Molecular regulation of skeletal muscle mass

Clinical and Experimental Pharmacology and Physiology

Volumn 37, Issue 3, 2010, Pages 378-384

  Russell, Aaron P ^a  

^a DEAKIN UNIVERSITY   (Australia)

Author keywords

Atrogin 1; Exercise; Muscle hypertrophy; Peroxisome proliferator activated receptor coactivator 1 (PGC 1 ); Striated activator of Rho signalling (STARS)

Indexed keywords

ATROGIN 1; MUSCLE RING FINGER 1 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE B; STRIATED ACTIVATOR OF RHO SIGNALLING; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AGING; CHRONIC DISEASE; CONFERENCE PAPER; ENZYME ACTIVATION; ENZYME ACTIVITY; EXERCISE; HUMAN; METABOLIC REGULATION; MUSCLE ATROPHY; MUSCLE HYPERTROPHY; MUSCLE MASS; NEUROMUSCULAR DISEASE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; EXERCISE; HEAT-SHOCK PROTEINS; HUMANS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 77649133891     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2009.05265.x     Document Type: Conference Paper

References (79)

1. Fry AC. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med. 2004 34 : 663 679.
2. Hjeltnes N, Galuska D, Bjornholm M et al. Exercise-induced overexpression of key regulatory proteins involved in glucose uptake and metabolism in tetraplegic persons: Molecular mechanism for improved glucose homeostasis. FASEB J. 1998 12 : 1701 1712.
3. Lynch GS. Therapies for improving muscle function in neuromuscular disorders. Exerc. Sport Sci. Rev. 2001 29 : 141 148.
4. Tisdale MJ. Cancer cachexia. Langenbecks Arch. Surg. 2004 389 : 299 305.
5. Jagoe RT, Goldberg AL. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr. Opin. Clin. Nutr. Metab. Care 2001 4 : 183 190.
6. Di Giovanni S, Molon A, Broccolini A et al. Constitutive activation of MAPK cascade in acute quadriplegic myopathy. Ann. Neurol. 2004 55 : 195 206.
7. Doucet M, Russell AP, Léger B et al. Muscle atrophy and hypertrophy signalling in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2007 176 : 261 269.
8. Bodine SC, Stitt TN, Gonzalez M et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001 3 : 1014 1019.
9. Stitt TN, Drujan D, Clarke BA et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 2004 14 : 395 403.
10. Rhoads RE. Signal transduction pathways that regulate eukaryotic protein synthesis. J. Biol. Chem. 1999 274 : 30337 30340.
11. Terada N, Patel HR, Takase K, Kohno K, Nairn AC, Gelfand EW. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl Acad. Sci. USA 1994 91 : 11477 11481.
12. Léger B, Cartoni R, Praz M et al. Akt signalling through GSK-3β, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 2006 576 : 923 933.
13. Léger B, Vergani L, Soraru G et al. Human skeletal muscle atrophy in amyotrophic lateral sclerosis reveals a reduction in Akt and an increase in atrogin-1. FASEB J. 2006 20 : 583 585.
14. Crossland H, Constantin-Teodosiu D, Gardiner SM, Constantin D, Greenhaff PL. A potential role for Akt/FOXO signalling in both protein loss and the impairment of muscle carbohydrate oxidation during sepsis in rodent skeletal muscle. J. Physiol. 2008 586 : 5589 5600.
15. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc. Natl Acad. Sci. USA 2002 99 : 9213 9218.
16. Hanai JI, Cao P, Tanksale P et al. The muscle-specific ubiquitin ligase atrogin-1/MAFbx mediates statin-induced muscle toxicity. J. Clin. Invest. 2007 117 : 3940 3951.
17. Sandri M, Sandri C, Gilbert A et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004 117 : 399 412.
18. Léger B, Derave W, De Bock K, Hespel P, Russell AP. Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res. 2008 11 : 163 75B.
19. Blaauw B, Mammucari C, Toniolo L et al. Akt activation prevents the force drop induced by eccentric contractions in dystrophin-deficient skeletal muscle. Hum. Mol. Genet. 2008 17 : 3686 3696.
20. Peter AK, Ko CY, Kim MH et al. Myogenic Akt signaling upregulates the utrophin-glycoprotein complex and promotes sarcolemma stability in muscular dystrophy. Hum. Mol. Genet. 2009 18 : 318 327.
21. Li YP, Chen Y, John J et al. TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 2005 19 : 362 370.
22. Mitch WE, Hu Z, Lee SW, Du J. Strategies for suppressing muscle atrophy in chronic kidney disease: Mechanisms activating distinct proteolytic systems. J. Ren. Nutr. 2005 15 : 23 7.
23. Yu Z, Li P, Zhang M, Hannink M, Stamler JS, Yan Z. Fiber type-specific nitric oxide protects oxidative myofibers against cachectic stimuli. PLoS ONE 2008 3 : e2086.
