Table of Contents
ISRN Hypertension
Volume 2013 (2013), Article ID 980824, 9 pages
http://dx.doi.org/10.5402/2013/980824
Review Article

Cardiac Effects of Exercise Training in Hypertension

Biobehavioral Research Laboratory and Department of Biobehavioral and Health Sciences, School of Nursing, University of Pennsylvania, 126 Claire M. Fagin Hall, 418 Curie Boulevard, Philadelphia, PA 19104-4217, USA

Received 29 November 2012; Accepted 18 December 2012

Academic Editors: A. A. Noorbala and A. A. Tahrani

Copyright © 2013 Joseph R. Libonati. 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. V. Chobanian, G. L. Bakris, H. R. Black et al., “The seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. The JNC 7 report,” Hypertension, vol. 42, pp. 1206–1252, 2003. View at Google Scholar
  2. P. M. Kearney, M. Whelton, K. Reynolds, P. Muntner, P. K. Whelton, and J. He, “Global burden of hypertension: analysis of worldwide data,” The Lancet, vol. 365, no. 9455, pp. 217–223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. R. S. Vasan, A. Beiser, S. Seshadri et al., “Residual lifetime risk for developing hypertension in middle-aged women and men: the Framingham heart study,” The Journal of the American Medical Association, vol. 287, no. 8, pp. 1003–1010, 2002. View at Google Scholar · View at Scopus
  4. J. A. Halbert, C. A. Silagy, P. Finucane, R. T. Withers, P. A. Hamdorf, and G. R. Andrews, “The effectiveness of exercise training in lowering blood pressure: a meta-analysis of randomised controlled trials of 4 weeks or longer,” Journal of Human Hypertension, vol. 11, no. 10, pp. 641–649, 1997. View at Google Scholar · View at Scopus
  5. S. P. Whelton, A. Chin, X. Xin, and J. He, “Effect of aerobic exercise on blood pressure: a meta-analysis of randomized, controlled trials,” Annals of Internal Medicine, vol. 136, no. 7, pp. 493–503, 2002. View at Google Scholar · View at Scopus
  6. R. H. Fagard, “Exercise characteristics and the blood pressure response to dynamic physical training,” Medicine and Science in Sports and Exercise, vol. 33, no. 6, pp. S484–S492, 2001. View at Google Scholar
  7. L. S. Pescatello, B. A. Franklin, R. Fagard, W. B. Farquhar, G. A. Kelley, and C. A. Ray, “American College of sports medicine position stand. Exercise and hypertension,” Medicine and Science in Sports and Exercise, vol. 36, no. 3, pp. 533–553, 2004. View at Google Scholar · View at Scopus
  8. G. A. Kelley, K. A. Kelley, and Z. V. Tran, “Aerobic exercise and resting blood pressure: a meta-analytic review of randomized, controlled trials,” Preventive Cardiology, vol. 4, no. 2, pp. 73–80, 2001. View at Google Scholar · View at Scopus
  9. G. A. Kelley, K. S. Kelley, and Z. V. Tran, “Walking and resting blood pressure in adults: a meta-analysis,” Preventive Medicine, vol. 33, no. 2 I, pp. 120–127, 2001. View at Google Scholar · View at Scopus
  10. M. Marceau, N. Kouame, Y. Lacourciere, and J. Cleroux, “Effects of different training intensities on 24-hour blood pressure in hypertensive subjects,” Circulation, vol. 88, no. 6, pp. 2803–2811, 1993. View at Google Scholar
  11. G. L. Jennings, G. Deakin, P. Korner, I. Meredith, B. Kingwell, and L. Nelson, “What is the dose-response relationship between exercise training and blood pressure?” Annals of Medicine, vol. 23, no. 3, pp. 313–318, 1991. View at Google Scholar · View at Scopus
  12. J. V. Jessup, D. T. Lowenthal, M. L. Pollock, and T. Turner, “The effects of endurance exercise training on ambulatory blood pressure in normotensive older adults,” Geriatric Nephrology and Urology, vol. 8, no. 2, pp. 103–109, 1998. View at Google Scholar · View at Scopus
  13. J. Kraul, J. Chrastek, and J. Adamirova, “The hypotensive effect of physical activity,” in Prevention of Ischemic Heart Disease: Principles and Practice, W. Rabb, Ed., pp. 359–371, Charles Thomas, Springfield, Ill, USA, 1966. View at Google Scholar
