Exercise training prevents oxidative stress and ubiquitin-proteasome system overactivity and reverse skeletal muscle atrophy in heart failure

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Cunha, Telma F ^a   Bacurau, Aline V N ^a   Moreira, Jose B N ^a   Paixão, Nathalie A ^a   Campos, Juliane C ^a   Ferreira, Julio C B ^a   Leal, Marcelo L ^a   Negrão, Carlos E ^a   Moriscot, Anselmo S ^a   Wisløff, Ulrik ^b   Brum, Patricia C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; LIPID HYDROPEROXIDE; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3;

AEROBIC EXERCISE; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE INTENSITY; HEART FAILURE; HUMAN; LIPID PEROXIDATION; MOUSE; MUSCLE ATROPHY; NONHUMAN; OXIDATIVE STRESS; PLANTARIS MUSCLE; PROTEIN CARBONYLATION; RANDOMIZED CONTROLLED TRIAL; SEDENTARY LIFESTYLE; SKELETAL MUSCLE;

AGED; AGED, 80 AND OVER; ANIMALS; EXERCISE THERAPY; FEMALE; HEART FAILURE; HUMANS; LIPID PEROXIDATION; MALE; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCULAR ATROPHY; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

MUS;

EID: 84864544174     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041701     Document Type: Article

References (61)