24. Cai D, Frantz JD, Tawa NE et al. IKKβ/NF-κB activation causes severe muscle wasting in mice. Cell 2004 119 : 285 298.
25. Sandri M, Lin J, Handschin C et al. PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl Acad. Sci. USA 2006 103 : 16260 16265.
26. Moylan JS, Smith JD, Chambers MA, McLoughlin TJ, Reid MB. TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am. J. Physiol. Cell Physiol. 2008 295 : C986 93.
27. 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 2001 98 : 14440 14445.
28. Larsen AE, Tunstall RJ, Carey KA et al. Actions of short-term fasting on human skeletal muscle myogenic and atrogenic gene expression. Ann. Nutr. Metab. 2006 50 : 476 481.
29. Drummond MJ, Glynn EL, Lujan HL, Dicarlo SE, Rasmussen BB. Gene and protein expression associated with protein synthesis and breakdown in paraplegic skeletal muscle. Muscle Nerve 2008 37 : 505 513.
30. Urso ML, Chen YW, Scrimgeour AG, Lee PC, Lee KF, Clarkson PM. Alterations in mRNA expression and protein products following spinal cord injury in humans. J. Physiol. 2007 579 : 877 892.
31. Léger B, Senese R, Al-Khodairy A et al. Atrogin-1, MuRF1 and FoXO, as well as phosphorylated GSK-3β and 4E-BP1 are reduced in skeletal muscle of chronic spinal cord injured patients. Muscle Nerve 2009 40 : 67 78.
32. Clavel S, Coldefy AS, Kurkdjian E, Salles J, Margaritis I, Derijard B. Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat tibialis anterior muscle. Mech. Ageing Dev. 2006 127 : 794 801.
33. 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. 2004 18 : 1025 1027.
34. Louis E, Raue U, Yang Y, Jemiolo B, Trappe S. Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 2007 103 : 1744 1751.
35. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Proteolytic gene expression differs at rest and after resistance exercise between young and old women. J. Gerontol. A Biol. Sci. Med. Sci. 2007 62 : 1407 1412.
36. Harber MP, Crane JD, Dickinson JM et al. Protein synthesis and the expression of growth-related genes are altered by running in human vastus lateralis and soleus muscles. Am. J. Physiol. Regul. Intergr. Comp. Physiol. 2009 296 : R708 14.
37. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am. J. Physiol. 1997 273 : E99 107.
38. Yang Y, Jemiolo B, Trappe S. Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers. J. Appl. Physiol. 2006 101 : 1442 1450.
39. Deldicque L, Theisen D, Bertrand L, Hespel P, Hue L, Francaux M. Creatine enhances differentiation of myogenic C2C12 cells by activating both p38 and Akt/PKB pathways. Am. J. Physiol. Cell Physiol. 2007 293 : C1263 71.
40. 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. 2006 290 : E849 55.
41. Nedergaard A, Vissing K, Overgaard K, Kjaer M, Schjerling P. Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise. Effect of different loading patterns and repeated exercise bouts. J. Appl. Physiol. 2007 103 : 1513 1522.
42. Kostek MC, Chen YW, Cuthbertson DJ et al. Gene expression responses over 24 h to lengthening and shortening contractions in human muscle. Major changes in CSRP3, MUSTN1, SIX1, and FBXO32. Physiol. Genomics 2007 31 : 42 52.
43. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998 92 : 829 839.
44. Finck BN, Kelly DP. PGC-1 coactivators: Inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006 116 : 615 622.
45. Knutti D, Kralli A. PGC-1, a versatile coactivator. Trends Endocrinol. Metab. 2001 12 : 360 365.
46. Russell AP. PGC-1α and exercise: Important partners in combating insulin resistance. Curr. Diabetes Rev. 2005 1 : 175 184.
47. Schreiber SN, Emter R, Hock MB et al. The estrogen-related receptor α (ERRα) functions in PPARγ coactivator 1α (PGC-1α)-induced mitochondrial biogenesis. Proc. Natl Acad. Sci. USA 2004 101 : 6472 6477.
48. Cartoni R, Léger B, Hock MB et al. Mitofusins 1/2 and ERRa expression are increased in human skeletal muscle after physical exercise. J. Physiol. 2005 567 : 349 358.
49. Lin J, Wu H, Tarr PT et al. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 2002 418 : 797 801.
50. Michael LF, Wu Z, Cheatham RB et al. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl Acad. Sci. USA 2001 98 : 3820 3825.
51. Patti ME, Butte AJ, Crunkhorn S et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl Acad. Sci. USA 2003 100 : 8466 8471.
52. Russell AP, Hesselink MK, Lo SK, Schrauwen P. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 2005 19 : 986 988.
53. Russell AP, Feilchenfeldt J, Schreiber S et al. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-γ coactivator-1 and peroxisome proliferator-activated receptor-α in skeletal muscle. Diabetes 2003 52 : 2874 2881.
