Changes in muscle mass with mechanical load: Possible cellular mechanisms

Applied Physiology, Nutrition and Metabolism

Volumn 34, Issue 3, 2009, Pages 328-335

  Spangenburg, Espen E ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Akt PKB; Hypertrophy; Insulin like growth factor; mTOR; Overload; Stretch

Indexed keywords

ADAPTATION; ANIMAL; BIOMECHANICS; CYTOLOGY; GENE EXPRESSION REGULATION; HUMAN; PHYSIOLOGY; RAT; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMECHANICS; GENE EXPRESSION REGULATION; HUMANS; MUSCLE, SKELETAL; RATS; SIGNAL TRANSDUCTION;

EID: 67651227757     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H09-010     Document Type: Review

References (64)

1. Adams, G.R. 2002. Invited Review: Autocrine/paracrine IGF-I and skeletal muscle adaptation. J. Appl. Physiol. 93: 1159-1167. PMID:12183514.
2. Adams, G.R., and Haddad, F. 1996. The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J. Appl. Physiol. 81: 2509-2516. PMID: 9018499.
3. Adams, G.R., and McCue, S.A. 1998. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J. Appl. Physiol. 84: 1716-1722. PMID:9572822.
4. Adams, G.R., Haddad, F., and Baldwin, K.M. 1999. Time course of changes in markers of myogenesis in overloaded rat skeletal muscles. J. Appl. Physiol. 87: 1705-1712. PMID:10562612.
5. Baar, K., and Esser, K. 1999. Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 276: C120-C127. PMID:9886927.
6. Baar, K., Nader, G., and Bodine, S. 2006. Resistance exercise, muscle loading/unloading and the control of muscle mass. Essays Biochem. 42: 61-74. doi:10.1042/bse0420061. PMID: 17144880.
7. Barton, E.R. 2006. Viral expression of insulin-like growth factor-I isoforms promotes different responses in skeletal muscle. J. Appl. Physiol. 100: 1778-1784. doi:10.1152/japplphysiol.01405. 2005. PMID:16439513.
8. Bassel-Duby, R., and Olson, E.N. 2006. Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 75: 19-37. doi:10.1146/annurev.biochem.75.103004.142622. PMID:16756483.
9. Bentzinger, C.F., Romanino, K., Cloetta, D., Lin, S., Mascarenhas, J.B., Oliveri, F., et al. 2008. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab. 8: 411-424. doi:10.1016/j.cmet. 2008.10.002. PMID:19046572.
10. Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., et al. 2001. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3: 1014-1019. doi:10.1038/ ncb1101-1014. PMID:11715023.
11. Burridge, K., and Chrzanowska-Wodnicka, M. 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12: 463-518. doi:10.1146/annurev.cellbio.12.1.463. PMID:8970735.
12. Burry, M., Hawkins, D., and Spangenburg, E.E. 2007. Lengthening contractions differentially affect p70s6k phosphorylation compared to isometric contractions in rat skeletal muscle. Eur. J. Appl. Physiol. 100: 409-415. doi:10.1007/s00421-007-0444-5. PMID:17401575.
13. Butterfield, T.A., and Best, T.M. 2009. Stretch-activated ion channel blockade attenuates adaptations to eccentric exercise. Med. Sci. Sports Exerc. 41: 351-356. PMID:19127190.
14. Carson, J.A. 1997. The regulation of gene expression in hypertrophying skeletal muscle. Exerc. Sport Sci. Rev. 25: 301-320. doi:10.1249/00003677-199700250-00013. PMID:9213096.
15. Carson, J.A., and Wei, L. 2000. Integrin signaling's potential for mediating gene expression in hypertrophying skeletal muscle. J. Appl. Physiol. 88: 337-343. PMID:10642399.
16. Carson, J.A., Schwartz, R.J., and Booth, F.W. 1996. SRF and TEF-1 control of chicken skeletal alpha-actin gene during slow-muscle hypertrophy. Am. J. Physiol. 270: C1624-C1633. PMID: 8764144.
