impact of eight weeks endurance training on biochemical parameters and obesity-induced oxidative stress in high fat diet-fed rats,” The Journal of Exercise Nutrition & Biochemistry, vol. 20, no. 1, pp. 29–35, 2016. View at Publisher · View at Google Scholar
  45. J. A. Ansari, U. Bhandari, K. K. Pillai, and S. E. Haque, “Effect of rosuvastatin on obesity-induced cardiac oxidative stress in Wistar rats--a preliminary study,” Indian Journal of Experimental Biology, vol. 50, no. 3, pp. 216–222, 2012. View at Google Scholar
  46. C. R. Frasier, R. C. Sloan, P. A. Bostian et al., “Short-term exercise preserves myocardial glutathione and decreases arrhythmias after thiol oxidation and ischemia in isolated rat hearts,” Journal of Applied Physiology, vol. 111, no. 6, pp. 1751–1759, 2011. View at Publisher · View at Google Scholar · View at Scopus