Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: Effect of different loading patterns and repeated exercise bouts

Journal of Applied Physiology

Volumn 103, Issue 5, 2007, Pages 1513-1522

  Nedergaard, A ^a,c   Vissing, K ^b   Overgaard, K ^b   Kjaer, M ^a   Schjerling, P ^c,d  

^a BISPEBJERG HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c Rigshospitalet   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Atrogin 1; Eccentric; Forkhead box O transcription factor; Muscle RING finger protein 1; Protein degradation

Indexed keywords

MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; PROTEASOME; PROTEIN ATROPIN 1; TRANSCRIPTION FACTOR FKHR; UBIQUITIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXERCISE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MUSCLE BIOPSY; NORMAL HUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ADULT; EXERCISE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCULAR DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; QUADRICEPS MUSCLE; RNA, MESSENGER; SKP CULLIN F-BOX PROTEIN LIGASES; TIME FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 35648993978     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01445.2006     Document Type: Article

References (58)

1. Arendt-Nielsen L. [Clinical use of pain measurement techniques]. Ugeskr Laeger 164: 1790-1795, 2002.
2. Belcastro AN, Shewchuk LD, Raj DA. Exercise-induced muscle injury: a calpain hypothesis. Mol Cell Biochem 179: 135-145, 1998.
3. Biolo G, Bosutti A, Iscra F, Toigo G, Gullo A, Guarnieri G. Contribution of the ubiquitin-proteasome pathway to overall muscle proteolysis in hypercatabolic patients. Metabolism 49: 689-691, 2000.
4. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol Endocrinol Metab 268: E514-E520, 1995.
5. 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 294: 1704-1708, 2001.
6. Centner T, Yano J, Kimura E, McElhinny AS, Pelin K, Witt CC, Bang ML, Trombitas K, Granzier H, Gregorio CC, Sorimachi H, Labeit S. Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. J Mol Biol 306: 717-726, 2001.
7. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
8. Coffey VG, Shield A, Canny BJ, Carey KA, Cameron-Smith D, Hawley JA. Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes. Am J Physiol Endocrinol Metab 290: E849-E855, 2006.
9. Crameri RM, Langberg H, Teisner B, Magnusson P, Schroder HD, Olesen JL, Jensen CH, Koskinen S, Suetta C, Kjaer M. Enhanced procollagen processing in skeletal muscle after a single bout of eccentric loading in humans. Matrix Biol 23: 259-264, 2004.
10. Cuthbertson DJ, Babraj J, Smith K, Wilkes E, Fedele MJ, Esser K, Rennie M. Anabolic signaling and protein synthesis in human skeletal muscle after dynamic shortening or lengthening exercise. Am J Physiol Endocrinol Metab 290: E731-E738, 2006.
11. Dheda K, Huggett JF, Bustin SA, Johnson MA, Rook G, Zumla A. Validation of housekeeping genes for normalizing RNA expression in real-time PCR. Biotechniques 37: 112-119, 2004.
12. Dietrichson P, Coakley J, Smith PE, Griffiths RD, Helliwell TR, Edwards RH. Conchotome and needle percutaneous biopsy of skeletal muscle. J Neurol Neurosurg Psychiatry 50: 1461-1467, 1987.
13. 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 113: 115-123, 2004.
14. Dupont-Versteegden EE, Fluckey JD, Knox M, Gaddy D, Peterson CA. The effect of flywheel-based resistance exercise on processes contributing to muscle atrophy during unloading in adult rats. J Appl Physiol 110: 202-212, 2006.
15. Gibala MJ, Interisano SA, Tarnopolsky MA, Roy BD, MacDonald JR, Yarasheski KE, MacDougall JD. Myofibrillar disruption following acute concentric and eccentric resistance exercise in strength-trained men. Can J Physiol Pharmacol 78: 656-661, 2000.
16. Glass DJ. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5: 87-90, 2003.
17. Goldberg AL. Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899, 2003.
18. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001.
19. Hather BM, Tesch PA, Buchanan P, Dudley GA. Influence of eccentric actions on skeletal muscle adaptations to resistance training. Acta Physiol Scand 143: 177-185, 1991.
20. Imae M, Fu Z, Yoshida A, Noguchi T, Kato H. Nutritional and hormonal factors control the gene expression of FoxOs, the mammalian homologues of DAF-16. J Mol Endocrinol 30: 253-262, 2003.
21. Jones SW, Hill RJ, Krasney PA, O'Conner B, Peirce N, Greenhaff PL. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18: 1025-1027, 2004.
22. Jonsdottir IH, Schjerling P, Ostrowski K, Asp S, Richter EA, Pedersen BK. Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J Physiol 528: 157-163, 2000.
23. Jorgensen SB, Wojtaszewski JF, Viollet B, Andreelli F, Birk JB, Hellsten Y, Schjerling P, Vaulont S, Neufer PD, Richter EA, Pilegaard H. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J 19: 1146-1148, 2005.
24. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123, 2004.
