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

Volumn 125, Issue 22, 2012, Pages 2716-2727

  Gielen, Stephan ^a   Sandri, Marcus ^b   Kozarez, Irina ^b   Kratzsch, Jürgen ^c   Teupser, Daniel ^c   Thiery, Joachim ^c   Erbs, Sandra ^b   Mangner, Norman ^b   Lenk, Karsten ^b   Hambrecht, Rainer ^d   Schuler, Gerhard ^b   Adams, Volker ^b  

^a MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^d Zentralkrankenhaus Links der Weser   (Germany)

Author keywords

Aging; Chronic heart failure; Exercise training; Ubiquitin proteasome system

Indexed keywords

ACETYLSALICYLIC ACID; ANTIVITAMIN K; ATROGIN 1; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CATHEPSIN L; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; MUSCLE RING FINGER 1 PROTEIN; PROTEASOME; SOMATOMEDIN C; SPIRONOLACTONE; UBIQUITIN;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CARDIOPULMONARY EXERCISE TEST; CONTROLLED STUDY; DYSLIPIDEMIA; ENDURANCE TRAINING; HEART FAILURE; HUMAN; HYPERTENSION; LYSOSOME; MAJOR CLINICAL STUDY; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE FUNCTION; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; WESTERN BLOTTING;

AGED; AGING; BIOPSY; CATHEPSIN L; CHRONIC DISEASE; EXERCISE; GERMANY; HEART FAILURE; HUMANS; MIDDLE AGED; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHYSICAL ENDURANCE; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, MESSENGER; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84861881181     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.047381     Document Type: Article

References (43)