  14. F. M. Fouad, J. M. Slominski, and R. C. Tarazi, “Left ventricular diastolic function in hypertension: relation to left ventricular mass and systolic function,” Journal of the American College of Cardiology, vol. 3, no. 6, pp. 1500–1506, 1984. View at Google Scholar · View at Scopus
  15. E. D. Frohlich, C. Apstein, A. V. Chobanian et al., “The heart in hypertension,” The New England Journal of Medicine, vol. 327, no. 14, pp. 998–1008, 1992. View at Google Scholar · View at Scopus
  16. O. H. Cingolani, X. P. Yang, M. A. Cavasin, and O. A. Carretero, “Increased systolic performance with diastolic dysfunction in adult spontaneously hypertensive rats,” Hypertension, vol. 41, no. 2, pp. 249–254, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. M. M. Redfield, S. J. Jacobsen, J. C. Burnett Jr., D. W. Mahoney, K. R. Bailey, and R. J. Rodeheffer, “Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic,” The Journal of the American Medical Association, vol. 289, no. 2, pp. 194–202, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Frey and E. N. Olson, “Cardiac hypertrophy: the good, the bad and the ugly,” Annual Review of Physiology, vol. 65, pp. 45–79, 2003. View at Publisher · View at Google Scholar
  19. J. D. Molkentin, “Calcineurin—NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs,” Cardiovascular Research, vol. 63, no. 3, pp. 467–475, 2004. View at Publisher · View at Google Scholar
  20. J. D. Molkentin, J. R. Lu, C. L. Antos et al., “A calcineurin-dependent transcriptional pathway for cardiac hypertrophy,” Cell, vol. 93, no. 2, pp. 215–228, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Zou, Y. Hiroi, H. Uozumi et al., “Calcineurin plays a critical role in the development of pressure overload-induced cardiac hypertrophy,” Circulation, vol. 104, no. 1, pp. 97–101, 2001. View at Google Scholar · View at Scopus
  22. J. A. Hill, M. Karimi, W. Kutschke et al., “Cardiac hypertrophy is not a required compensatory response to short-term pressure overload,” Circulation, vol. 101, no. 24, pp. 2863–2869, 2000. View at Google Scholar · View at Scopus
  23. T. Taigen, L. J. de Windt, H. W. Lim, and J. D. Molkentin, “Targeted inhibition of calcineurin prevents agonist-induced cardiomyocyte hypertrophy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 3, pp. 1196–1201, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. L. J. de Windt, H. W. Lim, O. F. Bueno et al., “Targeted inhibition of calcineurin attenuates cardiac hypertrophy in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 6, pp. 3322–3327, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. S. C. Kolwicz, S. M. MacDonnell, B. F. Renna et al., “Left ventricular remodeling with exercise in hypertension,” American Journal of Physiology, vol. 297, no. 4, pp. H1361–H1368, 2009. View at Publisher · View at Google Scholar
  26. A. P. Beltrami, L. Barlucchi, D. Torella et al., “Adult cardiac stem cells are multipotent and support myocardial regeneration,” Cell, vol. 114, no. 6, pp. 763–776, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Anversa and B. Nadal-Ginard, “Myocyte renewal and ventricular remodelling,” Nature, vol. 415, no. 6868, pp. 240–243, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Nadal-Ginard, J. Kajstura, A. Leri, and P. Anversa, “Myocyte death, growth, and regeneration in cardiac hypertrophy and failure,” Circulation Research, vol. 92, no. 2, pp. 139–150, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. B. F. Renna, S. M. MacDonnell, P. O. Reger, D. L. Crabbe, S. R. Houser, and J. R. Libonati, “Relative systolic dysfunction in female spontaneously hypertensive rat myocardium,” Journal of Applied Physiology, vol. 103, no. 1, pp. 353–358, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. J. R. Libonati, A. Sabri, C. Xiao, S. M. Macdonnell, and B. F. Renna, “Exercise training improves systolic function in hypertensive myocardium,” Journal of Applied Physiology, vol. 111, no. 6, pp. 1637–1643, 2011. View at Publisher · View at Google Scholar