17. Chan, A.Y., and Dyck, J.R. 2005. Activation of AMP-activated protein kinase (AMPK) inhibits protein synthesis: a potential strategy to prevent the development of cardiac hypertrophy. Can. J. Physiol. Pharmacol. 83: 24-28. doi:10.1139/y04-107. PMID:15759047.
18. Chesley, A., MacDougall, J.D., Tarnopolsky, M.A., Atkinson, S.A., and Smith, K. 1992. Changes in human muscle protein synthesis after resistance exercise. J. Appl. Physiol. 73: 1383-1388. PMID:1280254.
19. DeVol, D.L., Rotwein, P., Sadow, J.L., Novakofski, J., and Bechtel, P.J. 1990. Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am. J. Physiol. 259: E89-E95. PMID:2372054.
20. Drummond, M.J., Miyazaki, M., Dreyer, H.C., Pennings, B., Dhanani, S., Volpi, E., Esser, K.A., Rasmussen, B.B. 2008. Expression of growth-related genes in young and old human skeletal muscle following an acute stimulation of protein synthesis. J. Appl. Physiol. [Epub ahead of print]. PMID:18787087.
21. Fluck, M., Carson, J.A., Gordon, S.E., Ziemiecki, A., and Booth, F.W. 1999a. Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am. J. Physiol. 277: C152-C162. PMID:10409118.
22. Fluck, M., Carson, J.A., Schwartz, R.J., and Booth, F.W. 1999b. SRF protein is upregulated during stretch-induced hypertrophy of rooster ALD muscle. J. Appl. Physiol. 86: 1793-1799. PMID:10368339.
23. Franco, A., Jr., and Lansman, J.B. 1990a. Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature, 344: 670-673. doi:10.1038/344670a0. PMID:1691450.
24. Franco, A., Jr., and Lansman, J.B. 1990b. Stretch-sensitive channels in developing muscle cells from a mouse cell line. J. Physiol. 427: 361-380. PMID:2170636.
25. Gan, B., Yoo, Y., and Guan, J.L. 2006. Association of focal adhesion kinase with tuberous sclerosis complex 2 in the regulation of s6 kinase activation and cell growth. J. Biol. Chem. 281: 37321-37329. doi:10.1074/jbc.M605241200. PMID:17043358.
26. Glass, D.J. 2005. Skeletal muscle hypertrophy and atrophy signaling pathways. Int. J. Biochem. Cell Biol. 37: 1974-1984. PMID:16087388.
27. Goldberg, A.L. 1967. Work-induced growth of skeletal muscle in normal and hypophysectomized rats. Am. J. Physiol. 213: 1193-1198. PMID:6054866.
28. Goldspink, G., Wessner, B., and Bachl, N. 2008. Growth factors, muscle function and doping. Curr. Opin. Pharmacol. 8: 352-357. doi:10.1016/j.coph.2008.02.002. PMID:18353722.
29. Gordon, S.E., Fluck, M., and Booth, F.W. 2001. Selected contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J. Appl. Physiol. 90: 1174-1183. [Discussion 1165.] PMID:11181634.
30. Gordon, S.E., Lake, J.A., Westerkamp, C.M., and Thomson, D.M. 2008. Does AMP-activated protein kinase negatively mediate aged fast-twitch skeletal muscle mass? Exerc. Sport Sci. Rev. 36: 179-186. doi:10.1097/JES.0b013e3181877e13. PMID: 18815486.
31. Gulati, P., Gaspers, L.D., Dann, S.G., Joaquin, M., Nobukuni, T., Natt, F., et al. 2008. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab. 7: 456-465. doi:10.1016/j.cmet.2008.03.002. PMID:18460336.
32. Hawke, T.J., and Garry, D.J. 2001. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91: 534-551. PMID:11457764.
33. Hornberger, T.A., Armstrong, D.D., Koh, T.J., Burkholder, T.J., and Esser, K.A. 2005. Intracellular signaling specificity in response to uniaxial vs. multiaxial stretch: implications for mechanotransduction. Am. J. Physiol. Cell Physiol. 288: C185-C194. PMID:15371259.
