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Activation of mTOR for the loss of skeletal muscle in a hindlimb-suspended rat model

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Abstract

The hindlimb-suspended or unloading rodent model was developed to mimic the microgravity of a spaceflight environment and has been used extensively to study the physiological responses to various aspects of musculoskeletal loading and unloading. This study investigated a compensating response to skeletal muscle loss in a hindlimb-suspended model that involves up-regulation of mTOR phosphorylation at four weeks. Body weight and muscle volume significantly decreased over four weeks in the hindlimb-suspended group compared with the sham control. Expressions of p-mTOR, raptor protein, p-p70S6K, p-Akt, and p-ERK, anti- or pro-apoptotic p53, Bcl-2, Bcl-XL, Bax, and Bak proteins were significantly increased in the hindlimb-suspended group compared to the sham control at four weeks. These results indicate that p-mTOR and p-Akt/p-ERK proteins might be up-regulated to compensate for the loss of skeletal muscle in the hindlimb-suspended model. Expressions of p-AMPK, IRS1, and IRS2 proteins were significantly increased, but that of p-eIF2α was significantly reduced in the hindlimb-suspended group compared to the sham control at four weeks. Our results suggest that the loss of skeletal muscle in a hindlimb-suspended model induces activation of p-mTOR and p-Akt/p-ERK proteins, and that these signaling pathways may preserve protein synthesis and cell growth in skeletal muscles of hindlimb-suspended animals.

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References

  1. Morey-Holton E., Globus R. K., Kaplansky A., and Durnova G., “The Hindlimb Unloading Rat Model: Literature Overview, Technique Update and Comparison with Space Flight Data,” Advances in Space Biology and Medicine, Vol. 10, pp. 7–40, 2005.

    Article  Google Scholar 

  2. Morey-Holton E. R. and Globus R. K., “Hindlimb Unloading Rodent Model: Technical Aspects,” Journal of Applied Physiology, Vol. 92, No. 4, pp. 1367–1377, 2002.

    Article  Google Scholar 

  3. Bunn J. A., Buford T. W., Serra M. C., Kreider R. B., and Willoughby D. S., “Protein and Amino Acid Supplementation Does Not Alter Proteolytic Gene Expression Following Immobilization,” Journal of Nutrition and Metabolism, Vol. 2011, Article ID: 539690, 2011.

    Google Scholar 

  4. De Boer M. D., Maganaris C. N., Seynnes O. R., Rennie M. J., and Narici M. V., “Time Course of Muscular, Neural and Tendinous Adaptations to 23 Day Unilateral Lower-Limb Suspension in Young Men,” The Journal of Physiology, Vol. 583, No. 3, pp. 1079–1091, 2007.

    Article  Google Scholar 

  5. Hornsby, G., Watt, P., Murdoch, G., and Renniei, M., “Decrease in Human Quadriceps Muscle Protein Turnover Consequent Upon Leg Immobilization,” Clinical Science, Vol. 72, No. 4, pp. 503–509, 1987.

    Google Scholar 

  6. Akima, H., Hotta, N., Sato, K., Ishida, K., Koike, T., and Katayama, K., “Cycle Ergometer Exercise to Counteract Muscle Atrophy during Unilateral Lower Limb Suspension,” Aviation, Space, and Environmental Medicine, Vol. 80, No. 7, pp. 652–656, 2009.

    Article  Google Scholar 

  7. Ploutz-Snyder, L. L., Tesch, P. A., Crittenden, D. J., and Dudley, G. A., “Effect of Unweighting on Skeletal Muscle Use during Exercise,” Journal of Applied Physiology, Vol. 79, No. 1, pp. 168–175, 1995.

    Google Scholar 

  8. Biolo, G., Ciocchi, B., Lebenstedt, M., Barazzoni, R., Zanetti, M., et al., “Short Term Bed Rest Impairs Amino AcidInduced Protein Anabolism in Humans,” The Journal of Physiology, Vol. 558, No. 2, pp. 381–388, 2004.