  31. P. M. Kang and S. Izumo, “Apoptosis and heart failure: a critical review of the literature,” Circulation Research, vol. 86, no. 11, pp. 1107–1113, 2000. View at Google Scholar · View at Scopus
  32. S. Nagata, “Apoptosis by death factor,” Cell, vol. 88, no. 3, pp. 355–365, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. C. H. Conrad, W. W. Brooks, J. A. Hayes, S. Sen, K. G. Robinson, and O. H. L. Bing, “Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat,” Circulation, vol. 91, no. 1, pp. 161–170, 1995. View at Google Scholar · View at Scopus
  34. O. H. L. Bing, W. W. Brooks, K. G. Robinson et al., “The spontaneously hypertensive rat as a model of the transition from compensated left ventricular hypertrophy to failure,” Journal of Molecular and Cellular Cardiology, vol. 27, no. 1, pp. 383–396, 1995. View at Google Scholar · View at Scopus
  35. S. R. Datta, A. Brunet, and M. E. Greenberg, “Cellular survival: a play in three akts,” Genes and Development, vol. 13, no. 22, pp. 2905–2927, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Del Peso, M. González-García, C. Page, R. Herrera, and G. Nuñez, “Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt,” Science, vol. 278, no. 5338, pp. 687–689, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. S. G. Kennedy, E. S. Kandel, T. K. Cross, and N. Hay, “Akt/ PKB inhibits cell death by preventing the release of cytochrome c from mitochondria,” Molecular and Cellular Biology, vol. 19, no. 8, pp. 5800–5810, 1990. View at Google Scholar
  38. M. H. Cardone, N. Roy, H. R. Stennicke et al., “Regulation of cell death protease caspase-9 by phosphorylation,” Science, vol. 282, no. 5392, pp. 1318–1321, 1998. View at Google Scholar · View at Scopus
  39. J. R. McMullen, T. Shioi, L. Zhang et al., “Phosphoinositide 3-kinase(p110α) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 21, pp. 12355–12360, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. R. McMullen, T. Shioi, W. Y. Huang et al., “The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110α) pathway,” The Journal of Biological Chemistry, vol. 279, no. 6, pp. 4782–4793, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Wiedemann, T. Wessela, K. Schwarz et al., “Inhibition of anti-apoptotic signals by Wortmannin induces apoptosisin the remote myocardium after LAD ligation: evidence for a protein kinase C-δ-dependent pathway,” Molecular and Cellular Biochemistry, vol. 372, no. 1-2, pp. 275–283, 2013. View at Publisher · View at Google Scholar
  42. F. L. Atkins, O. H. L. Bing, P. G. DiMauro, C. H. Conrad, K. G. Robinson, and W. W. Brooks, “Modulation of left and right ventricular β-adrenergic receptors from spontaneously hypertensive rats with left ventricular hypertrophy and failure,” Hypertension, vol. 26, no. 1, pp. 78–82, 1995. View at Google Scholar · View at Scopus
  43. C. Limas and C. J. Limas, “Reduced number of β-adrenergic receptors in the myocardium of spontaneously hypertensive rats,” Biochemical and Biophysical Research Communications, vol. 83, no. 2, pp. 710–714, 1978. View at Google Scholar · View at Scopus
  44. D. J. Choi, W. J. Koch, J. J. Hunter, and H. A. Rockman, “Mechanism of β-adrenergic receptor desensitization in cardiac hypertrophy is increased β-adrenergic receptor kinase,” The Journal of Biological Chemistry, vol. 272, no. 27, pp. 17223–17229, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. L. F. Santana, E. G. Chase, V. S. Votaw, M. T. Nelson, and R. Greven, “Functional coupling of calcineurin and protein kinase A in mouse ventricular myocytes,” Journal of Physiology, vol. 544, no. 1, pp. 57–69, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. S. M. MacDonnell, H. Kubo, D. M. Harris et al., “Calcineurin inhibition normalizes β-adrenergic responsiveness in the spontaneously hypertensive rat,” American Journal of Physiology, vol. 293, no. 5, pp. H3122–H3129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Bers, Excitation-Contraction Coupling and Cardiac Contractile Force, Kluwer Academic, New York, NY, USA, 2nd edition, 2003.