25. Kim PL, Staron RS, Phillips SM. Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J Physiol 568: 283-290, 2005.
26. Kwak KS, Zhou X, Solomon V, Baracos VE, Davis J, Bannon AW, Boyle WJ, Lacey DL, Han HQ. Regulation of protein catabolism by muscle-specific and cytokine-inducible ubiquitin ligase E3alpha-II during cancer cachexia. Cancer Res 64: 8193-8198, 2004.
27. LaStayo PC, Pierotti DJ, Pifer J, Hoppeler H, Lindstedt SL. Eccentric ergometry: increases in locomotor muscle size and strength at low training intensities. Am J Physiol Regul Integr Comp Physiol 278: R1282-R1288, 2000.
28. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51, 2004.
29. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP. Akt signalling through GSK-3β, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 576: 923-933, 2006.
30. Li YP, 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 19: 362-370, 2005.
31. Malm C. Exercise-induced muscle damage and inflammation: fact or fiction? Acta Physiol Scand 171: 233-239, 2001.
32. 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 157: 125-136, 2002.
33. McElhinny AS, Perry CN, Witt CC, Labeit S, Gregorio CC. Muscle-specific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development. J Cell Sci 117: 3175-3188, 2004.
34. McHugh MP. Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13: 88-97, 2003.
35. McHugh MP, Connolly DA, Eston RG, Gleim GW. Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med 27: 157-170, 1999.
36. Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10: 1173-1183, 1996.
37. Miller BF, Olesen JL, Hansen M, Dossing S, Crameri RM, Welling RJ, Langberg H, Flyvbjerg A, Kjaer M, Babraj JA, Smith K, Rennie MJ. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567: 1021-1033, 2005.
38. Moore DR, Phillips SM, Babraj JA, Smith K, Rennie MJ. Myofibrillar and collagen protein synthesis in human skeletal muscle in young men after maximal shortening and lengthening contractions. Am J Physiol Endocrinol Metab 288: E1153-E1159, 2005.
39. Newham DJ, Jones DA, Edwards RH. Large delayed plasma creatine kinase changes after stepping exercise. Muscle Nerve 6: 380-385, 1983.
40. Nosaka K, Sakamoto K, Newton M, Sacco P. How long does the protective effect on eccentric exercise-induced muscle damage last? Med Sci Sports Exerc 33: 1490-1495, 2001.
41. Phillips SM, Parise G, Roy BD, Tipton KD, Wolfe RR, Tamopolsky MA. Resistance-training-induced adaptations in skeletal muscle protein turnover in the fed state. Can J Physiol Pharmacol 80: 1045-1053, 2002.
42. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol Endocrinol Metab 273: E99-E107, 1997.
43. Phillips SM, Tipton KD, Ferrando AA, Wolfe RR. Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Physiol Endocrinol Metab 276: E118-E124, 1999.
44. Sandri M, Carraro U, Podhorska-Okolov M, Rizzi C, Arslan P, Monti D, Franceschi C. Apoptosis, DNA damage and ubiquitin expression in normal and mdx muscle fibers after exercise. FEBS Lett 373: 291-295, 1995.
45. 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 117: 399-412, 2004.
46. Schjerling P. The importance of internal controls in mRNA quantification. J Appl Physiol 90: 401-402, 2001.
47. Solomon V, Goldberg AL. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J Biol Chem 271: 26690-26697, 1996.
48. 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 273: 25216-25222, 1998.
49. Spencer JA, Eliazer S, Ilaria RL Jr, Richardson JA, Olson EN. Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol 150: 771-784, 2000.
50. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403, 2004.
51. Stupka N, Tarnopolsky MA, Yardley NJ, Phillips SM. Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol 91: 1669-1678, 2001.
52. 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 280: 2847-2856, 2005.
53. Vissing K, Andersen JL, Schjerling P. Are exercise-induced genes induced by exercise? FASEB J 19: 94-96, 2005.
54. White JD, Scaffidi A, Davies M, McGeachie J, Rudnicki MA, Grounds MD. Myotube formation is delayed but not prevented in MyoD-deficient skeletal muscle: studies in regenerating whole muscle grafts of adult mice. J Histochem Cytochem 48: 1531-1544, 2000.
55. Willoughby DS, Taylor M, Taylor L. Glucocorticoid receptor and ubiquitin expression after repeated eccentric exercise. Med Sci Sports Exerc 35: 2023-2031, 2003.
56. Witt SH, Granzier H, Witt CC, Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 350: 713-722, 2005.
57. Workeneh BT, Rondon-Berrios H, Zhang L, Hu Z, Ayehu G, Ferrando A, Kopple JD, Wang H, Storer T, Fournier M, Lee SW, Du J, Mitch WE. Development of a diagnostic method for detecting increased muscle protein degradation in patients with catabolic conditions. J Am Soc Nephrol 17: 3233-3239, 2006.
58. Yang Y, Jemiolo B, Trappe S. Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers. J Appl Physiol 101: 1442-1450, 2006.