Rat hindlimb unloading down-regulates insulin like growth factor-1 signaling and AMP-activated protein kinase, and leads to severe atrophy of the soleus muscle

Applied Physiology, Nutrition and Metabolism

Volumn 32, Issue 6, 2007, Pages 1115-1123

  Han, Bing ^a,b   Zhu, Mei J ^b   Ma, Changwei ^a   Du, Min ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF WYOMING   (United States)

Author keywords

AMP activated protein kinase; Hindlimb unloading; Insulin like growth factor 1; Muscle atrophy; Rat

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; AMP ACTIVATED PROTEIN KINASES; AMP-ACTIVATED PROTEIN KINASES; INSULIN RECEPTOR SUBSTRATE 1 PROTEIN; INSULIN RECEPTOR SUBSTRATE-1 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MULTIENZYME COMPLEX; ONCOPROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SERINE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; ATROPHY; GENETICS; IMMOBILIZATION; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ACETYL-COA CARBOXYLASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ATROPHY; BLOTTING, WESTERN; HINDLIMB SUSPENSION; INSULIN-LIKE GROWTH FACTOR I; MALE; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; ONCOGENE PROTEIN V-AKT; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; SERINE; SIGNAL TRANSDUCTION;

EID: 39049169099     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H07-102     Document Type: Article

References (73)