    Article  Google Scholar 

  9. de Boer, M. D., Seynnes, O. R., di Prampero, P. E., Pišot, R., et al., “Effect of 5 Weeks Horizontal Bed Rest on Human Muscle Thickness and Architecture of Weight Bearing and Non-Weight Bearing Muscles,” European Journal of Applied Physiology, Vol. 104, No. 2, pp. 401–407, 2008.

    Article  Google Scholar 

  10. Drummond, M. J., Dickinson, J. M., Fry, C. S., Walker, D. K., Gundermann, D. M., et al., “Bed Rest Impairs Skeletal Muscle Amino Acid Transporter Expression, mTORC1 Signaling, and Protein Synthesis in Response to Essential Amino Acids in Older Adults,” American Journal of Physiology-Endocrinology and Metabolism, Vol. 302, No. 9, pp. E1113–E1122, 2012.

    Google Scholar 

  11. Ferrando, A. A., Lane, H. W., Stuart, C. A., Davis-Street, J., and Wolfe, R. R., “Prolonged Bed Rest Decreases Skeletal Muscle and Whole Body Protein Synthesis,” American Journal of Physiology-Endocrinology and Metabolism, Vol. 270, No. 4, pp. E627–E633, 1996.

    Google Scholar 

  12. Goodman, C. A., Mayhew, D. L., and Hornberger, T. A., “Recent Progress Toward Understanding the Molecular Mechanisms that Regulate Skeletal Muscle Mass,” Cellular Signalling, Vol. 23, No. 12, pp. 1896–1906, 2011.

    Article  Google Scholar 

  13. Hornberger, T. A., Sukhija, K. B., and Chien, S., “Regulation of mTOR By Mechanically Induced Signaling Events in Skeletal Muscle,” Cell Cycle, Vol. 5, No. 13, pp. 1391–1396, 2006.

    Article  Google Scholar 

  14. Kelleher, A. R., Kimball, S. R., Dennis, M. D., Schilder, R. J., and Jefferson, L. S., “The mTORC1 Signaling Repressors Redd1/2 are Rapidly Induced and Activation of P70s6k1 by Leucine is Defective in Skeletal Muscle of an Immobilized Rat Hindlimb,” American Journal of Physiology-Endocrinology and Metabolism, Vol. 304, No. 2, pp. E229–E236, 2013.

    Google Scholar 

  15. Banerjee, A. and Guttridge, D. C., “Mechanisms for Maintaining Muscle,” Current Opinion in Supportive and Palliative Care, Vol. 6, No. 4, pp. 451–456, 2012.

    Article  Google Scholar 

  16. Phillips, B. E., Hill, D. S., and Atherton, P. J., “Regulation of Muscle Protein Synthesis in Humans,” Current Opinion in Clinical Nutrition & Metabolic Care, Vol. 15, No. 1, pp. 58–63, 2012.

    Article  Google Scholar 

  17. Phillips, S. M., Glover, E. I., and Rennie, M. J., “Alterations of Protein Turnover Underlying Disuse Atrophy in Human Skeletal Muscle,” Journal of Applied Physiology, Vol. 107, No. 3, pp. 645–654, 2009.

    Article  Google Scholar 

  18. Booth, F. and Seider, M., “Early Change in Skeletal Muscle Protein Synthesis after Limb Immobilization of Rats,” Journal of Applied Physiology, Vol. 47, No. 5, pp. 974–977, 1979.

    Google Scholar 

  19. Glover, E. I., Phillips, S. M., Oates, B. R., Tang, J. E., Tarnopolsky, M. A., et al., “Immobilization Induces Anabolic Resistance in Human Myofibrillar Protein Synthesis with Low and High Dose Amino Acid Infusion,” The Journal of Physiology, Vol. 586, No. 24, pp. 6049–6061, 2008.

    Article  Google Scholar 

  20. Krawiec, B. J., Frost, R. A., Vary, T. C., Jefferson, L. S., and Lang, C. H., “Hindlimb Casting Decreases Muscle Mass in Part by Proteasome-Dependent Proteolysis but Independent of Protein Synthesis,” American Journal of Physiology-Endocrinology and Metabolism, Vol. 289, No. 6, pp. E969–E980, 2005.