  48. M. Castellano and M. Böhm, “The cardiac β-adrenoceptor-mediated signaling pathway and its alterations in hypertensive heart disease,” Hypertension, vol. 29, no. 3, pp. 715–722, 1997. View at Google Scholar · View at Scopus
  49. Z. M. Huang, J. I. Gold, and W. J. Koch, “G protein-coupled receptor kinases in normal and failing myocardium,” Frontiers in Bioscience, vol. 16, pp. 3047–3060, 2011. View at Google Scholar
  50. W. Zhu, N. Petrashevskaya, S. Ren et al., “Gi-biased β2AR signaling links GRK2 upregulation to heart failure,” Circulation Research, vol. 110, no. 2, pp. 265–274, 2012. View at Publisher · View at Google Scholar
  51. C. Gauthier, G. Tavernier, F. Charpentier, D. Langin, and H. Le Marec, “Functional β3-adrenoceptor in the human heart,” Journal of Clinical Investigation, vol. 98, no. 2, pp. 556–562, 1996. View at Google Scholar · View at Scopus
  52. D. M. Kaye, S. D. Wiviott, and R. A. Kelly, “Activation of nitric oxide synthase (NOS3) by mechanical activity alters contractile activity in a Ca2+-independent manner in cardiac myocytes: role of troponin 1 phosphorylation,” Biochemical and Biophysical Research Communications, vol. 256, no. 2, pp. 398–403, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Bevegard, A. Holmgren, and B. Jonsson, “Circulatory studies in well trained athletes at rest and during heavy exercise. With special reference to stroke volume and the influence of body position,” Acta Physiologica Scandinavica, vol. 57, pp. 26–50, 1963. View at Google Scholar · View at Scopus
  54. J. R. Libonati, “Myocardial diastolic function and exercise,” Medicine and Science in Sports and Exercise, vol. 31, no. 12, pp. 1741–1747, 1999. View at Google Scholar · View at Scopus
  55. A. J. Woodiwiss and G. R. Norton, “Exercise-induced cardiac hypertrophy is associated with an increased myocardial compliance,” Journal of Applied Physiology, vol. 78, no. 4, pp. 1303–1311, 1995. View at Google Scholar · View at Scopus
  56. A. J. Woodiwiss, W. J. Kalk, and G. R. Norton, “Habitual exercise attenuates myocardial stiffness in diabetes mellitus in rats,” American Journal of Physiology, vol. 271, no. 5, pp. H2126–H2133, 1996. View at Google Scholar · View at Scopus
  57. R. L. Moore and B. M. Palmer, “Exercise training and cellular adaptations of normal and diseased hearts,” Exercise and Sport Sciences Reviews, vol. 27, pp. 285–315, 1999. View at Google Scholar · View at Scopus
  58. J. Scheuer, A. Malhotra, and C. Hirsch, “Physiologic cardiac hypertrophy corrects contractile protein abnormalities associated with pathologic hypertrophy in rats,” Journal of Clinical Investigation, vol. 70, no. 6, pp. 1300–1305, 1982. View at Google Scholar · View at Scopus
  59. P. O. Reger, M. F. Barbe, M. Amin et al., “Myocardial hypoperfusion/reperfusion tolerance with exercise training in hypertension,” Journal of Applied Physiology, vol. 100, no. 2, pp. 541–547, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. J. L. J. Vanoverschelde, B. Essamri, R. Vanbutsele et al., “Contribution of left ventricular diastolic function to exercise capacity in normal subjects,” Journal of Applied Physiology, vol. 74, no. 5, pp. 2225–2233, 1993. View at Google Scholar · View at Scopus
  61. C. D. Garciarena, O. A. Pinilla, M. B. Nolly et al., “Endurance training in the spontaneously hypertensive rat conversion of pathological into physiological cardiac hypertrophy,” Hypertension, vol. 53, no. 4, pp. 708–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. R. M. da Costa Rebelo, R. Schreckenberg, and K. D. Schlüter, “Adverse cardiac remodelling in spontaneously hypertensive rats: acceleration by high aerobic exercise intensity,” Journal of Physiology, vol. 590, no. 21, pp. 5389–5400, 2012. View at Publisher · View at Google Scholar