1. Adams, G.R., Caiozzo, V.J., and Baldwin, K.M. 2003. Skeletal muscle unweighting: spaceflight and ground-based models. J. Appl. Physiol. 95: 2185-2201.
2. Allen, D.L., Linderman, J.K., Roy, R.R., Grindeland, R.E., Mukku, V., and Edgerton, V.R. 1997. Growth hormone/IGF-I and/or resistive exercise maintains myonuclear number in hindlimb unweighted muscles. J. Appl. Physiol. 83: 1857-1861.
3. Anthony, J.C., Anthony, T.G., Kimball, S.R., and Jefferson, L.S. 2001. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131: 856S-860S.
4. Armstrong, R.B., and Phelps, R.O. 1984. Muscle fiber type composition of the rat hindlimb. Am. J. Anat. 171: 259-272. doi:10. 1002/aja.1001710303.
5. Baldwin, K.M., Herrick, R.E., and McCue, S.A. 1993. Substrate oxidation capacity in rodent skeletal muscle: effects of exposure to zero gravity. J. Appl. Physiol. 75: 2466-2470.
6. Bigbee, A.J., Grindeland, R.E., Roy, R.R., Zhong, H., Gosselink, K.L., Arnaud, S., and Edgerton, V.R. 2006. Basal and evoked levels of bioassayable growth hormone are altered by hindlimb unloading. J. Appl. Physiol. 100: 1037-1042. doi:10.1152/japplphysiol.00615.2005.
7. Bikle, D.D., Harris, J., Halloran, B.P., and Morey-Holton, E.R. 1994. Skeletal unloading induces resistance to insulin-like growth factor I. J. Bone Miner. Res. 9: 1789-1796.
8. Blanc, S., Normand, S., Pachiaudi, C., Fortrat, J.O., Laville, M., and Gharib, C. 2000. Fuel homeostasis during physical inactivity induced by bed rest. J. Clin. Endocrinol. Metab. 85: 2223-2233. doi:10.1210/jc.85.6. 2223.
9. Bodine, S.C., Latres, E., Baumhueter, S., Lai, V.K., Nunez, L., Clarke, B.A., et al. 2001a. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science, 294: 1704-1708. doi:10.1126/science. 1065874.
10. Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., et al. 2001b. 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.
11. Bolster, D.R., Kubica, N., Crozier, S.J., Williamson, D.L., Farrell, P.A., Kimball, S.R., and Jefferson, L.S. 2003. Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J. Physiol. 553: 213-220. doi:10.1113/jphysiol.2003.047019.
12. Bush, J.A., Kimball, S.R., O'Connor, P.M., Suryawan, A., Orellana, R.A., Nguyen, H.V., et al. 2003. Translational control of protein synthesis in muscle and liver of growth hormone-treated pigs. Endocrinology, 144: 1273-1283. doi:10.1210/en.2002-220983.
13. Cheng, S.W., Fryer, L.G., Carling, D., and Shepherd, P.R. 2004. Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J. Biol. Chem. 279: 15719-15722. doi:10.1074/jbc. C300534200.
14. Chiang, G.G., and Abraham, R.T. 2005. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J. Biol. Chem. 280: 25485-25490. doi:10.1074/jbc.M501707200.
15. Cross, D.A., Alessi, D.R., Cohen, P., Andjelkovich, M., and Hemmings, B.A. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 378: 785-789. doi:10.1038/378785a0.
16. De-Doncker, L., Kasri, M., Picquet, F., and Falempin, M. 2005. Physiologically adaptive changes of the L5 afferent neurogram and of the rat soleus EMG activity during 14 days of hindlimb unloading and recovery. J. Exp. Biol. 208: 4585-4592. doi:10.1242/jeb.01931.
17. Du, M., Zhu, M.J., Means, W.J., Hess, B.W., and Ford, S.P. 2004. Effect of nutrient restriction on calpain and calpastatin content of skeletal muscle from cows and fetuses. J. Anim. Sci. 82: 2541-2547.
18. Edgerton, V.R., Zhou, M.Y., Ohira, Y., Klitgaard, H., Jiang, B., Bell, G., et al. 1995. Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J. Appl. Physiol. 78: 1733-1739.
19. Fitts, R.H., Riley, D.R., and Widrick, J.J. 2000. Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J. Appl. Physiol. 89: 823-839.
20. Fitts, R.H., Riley, D.R., and Widrick, J.J. 2001. Functional and structural adaptations of skeletal muscle to microgravity. J. Exp. Biol. 204: 3201-3208.
21. Frost, R.A., Nystrom, G.J., Jefferson, L.S., and Lang, C.H. 2006. Hormone, cytokine, and nutritional regulation of sepsis-induced increases in atrogin-1 and MuRF1 in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 292: E501-E512. doi:10.1152/ajpendo.00359.2006.
22. Giger, J.M., Haddad, F., Qin, A.X., Zeng, M., and Baldwin, K.M. 2005. Effect of unloading on type I myosin heavy chain gene regulation in rat soleus muscle. J. Appl. Physiol. 98: 1185-1194. doi:10.1152/japplphysiol.01099. 2004.
23. Greenleaf, J.E., Bulbulian, R., Bernauer, E.M., Haskell, W.L., and Moore, T. 1989. Exercise-training protocols for astronauts in microgravity. J. Appl. Physiol. 67: 2191-2204.
24. Haddad, F., Herrick, R.E., Adams, G.R., and Baldwin, K.M. 1993. Myosin heavy-chain expression in rodent skeletal muscle - effects of exposure to zero-gravity. J. Appl. Physiol. 75: 2471-2477.
25. Haddad, F., Roy, R.R., Zhong, H., Edgerton, V.R., and Baldwin, K.M. 2003. Atrophy responses to muscle inactivity. II. Molecular markers of protein deficits. J. Appl. Physiol. 95: 791-802.