34. Hornberger, T.A., Chu, W.K., Mak, Y.W., Hsiung, J.W., Huang, S.A., and Chien, S. 2006. The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 103: 4741-4746. doi:10.1073/pnas.0600678103. PMID:16537399.
35. Hornberger, T.A., Sukhija, K.B., Wang, X.R., and Chien, S. 2007. mTOR is the rapamycin-sensitive kinase that confers mechanically-induced phosphorylation of the hydrophobic motif site Thr(389) in p70(S6k). FEBS Lett. 581: 4562-4566. doi:10. 1016/j.febslet.2007.08.045. PMID:17825298.
36. Janssen, I., Baumgartner, R.N., Ross, R., Rosenberg, I.H., and Roubenoff, R. 2004. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am. J. Epidemiol. 159: 413-421. doi:10.1093/aje/kwh058. PMID: 14769646.
37. Kurek, J., Bower, J., Romanella, M., and Austin, L. 1996. Leukaemia inhibitory factor treatment stimulates muscle regeneration in the mdx mouse. Neurosci. Lett. 212: 167-170. doi:10.1016/ 0304-3940(96)12802-0. PMID:8843099.
38. Lorenz, M.C., and Heitman, J. 1995. TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J. Biol. Chem. 270: 27531-27537. doi:10.1074/jbc.270. 10.5483. PMID:7499212.
39. Mackenzie, M.G., Hamilton, D.L., Murray, J.T., Taylor, P.M., and Baar, K. 2009. mVps34 is activated following high-resistance contractions. J. Physiol. 587: 253-260. doi:10.1113/jphysiol. 2008.159830. PMID:19015198.
40. McGee, S.L., Mustard, K.J., Hardie, D.G., and Baar, K. 2008. Normal hypertrophy accompanied by phosphoryation and activation of AMP-activated protein kinase alpha1 following overload in LKB1 knockout mice. J. Physiol. 586: 1731-1741. doi:10.1113/ jphysiol.2007.143685. PMID:18202101.
41. Miyazaki, M., and Esser, K.A. 2008. Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. J. Appl. Physiol. [Epub ahead of print.] PMID:11299288.
42. Miyazaki, M., and Esser, K.A. 2009. REDD2 is enriched in skeletal muscle and inhibits mTOR signaling in response to leucine and stretch. Am. J. Physiol. Cell. Physiol. [Epub ahead of print.] PMID:11299288.
43. Nader, G.A., and Esser, K.A. 2001. Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J. Appl. Physiol. 90: 1936-1942. PMID:11299288.
44. O'Connor, R.S., Pavlath, G.K., McCarthy, J.J., and Esser, K.A. 2007. Last Word on Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J. Appl. Physiol. 103: 1107. doi:10.1152/japplphysiol.00502.2007. PMID: 17724310.
45. Oh, H., Fujio, Y., Kunisada, K., Hirota, H., Matsui, H., Kishimoto, T., and Yamauchi-Takihara, K. 1998. Activation of phosphatidylinositol 3-kinase through glycoprotein 130 induces protein kinase B and p70 S6 kinase phosphorylation in cardiac myocytes. J. Biol. Chem. 273: 9703-9710. doi:10.1074/jbc.273.16.9703. PMID:9545305.
46. Ohanna, M., Sobering, A.K., Lapointe, T., Lorenzo, L., Praud, C., Petroulakis, E., et al. 2005. Atrophy of S6K1-/- skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat. Cell Biol. 7: 286-294. doi:10.1038/ncb1231. PMID: 15723049.
47. Peterson, R.T., Beal, P.A., Comb, M.J., and Schreiber, S.L. 2000. FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J. Biol. Chem. 275: 7416-7423. doi:10.1074/jbc.275.10.7416. PMID:10702316.
48. Rennie, M.J., Wackerhage, H., Spangenburg, E.E., and Booth, F.W. 2004. Control of the size of the human muscle mass. Annu. Rev. Physiol. 66: 799-828. doi:10.1146/annurev.physiol.66.052102. 134444. PMID:14977422.
49. Reynolds, T.H. 4th., Bodine, S.C., Lawrence, J.C. Jr. 2002. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J. Biol. Chem. 277: 17657-17662. doi:10.1074/jbc.M201142200. PMID:11884412.