  63. J. R. Libonati, “Cardiac remodeling and exercise training in hypertension,” Current Hypertension Reviews, vol. 7, no. 1, pp. 20–28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. H. P. Baglivo, G. Fabregues, H. Burrieza, R. C. Esper, M. Talarico, and R. J. Esper, “Effect of moderate physical training on left ventricular mass in mild hypertensive persons,” Hypertension, vol. 15, no. 2, supplement, pp. I-153–I-156, 1990. View at Google Scholar · View at Scopus
  65. P. A. Ades, P. G. S. Gunther, W. L. Meyer, T. C. Gibson, J. Maddalena, and T. Orfeo, “Cardiac and skeletal muscle adaptations to training in systemic hypertension and effect of beta blockade (metoprolol or propranolol),” American Journal of Cardiology, vol. 66, no. 5, pp. 591–596, 1990. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Jamshidi, H. E. Montgomery, H. W. Hense et al., “Peroxisome proliferator—activated receptor alpha gene regulates left ventricular growth in response to exercise and hypertension,” Circulation, vol. 105, no. 8, pp. 950–955, 2002. View at Google Scholar
  67. A. Hinderliter, A. Sherwood, E. C. D. Gullette et al., “Reduction of left ventricular hypertrophy after exercise and weight loss in overweight patients with mild hypertension,” Archives of Internal Medicine, vol. 162, no. 12, pp. 1333–1339, 2002. View at Google Scholar · View at Scopus
  68. K. J. Stewart, P. Ouyang, A. C. Bacher, S. Lima, and E. P. Shapiro, “Exercise effects on cardiac size and left ventricular diastolic function: relationships to changes in fitness, fatness, blood pressure and insulin resistance,” Heart, vol. 92, no. 7, pp. 893–898, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Palatini, P. Visentin, F. Dorigatti et al., “Regular physical activity prevents development of left ventricular hypertrophy in hypertension,” European Heart Journal, vol. 30, no. 2, pp. 225–232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. P. F. Kokkinos, P. Narayan, J. A. Colleran et al., “Effects of regular exercise on blood pressure and left ventricular hypertrophy in African-American men with severe hypertension,” The New England Journal of Medicine, vol. 333, no. 22, pp. 1462–1467, 1995. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Zanettini, D. Bettega, O. Agostoni et al., “Exercise training in mild hypertension: effects on blood pressure, left ventricular mass and coagulation factor VII and fibrinogen,” Cardiology, vol. 88, no. 5, pp. 468–473, 1997. View at Google Scholar · View at Scopus
  72. M. J. Turner, R. J. Spina, W. M. Kohrt, and A. A. Ehsani, “Effect of endurance exercise training onleft ventricular size and remodeling in older adults with hypertension,” Journals of Gerontology—Series A, vol. 55, no. 4, pp. M245–M251, 2000. View at Google Scholar · View at Scopus
  73. M. R. Rinder, R. J. Spina, L. R. Peterson, C. J. Koenig, C. R. Florence, and A. A. Ehsani, “Comparison of effects of exercise and diuretic on left ventricular geometry, mass, and insulin resistance in older hypertensive adults,” American Journal of Physiology, vol. 287, no. 2, pp. R360–R368, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Boman, M. Olofsson, B. Dahlöf et al., “Left ventricular structure and function in sedentary and physically active subjects with left ventricular hypertrophy (the LIFE study),” American Journal of Cardiology, vol. 95, no. 2, pp. 280–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. M. J. Fregly, “Effect of an exercise regimen on development of hypertension in rats,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 56, no. 2, pp. 381–387, 1984. View at Google Scholar · View at Scopus