    Google Scholar 

  21. Magne, H., SavaryAuzeloux, I., Migné, C., Peyron, M. A., Combaret, L., Rémond, D., and Dardevet, D., “Contrarily to whey and High Protein Diets, Dietary Free Leucine Supplementation Cannot Reverse the Lack of Recovery of Muscle Mass after Prolonged Immobilization during Ageing,” The Journal of Physiology, Vol. 590, No. 8, pp. 2035–2049, 2012.

    Article  Google Scholar 

  22. Dillon, E. L., “Nutritionally Essential Amino Acids and Metabolic Signaling in Aging,” Amino Acids, Vol. 45, No. 3, pp. 431–441, 2013.

    Article  MathSciNet  Google Scholar 

  23. Ge, Y. and Chen, J., “Mammalian Target of Rapamycin (mTOR) Signaling Network in Skeletal Myogenesis,” Journal of Biological Chemistry, Vol. 287, No. 52, pp. 43928–43935, 2012.

    Article  Google Scholar 

  24. Rutter, G., Dasilvaxavier, G., and Leclerc, I., “Roles of 5-Amp-Activated Protein Kinase (Ampk) in Mammalian Glucose Homoeostasis,” Biochemical Journal, Vol. 375, No. pp. 1–16, 2003.

    Article  Google Scholar 

  25. Schiaffino, S., Dyar, K. A., Ciciliot, S., Blaauw, B., and Sandri, M., “Mechanisms Regulating Skeletal Muscle Growth and Atrophy,” FEBS Journal, Vol. 280, No. 17, pp. 4294–4314, 2013.

    Article  Google Scholar 

  26. Witczak, C., Sharoff, C., and Goodyear, L., “Amp-Activated Protein Kinase in Skeletal Muscle: from Structure and Localization to Its Role as a Master Regulator of Cellular Metabolism,” Cellular and Molecular Life Sciences, Vol. 65, No. 23, pp. 3737–3755, 2008.

    Article  Google Scholar 

  27. Glass, D. J., “Pi3 Kinase Regulation of Skeletal Muscle Hypertrophy and Atrophy,” in: Phosphoinositide 3-Kinase in Health and Disease, Rommel, C., Vanhaesebroeck, B., and Vogt, P., (Eds.), Springer, pp. 267–278, 2011.

    Google Scholar 

  28. Latres, E., Amini, A. R., Amini, A. A., Griffiths, J., Martin, F. J., et al., “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,” Journal of Biological Chemistry, Vol. 280, No. 4, pp. 2737–2744, 2005.

    Article  Google Scholar 

  29. Musi, N. and Goodyear, L. J., “Insulin Resistance and Improvements in Signal Transduction,” Endocrine, Vol. 29, No. 1, pp. 73–80, 2006.

    Article  Google Scholar 

  30. Bertrand, L., Ginion, A., Beauloye, C., Hebert, A. D., Guigas, B., et al., “Ampk activation Restores the Stimulation of Glucose Uptake in an in Vitro Model of Insulin-Resistant Cardiomyocytes Via the Activation of Protein Kinase B,” American Journal of Physiology-Heart and Circulatory Physiology, Vol. 291, No. 1, pp. H239–H250, 2006.

    Google Scholar 

  31. Long, Y. C., Cheng, Z., Copps, K. D., and White, M. F., “Insulin Receptor Substrates Irs1 and Irs2 Coordinate Skeletal Muscle Growth and Metabolism Via the Akt and Ampk Pathways,” Molecular and Cellular Biology, Vol. 31, No. 3, pp. 430–441, 2011.

    Article  Google Scholar 

  32. Longnus, S., Segalen, C., Giudicelli, J., Sajan, M., Farese, R., and Van Obberghen, E., “Insulin Signalling Downstream of Protein Kinase B is Potentiated by 5’ Amp-Activated Protein Kinase in Rat Hearts in Vivo,” Diabetologia, Vol. 48, No. 12, pp. 2591–2601, 2005.