50. Sakuma, K., Watanabe, K., Sano, M., Uramoto, I., and Totsuka, T. 2000. Differential adaptation of growth and differentiation factor 8/myostatin, fibroblast growth factor 6 and leukemia inhibitory factor in overloaded, regenerating and denervated rat muscles. Biochim. Biophys. Acta, 1497: 77-88. doi:10.1016/S0167-4889(00)00044-6. PMID:10838161.
51. Sancak, Y., Thoreen, C.C., Peterson, T.R., Lindquist, R.A., Kang, S.A., Spooner, E., et al. 2007. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol. Cell, 25: 903-915. doi:10.1016/j.molcel.2007.03.003. PMID:17386266.
52. Spangenburg, E.E., and Booth, F.W. 2002. Multiple signaling pathways mediate LIF-induced skeletal muscle satellite cell proliferation. Am. J. Physiol. Cell Physiol. 283: C204-C211. PMID: 12055089.
53. Spangenburg, E.E., and Booth, F.W. 2006. Leukemia inhibitory factor restores the hypertrophic response to increased loading in the LIF(-/-) mouse. Cytokine, 34: 125-130. doi:10.1016/j.cyto. 2006.05.001. PMID:16781162.
54. Spangenburg, E.E., and McBride, T.A. 2006. Inhibition of stretch-activated channels during eccentric muscle contraction attenuates p70S6K activation. J. Appl. Physiol. 100: 129-135. doi:10. 1152/japplphysiol.00619.2005. PMID:16179399.
55. Spangenburg, E.E., Le Roith, D., Ward, C.W., and Bodine, S.C. 2008. A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy. J. Physiol. 586: 283-291. doi:10.1113/jphysiol.2007.141507. PMID:17974583.
56. Thomson, D.M., and Gordon, S.E. 2005. Diminished overload-induced hypertrophy in aged fast-twitch skeletal muscle is associated with AMPK hyperphosphorylation. J. Appl. Physiol. 98: 557-564. doi:10.1152/japplphysiol.00811.2004. PMID: 15465886.
57. Thomson, D.M., Fick, C.A., and Gordon, S.E. 2008. AMPK activation attenuates S6K1, 4E-BP1, and eEF2 signaling responses to high-frequency electrically stimulated skeletal muscle contractions. J. Appl. Physiol. 104: 625-632. doi:10.1152/japplphysiol. 00915.2007. PMID:18187610.
58. Vyas, D.R., Spangenburg, E.E., Abraha, T.W., Childs, T.E., and Booth, F.W. 2002. GSK-3beta negatively regulates skeletal myotube hypertrophy. Am. J. Physiol. Cell Physiol. 283: C545-C551. PMID:12107064.
59. Wan, M., Wu, X., Guan, K.L., Han, M., Zhuang, Y., and Xu, T. 2006. Muscle atrophy in transgenic mice expressing a human TSC1 transgene. FEBS Lett. 580: 5621-5627. doi:10.1016/j. febslet.2006.09.008. PMID:16996505.
60. Wong, T.S., and Booth, F.W. 1988. Skeletal muscle enlargement with weight-lifting exercise by rats. J. Appl. Physiol. 65: 950-954. PMID:2459101.
61. Wong, T.S., and Booth, F.W. 1990a. Protein metabolism in rat gastrocnemius muscle after stimulated chronic concentric exercise. J. Appl. Physiol. 69: 1709-1717. PMID:1703145.
62. Wong, T.S., and Booth, F.W. 1990b. Protein metabolism in rat tibialis anterior muscle after stimulated chronic eccentric exercise. J. Appl. Physiol. 69: 1718-1724. PMID:1703146.
63. Xia, H., Nho, R.S., Kahm, J., Kleidon, J., and Henke, C.A. 2004. Focal adhesion kinase is upstream of phosphatidylinositol 3-kinase/Akt in regulating fibroblast survival in response to contraction of type I collagen matrices via a beta 1 integrin viability signaling pathway. J. Biol. Chem. 279: 33024-33034. doi:10. 1074/jbc.M313265200. PMID:15166238.
64. Yeung, E.W., Whitehead, N.P., Suchyna, T.M., Gottlieb, P.A., Sachs, F., and Allen, D.G. 2005. Effects of stretch-activated channel blockers on (Ca2+)i and muscle damage in the mdx mouse. J. Physiol. 562: 367-380. doi:10.1113/jphysiol.2004.075275. PMID:15528244.