  76. S. E. DiCarlo, H. L. Collins, D. W. Rodenbaugh, M. R. Smitha, R. D. Berger, and V. K. Yeragani, “Daily exercise reduces measures of heart rate and blood pressure variability in hypertensive rats,” Clinical and Experimental Hypertension, vol. 24, no. 3, pp. 221–234, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. N. S. Gava, A. C. Veras-Silva, C. E. Negrao, and E. M. Krieger, “Low-intensity exercise training attenuates cardiac β-adrenergic tone during exercise in spontaneously hypertensive rats,” Hypertension, vol. 26, no. 6, pp. 1129–1133, 1995. View at Google Scholar · View at Scopus
  78. E. M. Krieger, P. C. Brum, and C. E. Negrão, “State-of-the-art lecture: influence of exercise training on neurogenic control of blood pressure in spontaneously hypertensive rats,” Hypertension, vol. 34, no. 4, part 2, pp. 720–723, 1999. View at Google Scholar · View at Scopus
  79. C. Y. Huang, A. L. Yang, Y. M. Lin et al., “Anti-apoptotic and pro-survival effects of exercise training on hypertensive hearts,” Journal of Applied Physiology, vol. 112, no. 5, pp. 883–891, 2012. View at Publisher · View at Google Scholar
  80. S. C. Kolwicz, S. M. MacDonnell, Z. V. Kendrick, S. R. Houser, and J. R. Libonati, “Voluntary wheel running and pacing-induced dysfunction in hypertension,” Clinical and Experimental Hypertension, vol. 30, no. 7, pp. 565–573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. S. C. Kolwicz, H. Kubo, S. M. MacDonnell, S. R. Houser, and J. R. Libonati, “Effects of forskolin on inotropic performance and phospholamban phosphorylation in exercise-trained hypertensive myocardium,” Journal of Applied Physiology, vol. 102, no. 2, pp. 628–633, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. B. F. Renna, H. Kubo, S. M. MacDonnell et al., “Enhanced acidotic myocardial Ca2+ responsiveness with training in hypertension,” Medicine and Science in Sports and Exercise, vol. 38, no. 5, pp. 847–855, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. L. V. Rossoni, R. A. Oliveira, R. R. Caffaro et al., “Cardiac benefits of exercise training in aging spontaneously hypertensive rats,” Journal of Hypertension, vol. 29, no. 12, pp. 2349–2358, 2011. View at Publisher · View at Google Scholar
  84. K. D. Marshall, B. N. Muller, M. Krenz et al., “Heart failure with preserved ejection fraction: chronic low-intensity interval exercise training preserves myocardial O2 balance and diastolic function,” Journal of Applied Physiology. In press. View at Publisher · View at Google Scholar
  85. M. Iemitsu, T. Miyauchi, S. Maeda et al., “Physiological and pathological cardiac hypertrophy induce different molecular phenotypes in the rat,” American Journal of Physiology, vol. 281, no. 6, pp. R2029–R2036, 2001. View at Google Scholar · View at Scopus
  86. J. R. Libonati and J. P. Gaughan, “Low-intensity exercise training improves survival in Dahl salt hypertension,” Medicine and Science in Sports and Exercise, vol. 38, no. 5, pp. 856–858, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. A. J. Chicco, S. A. McCune, C. A. Emter et al., “Low-intensity exercise training delays heart failure and improves survival in female hypertensive heart failure rats,” Hypertension, vol. 51, no. 4, pp. 1096–1102, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. P. A. Mole, “Increased contractile potential of papillary muscles from exercise-trained rat hearts,” American Journal of Physiology, vol. 3, no. 4, pp. H421–H425, 1978. View at Google Scholar · View at Scopus