1. American Heart Association. Heart Disease and Stroke Statistics: 2010 Update. Dallas, TX: American Heart Association; 2010.
2. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159:413-421. (Pubitemid 38200776)
3. Janssen I. Influence of sarcopenia on the development of physical disability: the Cardiovascular Health Study. J Am Geriatr Soc. 2006;54: 56-62.
4. Anker SD, Ponikowski P, Varney S, Chua TP, Clark AL, Webb-Peploe KM, Harrington D, Kox WJ, Poole-Wilson P, Coats AJS. Wasting as independent risk factor for mortality in chronic heart failure. Lancet. 1997;349:1050-1053. (Pubitemid 27158249)
5. Hambrecht R, Schulze PC, Gielen S, Linke A, Mobius-Winkler S, Yu J, Kratzsch JJ, Baldauf G, Busse MW, Schubert A, Adams V, Schuler G. Reduction of insulin-like growth factor-I expression in the skeletal muscle of noncachectic patients with chronic heart failure. J Am Coll Cardiol. 2002;39:1175-1181. (Pubitemid 34267422)
6. Gielen S, Adams V, Möbius-Winkler S, Linke A, Erbs S, Yu J, Kempf W, Schubert A, Schuler G, Hambrecht R. Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol. 2003;42:861-868. (Pubitemid 37059745)
7. Patterson C, Ike C, Willis PW, Stouffer GA, Willis MS. The bitter end: the ubiquitin-proteasome system and cardiac dysfunction. Circulation. 2007;115:1456-1463. (Pubitemid 46648383)
8. Herrmann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res. 2007;100:1276-1291. (Pubitemid 46742918)
9. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science. 2001; 294:1704-1708. (Pubitemid 33104839)
10. Adams V, Linke A, Wisloff U, Doring C, Erbs S, Krankel N, Witt CC, Labeit S, Muller-Werdan U, Schuler G, Hambrecht R. Myocardial expression of MuRF-1 and MAFbx after induction of chronic heart failure: effect on myocardial contractility. Cardiovasc Res. 2007;73: 120-129. (Pubitemid 44937197)
11. Li Y-P, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 2005;19: 362-370. (Pubitemid 40316524)
12. Wassermann K, Whipp BJ, Koyal SH, Beaver WL. Anaerobic threshold and respiratory gas exchange during exercise. J Appl Physiol. 1973;35: 236-243.
13. Niebauer J, Pflaum CD, Clark AL, Strasburger CJ, Hooper J, Poole-Wilson PA, Coats AJ, Anker SD. Deficient insulin-like growth factor I in chronic heart failure predicts altered body composition, anabolic deficiency, cytokine and neurohormonal activation. J Am Coll Cardiol. 1998; 32:393-397. (Pubitemid 28396488)
14. Kratzsch J, Blum WF, Schenker E, Keller E, Jahreis G, Haustein B, Ventz M, Rotzsch W. Measurements of insulin-like growth factor I (IGF-I) in normal adults, patients with liver cirrhosis and acromegaly: experience with a new competitive enzyme immunoassay. Exp Clin Endocrinol. 1993;101:144-149. (Pubitemid 23270622)
15. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest. 2004;113: 115-123. (Pubitemid 38541638)
16. Bechet D, Tassa A, Taillandier D, Combaret L, Attaix D. Lysosomal proteolysis in skeletal muscle. Int J Biochem Cell Biol. 2005;37: 2098-2114. (Pubitemid 41206824)
17. Bartoli M, Richard I. Calpains in muscle wasting. Int J Biochem Cell Biol. 2005;37:2115-2133. (Pubitemid 41206825)
18. Solomon V, Lecker SH, Goldberg AL. The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J Biol Chem. 1998;273:25216-25222. (Pubitemid 28443284)
19. Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr. 1999;129:227S-237S. (Pubitemid 29035981)
20. Lecker SH. Ubiquitin-protein ligases in muscle wasting: multiple parallel pathways? Curr Opin Clin Nutr Metab Care. 2003;6:271-275. (Pubitemid 40684602)
21. Murton AJ, Constantin D, Greenhaff PL. The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim Biophys Acta. 2008;1782:730-743.
22. Foletta VC, White LJ, Larsen AE, Léger B, Russell AP. The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pflugers Arch. 2011;461:325-335.
23. Altun M, Besche HC, Overkleeft HS, Piccirillo R, Edelmann MJ, Kessler BM, Goldberg AL, Ulfhake B. Muscle wasting in aged, sarcopenic rats is associated with enhanced activity of the ubiquitin proteasome pathway. J Biol Chem. 2010;285:39597-39608.
24. Timmerman KL, Volpi E. Amino acid metabolism and regulatory effects in aging. Curr Opin Clin Nutr Metab Care. 2008;11:45-49. (Pubitemid 350295226)
25. Salanova M, Schiffl G, Püttmann B, Schoser BG, Blottner D. Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long-term bed rest with and without countermeasures. J Anat. 2008;212:306-318. (Pubitemid 351325486)
26. Radom-Aizik S, Kaminski N, Hayek S, Halkin H, Cooper DM, Ben-Dov I. Effects of exercise training on quadriceps muscle gene expression in chronic obstructive pulmonary disease. J Appl Physiol. 2007;102: 1976-1984. (Pubitemid 46701970)
27. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 2007;6:376-385. (Pubitemid 350011998)
28. McElhinny AS, Kakinuma K, Sorimachi H, Labeit S, Gregorio CC. Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1. J Cell Biol. 2002;157:125-136. (Pubitemid 34847835)
29. Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP, Leibovitch SA. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem. 2005;280:2847-2856. (Pubitemid 40189393)
30. Lagirand-Cantaloube J, Offner N, Csibi A, Leibovitch MP, Batonnet-Pichon S, Tintignac LA, Segura CT, Leibovitch SA. The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J. 2008;27:1266-1276. (Pubitemid 351574748)
31. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004;117:399-412. (Pubitemid 38534545)
32. McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, Esser KA. FoxO1 induces apoptosis in skeletal myotubes in a DNA-bindingdependent manner. Am J Physiol. 2009;297:C548-C555.
33. Senf SM, Dodd SL, McClung JM, Judge AR. Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J. 2008;22:3836-3845.
34. Magnusson G, Gordon A, Kaijser L, Sylven C, Isberg B, Karpakka J, Saltin B. High intensity knee extensor training in patients with chronic heart failure. Eur Heart J. 1996;17:1048-1055. (Pubitemid 26252523)
35. Hambrecht R, Schulze PC, Gielen S, Linke A, Mobius-Winkler S, Erbs S, Kratzsch J, Schubert A, Adams V, Schuler G. Effects of exercise training on insulin-like growth factor-I expression in the skeletal muscle of noncachectic patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2005;12:401-406. (Pubitemid 41192174)
36. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaBindependent, FoxO1-dependent mechanism. J Cell Physiol. 2006;209: 501-514. (Pubitemid 44484641)
37. Lenk K, Erbs S, Hö llriege R, Beck E, Linke A, Gielen S, Möbius Winkler S, Sandri M, Hambrecht R, Schuler G, Adams V. Exercise training leads to a reduction of elevated myostatin levels in patients with chronic heart failure [published online ahead of print March 14, 2011]. Eur J Cardiovasc Prev Rehabil. http://www.ncbi.nlm.nih.gov/pubmed/21450574.
38. McMahon CD, Popovic L, Oldham JM, Jeanplong F, Smith HK, Kambadur R, Sharma M, Maxwell L, Bass JJ. Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension. Am J Physiol. 2003;285:E82-E87. (Pubitemid 36736364)
39. Heineke J, Auger-Messier M, Xu J, Sargent M, York A, Welle S, Molkentin JD. Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation. 2010;121: 419-425.
40. Forman DE, Clare R, Kitzman DW, Ellis SJ, Fleg JL, Chiara T, Fletcher G, Kraus WE. Relationship of age and exercise performance in patients with heart failure: the HF-ACTION study. Am Heart J. 2009;158: S6-S15.
41. Erbs S, Höllriegel R, Linke A, Beck EB, Adams V, Gielen S, Möbius-Winkler S, Sandri M, Kränkel N, Hambrecht R, Schuler G. Exercise training in patients with advanced chronic heart failure (NYHA IIIb) promotes restoration of peripheral vasomotor function, induction of endogenous regeneration, and improvement of left ventricular function. Circ Heart Fail. 2010;3:486-494.
42. Muscaritoli M, Anker SD, Argilés J, Aversa Z, Bauer JM, Biolo G, Boirie Y, Bosaeus I, Cederholm T, Costelli P, Fearon KC, Laviano A, Maggio M, Rossi Fanelli F, Schneider SM, Schols A, Sieber CC. Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) "cachexia-anorexia in chronic wasting diseases" and "nutrition in geriatrics." Clin Nutr. 2010;29: 154-159.
43. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel J-P, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39:412-423.