26. Haddad, F., Adams, G.R., Bodell, P.W., and Baldwin, K.M. 2006. Isometric resistance exercise fails to counteract skeletal muscle atrophy processes during the initial stages of unloading. J. Appl. Physiol. 100: 433-441. doi:10.1152/japplphysiol.01203.2005.
27. Hara, K., Maruki, Y., Long, X., Yoshino, K., Oshiro, N., Hidayat, S., et al. 2002. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell, 110: 177-189. doi:10.1016/S0092-8674(02)00833-4.
28. Hardie, D.G. 2004. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med. Sci. Sports Exerc. 36: 28-34. doi:10.1249/01.MSS.0000106171.38299.64.
29. Hardt, S.E., and Sadoshima, J. 2002. Glycogen synthase kinase-3β: a novel regulator of cardiac hypertrophy and development. Circ. Res. 90: 1055-1063. doi:10.1161/01.RES.0000018952.70505.F1.
30. Hawley, S.A., Pan, D.A., Mustard, K.J., Ross, L., Bain, J., Edelman, A.M., et al. 2005. Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2: 9-19. doi:10.1016/j.cmet.2005.05.009.
31. He, J., Watkins, S., and Kelley, D.E. 2001. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes, 50: 817-823. doi:10.2337/diabetes.50.4. 817.
32. Huey, K.A., Roy, R.R., Baldwin, K.M., and Edgerton, V.R. 2001. Temporal effects of inactivty on myosin heavy chain gene expression in rat slow muscle. Muscle Nerve, 24: 517-526. doi:10.1002/mus.1035.
33. Huey, K.A., Roy, R.R., Haddad, F., Edgerton, V.R., and Baldwin, K.M. 2002. Transcriptional regulation of the type I myosin heavy chain promoter in inactive rat soleus. Am. J. Physiol. Cell Physiol. 282: C528-C537.
34. Inoki, K., Zhu, T., and Guan, K.L. 2003.TSC2mediates cellular energy response to control cell growth and survival. Cell, 115: 577-590. doi:10.1016/S0092-8674(03)00929-2.
35. Jakobsen, S.N., Hardie, D.G., Morrice, N., and Tornqvist, H.E. 2001. 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J. Biol. Chem. 276: 46912-46916. doi:10.1074/jbc.C100483200.
36. Khamzina, L., Veilleux, A., Bergeron, S., and Marette, A. 2005. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology, 146: 1473-1481. doi:10.1210/en.2004-0921.
37. Kim, J., Solis, R.S., Arias, E.B., and Cartee, G.D. 2004. Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5′ AMP-activated protein kinase phosphorylation. J. Appl. Physiol. 96: 575-583. doi:10.1152/japplphysiol.00909.2003.
38. Latres, E., Amini, A.R., Amini, A.A., Griffiths, J., Martin, F.J., Wei, Y., et al. 2005. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/ mTOR) pathway. J. Biol. Chem. 280: 2737-2744. doi:10.1074/jbc.M407517200.
39. LeBlanc, A., Lin, C., Shackelford, L., Sinitsyn, V., Evans, H., Belichenko, O., et al. 2000. Muscle volume, MRI relaxation times (T2), and body composition after spaceflight. J. Appl. Physiol. 89: 2158-2164.
40. Mozdziak, P.E., Pulvermacher, P.M., and Schultz, E. 2001. Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading. J. Appl. Physiol. 91: 183-190.
41. Nyholm, B., Qu, Z., Kaal, A., Pedersen, S.B., Gravholt, C.H., Andersen, J.L., et al. 1997. Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes, 46: 1822-1828. doi:10.2337/diabetes.46.11.1822.
42. 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.
43. O'Keefe, M.P., Perez, F.R., Kinnick, T.R., Tischler, M.E., and Henriksen, E.J. 2004a. Development of whole-body and skeletal muscle insulin resistance after one day of hindlimb suspension. Metabolism, 53: 1215-1222. doi:10.1016/j.metabol.2004.02.025.
44. O'Keefe, M.P., Perez, F.R., Sloniger, J.A., Tischler, M.E., and Henriksen, E.J. 2004b. Enhanced insulin action on glucose transport and insulin signaling in 7-day unweighted rat soleus muscle. J. Appl. Physiol. 97: 63-71. doi:10.1152/japplphysiol.01361.2003.
45. Ozes, O.N., Akca, H., Mayo, L.D., Gustin, J.A., Maehama, T., Dixon, J.E., et al. 2001. A phosphatidylinositol 3-kinase/Akt/ mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc. Natl. Acad. Sci. U.S.A. 98: 4640-4645. doi:10.1073/pnas.051042298.
46. Pap, M., and Cooper, G.M. 2002. Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β signaling pathway. Mol. Cell. Biol. 22: 578-586. doi:10.1128/MCB.22.2.578-586.2002.
47. Park, E., and Schultz, E. 1993. A simple hindlimb suspension apparatus. Aviat. Space Environ. Med. 64: 401-404.
48. Park, I.H., Erbay, E., Nuzzi, P., and Chen, J. 2005. Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp. Cell Res. 309: 211-219. doi:10.1016/j.yexcr.2005.05.017.
49. Peraldi, P., and Spiegelman, B. 1998. TNF-α and insulin resistance: summary and future prospects. Mol. Cell. Biochem. 182: 169-175. doi:10.1023/A:1006865715292.
50. Picquet, F., De-Doncker, L., and Falempin, M. 2004. Enhancement of hybrid-fiber types in rat soleus muscle after clenbuterol administration during hindlimb unloading. Can. J. Physiol. Pharmacol. 82: 311-318. doi:10.1139/y04-034.