54. Terada S, Tabata I. Effects of acute bouts of running and swimming exercise on PGC-1α protein expression in rat epitrochlearis and soleus muscle. Am. J. Physiol. Endocrinol. Metab. 2004 286 : E208 16.
55. Vescovo G, Ravara B, Gobbo V, Angelini A, Dalla Libera L. Skeletal muscle fibres synthesis in heart failure. Role of PGC-1α, calcineurin and GH. Int. J. Cardiol. 2005 104 : 298 306.
56. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J. Physiol. 2003 551 : 491 501.
57. Remels AH, Schrauwen P, Broekhuizen R et al. Peroxisome proliferator-activated receptor expression is reduced in skeletal muscle in COPD. Eur. Respir. J. 2007 30 : 245 252.
58. Gastaldi G, Russell A, Golay A et al. Upregulation of peroxisome proliferator-activated receptor γ coactivator gene (PGC1A) during weight loss is related to insulin sensitivity but not to energy expenditure. Diabetologia 2007 50 : 2348 2355.
59. Ling C, Poulsen P, Carlsson E et al. Multiple environmental and genetic factors influence skeletal muscle PGC-1α and PGC-1β gene expression in twins. J. Clin. Invest. 2004 114 : 1518 1526.
60. Zhao J, Brault JJ, Schild A et al. FoxO3 coordinately activates protein degradation by thenautophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007 6 : 472 483.
61. Miura S, Tomitsuka E, Kamei Y et al. Overexpression of peroxisome proliferator-activated receptor γ co-activator-1α leads to muscle atrophy with depletion of ATP. Am. J. Pathol. 2006 169 : 1129 1139.
62. Wallace DC. Mitochondrial diseases in man and mouse. Science 1999 283 : 1482 1488.
63. Arai A, Spencer JA, Olson EN. STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J. Biol. Chem. 2002 277 : 24453 24459.
64. Mahadeva H, Brooks G, Lodwick D, Chong NW, Samani NJ. ms1, a novel stress-responsive, muscle-specific gene that is up-regulated in the early stages of pressure overload-induced left ventricular hypertrophy. FEBS Lett. 2002 521 : 100 104.
65. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 1999 98 : 159 169.
66. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003 113 : 329 342.
67. Kuwahara K, Teg Pipes GC, McAnally J et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J. Clin. Invest. 2007 117 : 1324 1334.
68. Ounzain S, Dacwag CS, Samani NJ, Imbalzano AN, Chong NW. Comparative in silico analysis identifies bona fide MyoD binding sites within the myocyte stress 1 gene promoter. BMC Mol. Biol. 2008 9 : 50.
69. Xu Q, Wu Z. The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J. Biol. Chem. 2000 275 : 36750 36757.
70. Guerfali I, Manissolle C, Durieux AC, Bonnefoy R, Bartegi A, Freyssenet D. Calcineurin A and CaMKIV transactivate PGC-1α promoter, but differentially regulate cytochrome c promoter in rat skeletal muscle. Pflügers Arch. 2007 454 : 297 305.
71. McClung JM, Thompson RW, Lowe LL, Carson JA. RhoA expression during recovery from skeletal muscle disuse. J. Appl. Physiol. 2004 96 : 1341 1348.
72. Fluck M, Carson JA, Schwartz RJ, Booth FW. SRF protein is upregulated during stretch-induced hypertrophy of rooster ALD muscle. J. Appl. Physiol. 1999 86 : 1793 1799.
73. Sakuma K, Nishikawa J, Nakao R, Nakano H, Sano M, Yasuhara M. Serum response factor plays an important role in the mechanically overloaded plantaris muscle of rats. Histochem. Cell Biol. 2003 119 : 149 160.
74. Li S, Czubryt MP, McAnally J et al. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc. Natl Acad. Sci. USA 2005 102 : 1082 1087.
75. Lamon S, Wallace MA, Léger B, Russell AP. Regulation of STARS and its downstream targets suggest a novel pathway involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 2009 587 : 1795 1803.
76. Carson JA, Schwartz RJ, Booth FW. SRF and TEF-1 control of chicken skeletal α-actin gene during slow-muscle hypertrophy. Am. J. Physiol. 1996 270 : C1624 33.
77. Allen DL, Sartorius CA, Sycuro LK, Leinwand LA. Different pathways regulate expression of the skeletal myosin heavy chain genes. J. Biol. Chem. 2001 276 : 43524 43533.
78. Charvet C, Houbron C, Parlakian A et al. New role for serum response factor in postnatal skeletal muscle growth and regeneration via the interleukin 4 and insulin-like growth factor 1 pathways. Mol. Cell. Biol. 2006 26 : 6664 6674.
79. Sakuma K, Akiho M, Nakashima H, Akima H, Yasuhara M. Age-related reductions in expression of serum response factor and myocardin-related transcription factor A in mouse skeletal muscles. Biochim. Biophys. Acta 2008 1782 : 453 461.