1. Mancini DM, Walter G, Reichek N, Lenkinski R, McCully KK, et al. ((1992)) Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure. Circulation 85:: 1364--1373.
2. Vescovo G, Ambrosio GB, Dalla Libera L, ((2001)) Apoptosis and changes in contractile protein pattern in the skeletal muscle in heart failure. Acta Physiol Scand 171:: 305--310.
3. von Haehling S, Anker SD, ((2010)) Cachexia as a major underestimated and unmet medical need: facts and numbers. J Cachex Sarcopenia Muscle 1:: 1--5.
4. Jackman RW, Kandarian SC, ((2004)) The molecular basis of skeletal muscle atrophy. American Journal of Physiology Cell Physiology 287:: C834--843.
5. Tsutsui H, Kinugawa S, Matsushima S, Yokota T, ((2011)) Oxidative stress in cardiac and skeletal muscle dysfunction associated with diabetes mellitus. J Clin Biochem Nutr 48:: 68--71.
6. Guarnier FA, Cecchini AL, Suzukawa AA, Maragno AL, Simao AN, et al. ((2010)) Time course of skeletal muscle loss and oxidative stress in rats with Walker 256 solid tumor. Muscle Nerve 42:: 950--958.
7. Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, et al. ((2007)) Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 292:: H1009--1017.
8. Choksi KB, Nuss JE, Deford JH, Papaconstantinou J, ((2008)) Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes. Free Radic Biol Med 45:: 826--838.
9. Attaix D, Combaret L, Bechet D, Taillandier D, ((2008)) Role of the ubiquitin-proteasome pathway in muscle atrophy in cachexia. Curr Opin Support Palliat Care 2:: 262--266.
10. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL, ((2001)) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98:: 14440--14445.
11. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. ((2001)) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:: 1704--1708.
12. Aiken CT, Kaake RM, Wang X, Huang L, ((2011)) Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics 10: R110 006924.
13. Shang F, Taylor A, ((2011)) Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 51:: 5--16.
14. Gomes-Marcondes MC, Tisdale MJ, ((2002)) Induction of protein catabolism and the ubiquitin-proteasome pathway by mild oxidative stress. Cancer Lett 180:: 69--74.
15. Pellegrino MA, Desaphy JF, Brocca L, Pierno S, Camerino DC, et al. ((2011)) Redox homeostasis, oxidative stress and disuse muscle atrophy. J Physiol 589:: 2147--2160.
16. Kuwahara H, Horie T, Ishikawa S, Tsuda C, Kawakami S, et al. ((2010)) Oxidative stress in skeletal muscle causes severe disturbance of exercise activity without muscle atrophy. Free Radic Biol Med 48:: 1252--1262.
17. Anker SD, Ponikowski P, Varney S, Chua TP, Clark AL, et al. ((1997)) Wasting as independent risk factor for mortality in chronic heart failure. Lancet 349:: 1050--1053.
18. Wisloff U, Stoylen A, Loennechen JP, Bruvold M, Rognmo O, et al. ((2007)) Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 115:: 3086--3094.
19. Negrao CE, Middlekauff HR, ((2008)) Adaptations in autonomic function during exercise training in heart failure. Heart Fail Rev 13:: 51--60.
20. Gielen S, Adams V, Linke A, Erbs S, Mobius-Winkler S, et al. ((2005)) Exercise training in chronic heart failure: correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur J Cardiovasc Prev Rehabil 12:: 393--400.
21. Bacurau AV, Jardim MA, Ferreira JC, Bechara LR, Bueno CR Jr, et al. ((2009)) Sympathetic hyperactivity differentially affects skeletal muscle mass in developing heart failure: role of exercise training. J Appl Physiol 106:: 1631--1640.
22. Hein L, Altman JD, Kobilka BK, ((1999)) Two functionally distinct alpha2-adrenergic receptors regulate sympathetic neurotransmission. Nature 402:: 181--184.
23. Brum PC, Kosek J, Patterson A, Bernstein D, Kobilka B, ((2002)) Abnormal cardiac function associated with sympathetic nervous system hyperactivity in mice. Am J Physiol Heart Circ Physiol 283:: H1838--1845.
24. Ferreira JC, Moreira JB, Campos JC, Pereira MG, Mattos KC, et al. ((2011)) Angiotensin receptor blockade improves the net balance of cardiac Ca(2+) handling-related proteins in sympathetic hyperactivity-induced heart failure. Life Sci 88:: 578--585.
25. Bueno CR Jr, Ferreira JC, Pereira MG, Bacurau AV, Brum PC, ((2010)) Aerobic exercise training improves skeletal muscle function and Ca2+ handling-related protein expression in sympathetic hyperactivity-induced heart failure. J Appl Physiol 109:: 702--709.
26. Medeiros A, Rolim NP, Oliveira RS, Rosa KT, Mattos KC, et al. ((2008)) Exercise training delays cardiac dysfunction and prevents calcium handling abnormalities in sympathetic hyperactivity-induced heart failure mice. J Appl Physiol 104:: 103--109.
27. Ferreira JC, Bacurau AV, Evangelista FS, Coelho MA, Oliveira EM, et al. ((2008)) The role of local and systemic renin angiotensin system activation in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Am J Physiol Regul Integr Comp Physiol 294:: R26--32.
28. Oliveira RS, Ferreira JC, Gomes ER, Paixao NA, Rolim NP, et al. ((2009)) Cardiac anti-remodelling effect of aerobic training is associated with a reduction in the calcineurin/NFAT signalling pathway in heart failure mice. J Physiol 587:: 3899--3910.
29. Ferreira JC, Rolim NP, Bartholomeu JB, Gobatto CA, Kokubun E, et al. ((2007)) Maximal lactate steady state in running mice: effect of exercise training. Clin Exp Pharmacol Physiol 34:: 760--765.
30. Rolim NP, Medeiros A, Rosa KT, Mattos KC, Irigoyen MC, et al. ((2007)) Exercise training improves the net balance of cardiac Ca2+ handling protein expression in heart failure. Physiol Genomics 29:: 246--252.
31. Pereira MG, Ferreira JC, Bueno CR Jr, Mattos KC, Rosa KT, et al. ((2009)) Exercise training reduces cardiac angiotensin II levels and prevents cardiac dysfunction in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Eur J Appl Physiol 105:: 843--850.
32. Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolff SP, ((1994)) Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine. Anal Biochem 220:: 403--409.
33. Bartholomeu JB, Vanzelli AS, Rolim NP, Ferreira JC, Bechara LR, et al. ((2008)) Intracellular mechanisms of specific beta-adrenoceptor antagonists involved in improved cardiac function and survival in a genetic model of heart failure. J Mol Cell Cardiol 45:: 240--249.
34. Schulze PC, Fang J, Kassik KA, Gannon J, Cupesi M, et al. ((2005)) Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ Res 97:: 418--426.
35. van Hees HW, Li YP, Ottenheijm CA, Jin B, Pigmans CJ, et al. ((2008)) Proteasome inhibition improves diaphragm function in congestive heart failure rats. Am J Physiol Lung Cell Mol Physiol 294:: L1260--1268.
36. Dalla-Libera L, Vescovo G, ((2005)) Is Myosin Ubiquitinisation a mechanism of skeletal muscle atrophy in heart failure? Basic Appl Myol 15:: 6.
37. Goncalves DA, Silveira WA, Lira EC, Graca FA, Paula-Gomes S, et al. ((2012)) Clenbuterol suppresses proteasomal and lysosomal proteolysis and atrophy-related genes in denervated rat soleus muscles independently of Akt. Am J Physiol Endocrinol Metab 302:: E123--133.
38. Goncalves DA, Lira EC, Baviera AM, Cao P, Zanon NM, et al. ((2009)) Mechanisms involved in 3′,5′-cyclic adenosine monophosphate-mediated inhibition of the ubiquitin-proteasome system in skeletal muscle. Endocrinology 150:: 5395--5404.
39. Moylan JS, Reid MB, ((2007)) Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35:: 411--429.
40. Muller FL, Song W, Liu Y, Chaudhuri A, Pieke-Dahl S, et al. ((2006)) Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic Biol Med 40:: 1993--2004.
41. Ohta Y, Kinugawa S, Matsushima S, Ono T, Sobirin MA, et al. ((2011)) Oxidative stress impairs insulin signal in skeletal muscle and causes insulin resistance in postinfarct heart failure. Am J Physiol Heart Circ Physiol 300:: H1637--1644.
42. Jahngen-Hodge J, Obin MS, Gong X, Shang F, Nowell TR Jr, et al. ((1997)) Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J Biol Chem 272:: 28218--28226.
43. Jamart C, Raymackers JM, Li An G, Deldicque L, Francaux M, ((2011)) Prevention of muscle disuse atrophy by MG132 proteasome inhibitor. Muscle Nerve 43:: 708--716.
44. Beehler BC, Sleph PG, Benmassaoud L, Grover GJ, ((2006)) Reduction of skeletal muscle atrophy by a proteasome inhibitor in a rat model of denervation. Exp Biol Med (Maywood) 231:: 335--341.
45. Willis MS, Townley-Tilson WH, Kang EY, Homeister JW, Patterson C, ((2010)) Sent to destroy: the ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res 106:: 463--478.
46. Li YF, Wang X, ((2011)) The role of the proteasome in heart disease. Biochim Biophys Acta 1809:: 141--149.
47. Nowis D, Maczewski M, Mackiewicz U, Kujawa M, Ratajska A, et al. ((2010)) Cardiotoxicity of the anticancer therapeutic agent bortezomib. Am J Pathol 176:: 2658--2668.
48. Laughlin MH, Roseguini B, ((2008)) Mechanisms for exercise training-induced increases in skeletal muscle blood flow capacity: differences with interval sprint training versus aerobic endurance training. J Physiol Pharmacol 59 Suppl 7: 71--88.
49. Batista ML Jr, Rosa JC, Lopes RD, Lira FS, Martins E Jr, et al. ((2010)) Exercise training changes IL-10/TNF-alpha ratio in the skeletal muscle of post-MI rats. Cytokine 49:: 102--108.
50. Gielen S, Adams V, Mobius-Winkler S, Linke A, Erbs S, et al. ((2003)) Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol 42:: 861--868.
51. Renault V, Thornell LE, Butler-Browne G, Mouly V, ((2002)) Human skeletal muscle satellite cells: aging, oxidative stress and the mitotic clock. Exp Gerontol 37:: 1229--1236.
52. Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, et al. ((2004)) The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol 39:: 17--24.
53. Zaccagnini G, Martelli F, Magenta A, Cencioni C, Fasanaro P, et al. ((2007)) p66(ShcA) and oxidative stress modulate myogenic differentiation and skeletal muscle regeneration after hind limb ischemia. J Biol Chem 282:: 31453--31459.
54. Toth MJ, Ward K, van der Velden J, Miller MS, Vanburen P, et al. ((2011)) Chronic heart failure reduces Akt phosphorylation in human skeletal muscle: relationship to muscle size and function. J Appl Physiol 110:: 892--900.
55. Barton-Davis ER, Shoturma DI, Sweeney HL, ((1999)) Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 167:: 301--305.
56. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, et al. ((2001)) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27:: 195--200.
57. Gielen S, Sandri M, Kozarez I, Kratzsch J, Teupser D, et al. ((2012)) Exercise Training Attenuates MuRF-1 Expression in the Skeletal Muscle of Patients With Chronic Heart Failure Independent of Age: The Randomized Leipzig Exercise Intervention in Chronic Heart Failure and Aging Catabolism Study. Circulation 125:: 2716--2727.
58. Feuerstein G, Ruffolo RR Jr, ((1998)) Beta-blockers in congestive heart failure: the pharmacology of carvedilol, a vasodilating beta-blocker and antioxidant, and its therapeutic utility in congestive heart failure. Adv Pharmacol 42:: 611--615.
59. Chopra M, Beswick H, Clapperton M, Dargie HJ, Smith WE, et al. ((1992)) Antioxidant effects of angiotensin-converting enzyme (ACE) inhibitors: free radical and oxidant scavenging are sulfhydryl dependent, but lipid peroxidation is inhibited by both sulfhydryl- and nonsulfhydryl-containing ACE inhibitors. J Cardiovasc Pharmacol 19:: 330--340.
60. Matsuo T, Iwade K, Hirata N, Yamashita M, Ikegami H, et al. ((2005)) Improvement of arterial stiffness by the antioxidant and anti-inflammatory effects of short-term statin therapy in patients with hypercholesterolemia. Heart Vessels 20:: 8--12.
61. Murray D, Vandewalker G, Matherne GP, Mahoney LT, ((1987)) Pulsed Doppler and two-dimensional echocardiography: comparison of halothane and isoflurane on cardiac function in infants and small children. Anesthesiology 67:: 211--217.