51. Sacheck, J.M., Ohtsuka, A., McLary, S.C., and Goldberg, A.L. 2004. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am. J. Physiol. Endocrinol. Metab. 287: E591-E601. doi:10.1152/ajpendo.00073.2004.
52. Sakamoto, K., Aschenbach, W.G., Hirshman, M.F., and Goodyear, L.J. 2003. Akt signaling in skeletal muscle: regulation by exercise and passive stretch. Am. J. Physiol. Endocrinol. Metab. 285: E1081-E1088.
53. Sakata, T., Halloran, B.P., Elalieh, H.Z., Munson, S.J., Rudner, L., Venton, L., et al. 2003. Skeletal unloading induces resistance to insulin-like growth factor I on bone formation. Bone, 32: 669-680. doi:10.1016/S8756-3282(03)00088-7.
54. Sakata, T., Wang, Y., Halloran, B.P., Elalieh, H.Z., Cao, J., and Bikle, D.D. 2004. Skeletal unloading induces resistance to insulin-like growth factor-I (IGF-I) by inhibiting activation of the IGF-I signaling pathways. J. Bone Miner. Res. 19: 436-446. doi:10.1359/JBMR.0301241.
55. Sambandam, N., and Lopaschuk, G.D. 2003. AMP-activated protein kinase (AMPK) control of fatty acid and glucose metabolism in the ischemic heart. Prog. Lipid Res. 42: 238-256. doi:10.1016/S0163-7827(02)00065-6.
56. Schmelzle, T., and Hall, M.N. 2000. TOR, a central controller of cell growth. Cell, 103: 253-262. doi:10.1016/S0092-8674(00)00117-3.
57. Schulz, R.A., and Yutzey, K.E. 2004. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev. Biol. 266: 1-16. doi:10.1016/j.ydbio.2003.10.008.
58. Shen, W.H., Boyle, D.W., Wisniowski, P., Bade, A., and Liechty, E.A. 2005. Insulin and IGF-I stimulate the formation of the eukaryotic initiation factor 4F complex and protein synthesis in C2C12 myotubes independent of availability of external amino acids. J. Endocrinol. 185: 275-289. doi:10.1677/joe.1.06080.
59. Song, Y.H., Godard, M., Li, Y., Richmond, S.R., Rosenthal, N., and Delafontaine, P. 2005. Insulin-like growth factor I-mediated skeletal muscle hypertrophy is characterized by increased mTOR-p70S6K signaling without increased Akt phosphorylation. J. Investig. Med. 53: 135-142. doi:10.2310/6650.2005.00309.
60. Steinberg, G.R., Michell, B.J., van Denderen, B.J., Watt, M.J., Carey, A.L., Fam, B.C., et al. 2006. Tumor necrosis factor α-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab. 4: 465-474. doi:10.1016/j.cmet.2006.11.005.
61. Subramaniam, S., Shahani, N., Strelau, J., Laliberte, C., Brandt, R., Kaplan, D., et al. 2005. Insulin-like growth factor 1 inhibits extracellular signal-regulated kinase to promote neuronal survival via the phosphatidylinositol 3-kinase/protein kinase A/c-Raf pathway. J. Neurosci. 25: 2838-2852. doi:10.1523/JNEUROSCI. 5060-04.2005.
62. Suwa, M., Nakano, H., and Kumagai, S. 2003. Effects of chronic AICAR treatment on fiber composition, enzyme activity, UCP3, and PGC-1 in rat muscles. J.Appl.Physiol.95:960-968.
63. Suwa, M., Egashira, T., Nakano, H., Sasaki, H., and Kumagai, S. 2006. Metformin increases the PGC-1α protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo. J. Appl. Physiol. 101: 1685-1692. doi:10.1152/japplphysiol.00255.2006.
64. Talmadge, R.J., Roy, R.R., and Edgerton, V.R. 1996. Distribution of myosin heavy chain isoforms in non-weight-bearing rat soleus muscle fibers. J. Appl. Physiol. 81: 2540-2546.
65. Tobin, B.W., Uchakin, P.N., and Leeper-Woodford, S.K. 2002. Insulin secretion and sensitivity in space flight: diabetogenic effects. Nutrition, 18: 842-848. doi:10.1016/S0899-9007(02)00940-1.
66. Um, S.H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., et al. 2004. Absence of S6K1 protects against age-and diet-induced obesity while enhancing insulin sensitivity. Nature, 431: 200-205. doi:10.1038/nature02866.
67. Vary, T.C. 2006. IGF-I stimulates protein synthesis in skeletal muscle through multiple signaling pathways during sepsis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290: R313-R321.
68. Vary, T.C., Deiter, G., and Kimball, S.R. 2002. Phosphorylation of eukaryotic initiation factor eIF2Bepsilon in skeletal muscle during sepsis. Am. J. Physiol. Endocrinol. Metab. 283: E1032-E1039.
69. Widrick, J.J., Knuth, S.T., Norenberg, K.M., Romatowski, J.G., Bain, J.L., Riley, D.A., et al. 1999. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J. Physiol. 516: 915-930. doi:10.1111/j.1469-7793.1999.0915u.x.
70. 2+/calmodulin-dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2: 21-33. doi:10.1016/j.cmet.2005.06.005.
71. Zhong, S., Lowe, D.A., and Thompson, L.V. 2006. Effects of hindlimb unweighting and aging on rat semimembranosus muscle and myosin. J. Appl. Physiol. 101: 873-880. doi:10.1152/japplphysiol.00526.2005.
72. Zhu, M.J., Ford, S.P., Nathanielsz, P.W., and Du, M. 2004. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol. Reprod. 71: 1968-1973. doi:10.1095/biolreprod.104.034561.
73. Zhu, M.J., Ford, S.P., Means, W.J., Hess, B.W., Nathanielsz, P.W., and Du, M. 2006. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J. Physiol. 575: 241-250. doi:10.1113/jphysiol.2006. 112110.