  89. R. J. Spina, T. Ogawa, A. R. Coggan, J. O. Holloszy, and A. A. Ehsani, “Exercise training improves left ventricular contractile response to β-adrenergic agonist,” Journal of Applied Physiology, vol. 72, no. 1, pp. 307–311, 1992. View at Google Scholar · View at Scopus
  90. R. J. Spina, S. Rashid, V. G. Dávila-Román, and A. A. Ehsani, “Adaptations in β-adrenergic cardiovascular responses to training in older women,” Journal of Applied Physiology, vol. 89, no. 6, pp. 2300–2305, 2000. View at Google Scholar · View at Scopus
  91. R. J. Spina, M. J. Turner, and A. A. Ehsani, “β-adrenergic-mediated improvement in left ventricular function by exercise training in older men,” American Journal of Physiology, vol. 274, no. 2, pp. H397–H404, 1998. View at Google Scholar · View at Scopus
  92. R. Stones, A. Natali, R. Billeter, S. Harrison, and E. White, “Voluntary exercise-induced changes in β2-adrenoceptor signalling in rat ventricular myocytes,” Experimental Physiology, vol. 93, no. 9, pp. 1065–1075, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. O. E. Suman, D. Hasten, M. J. Turner, M. R. Rinder, R. J. Spina, and A. A. Ehsani, “Enhanced inotropic response to dobutamine in strength-trained subjects with left ventricular hypertrophy,” Journal of Applied Physiology, vol. 88, no. 2, pp. 534–539, 2000. View at Google Scholar · View at Scopus
  94. N. Takeda, P. Dominiak, D. Turck, H. Rupp, and R. Jacob, “The influence of endurance training on mechanical catecholamine responsiveness, β-adrenoceptor density and myosin isoenzyme pattern of rat ventricular myocardium,” Basic Research in Cardiology, vol. 80, no. 1, pp. 88–99, 1985. View at Google Scholar · View at Scopus
  95. M. G. Hopkins, R. J. Spina, and A. A. Ehsani, “Enhanced β-adrenergic-mediated cardiovascular responses in endurance athletes,” Journal of Applied Physiology, vol. 80, no. 2, pp. 516–521, 1996. View at Google Scholar · View at Scopus
  96. J. Barbier, F. Rannou-Bekono, J. Marchais, P. M. Berthon, P. Delamarche, and F. Carré, “Effect of training on β1 β2 β 3 adrenergic and M2 muscarinic receptors in rat heart,” Medicine and Science in Sports and Exercise, vol. 36, no. 6, pp. 949–954, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Barbier, S. Reland, N. Ville, F. Rannou-Bekono, S. Wong, and F. Carré, “The effects of exercise training on myocardial adrenergic and muscarinic receptors,” Clinical Autonomic Research, vol. 16, no. 1, pp. 61–65, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. E. O. Werle, G. Strobel, and H. Weicker, “Decrease in rat cardiac beta1- and beta2-adrenoceptors by training and endurance exercise,” Life Sciences, vol. 46, no. 1, pp. 9–17, 1990. View at Publisher · View at Google Scholar · View at Scopus
  99. G. E. Billman, M. Kukielka, R. Kelley, M. Moustafa-Bayoumi, and R. A. Altschuld, “Endurance exercise training attenuates cardiac β2-adrenoceptor responsiveness and prevents ventricular fibrillation in animals susceptible to sudden death,” American Journal of Physiology, vol. 290, no. 6, pp. H2590–H2599, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. B. J. Holycross, M. Kukielka, Y. Nishijima, R. A. Altschuld, C. A. Carnes, and G. E. Billman, “Exercise training normalizes β-adrenoceptor expression in dogs susceptible to ventricular fibrillation,” American Journal of Physiology, vol. 293, no. 5, pp. H2702–H2709, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. M. S. Houle, R. A. Altschuld, and G. E. Billman, “Enhanced in vivo and in vitro contractile responses to β2-adrenergic receptor stimulation in dogs susceptible to lethal arrhythmias,” Journal of Applied Physiology, vol. 91, no. 4, pp. 1627–1637, 2001. View at Google Scholar · View at Scopus
  102. M. Bohm, H. Dorner, P. Htun, H. Lensche, D. Platt, and E. Erdmann, “Effects of exercise on myocardial adenylate cyclase and G(i)α expression in senescence,” American Journal of Physiology, vol. 264, no. 3, part 2, pp. H805–H814, 1993. View at Google Scholar · View at Scopus
  103. W. R. Davidson Jr., S. P. Banerjee, and C. S. Liang, “Dobutamine-induced cardiac adaptations: comparison with exercise-trained and sedentary rats,” American Journal of Physiology, vol. 250, no. 5, part 2, pp. H725–H730, 1986. View at Google Scholar · View at Scopus
  104. G. L. Dohm, S. N. Pennington, and H. Barakat, “Effect of exercise training on adenyl cyclase and phosphodiesterase in skeletal muscle, heart, and liver,” Biochemical Medicine, vol. 16, no. 2, pp. 138–142, 1976. View at Google Scholar · View at Scopus
  105. D. Leosco, G. Rengo, G. Iaccarino et al., “Exercise training and β-blocker treatment ameliorate age-dependent impairment of β-adrenergic receptor signaling and enhance cardiac responsiveness to adrenergic stimulation,” American Journal of Physiology, vol. 293, no. 3, pp. H1596–H1603, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. D. Leosco, G. Rengo, G. Iaccarino et al., “Exercise promotes angiogenesis and improves β-adrenergic receptor signalling in the post-ischaemic failing rat heart,” Cardiovascular Research, vol. 78, no. 2, pp. 385–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. R. S. Mazzeo, D. A. Podolin, and V. Henry, “Effects of age and endurance training on β-adrenergic receptor characteristics in Fischer 344 rats,” Mechanisms of Ageing and Development, vol. 84, no. 2, pp. 157–169, 1995. View at Publisher · View at Google Scholar · View at Scopus
  108. R. L. Moore, M. Riedy, and P. D. Gollnick, “Effect of training on β-adrenergic receptor number in rat heart,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 52, no. 5, pp. 1133–1137, 1982. View at Google Scholar · View at Scopus
  109. J. L. Nieto, I. D. Laviada, A. Guillén, and A. Haro, “Adenylyl cyclase system is affected differently by endurance physical training in heart and adipose tissue,” Biochemical Pharmacology, vol. 51, no. 10, pp. 1321–1329, 1996. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Plourde, S. Rousseau-Migneron, and A. Nadeau, “β-adrenoceptor adenylate cyclase system adaptation to physical training in rat ventricular tissue,” Journal of Applied Physiology, vol. 70, no. 4, pp. 1633–1638, 1991. View at Google Scholar · View at Scopus
  111. J. R. Libonati and S. M. MacDonnell, “Cardiac β-adrenergic responsiveness with exercise,” European Journal of Applied Physiology, vol. 111, no. 11, pp. 2735–2741, 2011. View at Publisher · View at Google Scholar
  112. J. M. Scott, B. T. A. Esch, M. J. Haykowsky et al., “Sex differences in left ventricular function and β-receptor responsiveness following prolonged strenuous exercise,” Journal of Applied Physiology, vol. 102, no. 2, pp. 681–687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. R. L. Schultz, J. G. Swallow, R. P. Waters et al., “Effects of excessive long-term exercise on cardiac function and myocyte remodeling in hypertensive heart failure rats,” Hypertension, vol. 50, no. 2, pp. 410–416, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. P. O. Reger, S. C. Kolwicz, and J. R. Libonati, “Acute exercise exacerbates ischemia-induced diastolic rigor in hypertensive myocardium,” SpringerPlus, vol. 1, article 46, 2012. View at Publisher · View at Google Scholar