    Article  Google Scholar 

  33. Qiao, L. Y., Zhande, R., Jetton, T. L., Zhou, G., and Sun, X. J., “In Vivo Phosphorylation of Insulin Receptor Substrate 1 at Serine 789 by a Novel Serine Kinase in Insulin-Resistant Rodents,” Journal of Biological Chemistry, Vol. 277, No. 29, pp. 26530–26539, 2002.

    Article  Google Scholar 

  34. Tzatsos, A. and Tsichlis, P. N., “Energy Depletion Inhibits Phosphatidylinositol 3-Kinase/Akt Signaling and Induces Apoptosis Via Amp-Activated Protein Kinase-Dependent Phosphorylation of Irs-1 at Ser-794,” Journal of Biological Chemistry, Vol. 282, No. 25, pp. 18069–18082, 2007.

    Article  Google Scholar 

  35. Wang, C., Mao, X., Wang, L., Liu, M., Wetzel, M. D., et al., “Adiponectin Sensitizes Insulin Signaling by Reducing P70 S6 Kinase-Mediated Serine Phosphorylation of Irs-1,” Journal of Biological Chemistry, Vol. 282, No. 11, pp. 7991–7996, 2007.

    Article  Google Scholar 

  36. Bloomfield, S. A., Girten, B. E., and Weisbrode, S. E., “Effects of Vigorous Exercise Training and B-Agonist Administration on Bone Response to Hindlimb Suspension,” Journal of Applied Physiology, Vol. 83, No. 1, pp. 172–178, 1997.

    Google Scholar 

  37. Park, E. and Schultz, E., “A Simple Hindlimb Suspension Apparatus,” Aviation, Space, and Environmental Medicine, Vol. 64, No. 5, pp. 401–404, 1993.

    Google Scholar 

  38. Sarbassov, D. D., Ali, S. M., and Sabatini, D. M., “Growing Roles for the mTOR Pathway,” Current Opinion in Cell Biology, Vol. 17, No. 6, pp. 596–603, 2005.

    Article  Google Scholar 

  39. Steelman, L. S., Chappell, W. H., Abrams, S. L., Kempf, C. R., Long, J., et al., “Roles of the Raf/Mek/Erk and Pi3k/Pten/Akt/mTOR Pathways in Controlling Growth and Sensitivity to Therapy- Implications for Cancer and Aging,” Aging (Albany NY), Vol. 3, No. 3, pp. 192–222, 2011.

    Google Scholar 

  40. Ko, C. Y., Seo, D. H., and Kim, H. S., “Deterioration of Bone Quality in the Tibia and Fibula in Growing Mice during Skeletal Unloading: Gender-Related Differences,” Journal of Biomechanical Engineering, Vol. 133, No. 11, Paper No. 111003, 2011.

    Google Scholar 

  41. Waarsing, J., Day, J., Van der Linden, J., Ederveen, A., Spanjers, C., et al., “Detecting and Tracking Local Changes in the Tibiae of Individual Rats: A Novel Method to Analyse Longitudinal in Vivo Micro-Ct Data,” Bone, Vol. 34, No. 1, pp. 163–169, 2004.

    Article  Google Scholar 

  42. Seo, D. H., Kim, H. S., Ko, C. Y., Schreiber, J., Jang, Y. S., and Bae, K., “The Effects of Circadian Disturbances Induced by Night Shifts on the Mouse Peripheral Tissues,” Animal Cells and Systems, Vol. 16, No. 5, pp. 357–365, 2012.

    Article  Google Scholar 

  43. Luu, Y., Lublinsky, S., Ozcivici, E., Capilla, E., Pessin, J., et al., “In Vivo Quantification of Subcutaneous and Visceral Adiposity by Micro-Computed Tomography in a Small Animal Model,” Medical Engineering & Physics, Vol. 31, No. 1, pp. 34–41, 2009.

    Article  Google Scholar 

  44. Garman, R., Gaudette, G., Donahue, L. R., Rubin, C., and Judex, S., “Low-Level Accelerations Applied in the Absence of Weight Bearing can Enhance Trabecular Bone Formation,” Journal of Orthopaedic Research, Vol. 25, No. 6, pp. 732–740, 2007.

    Article  Google Scholar 

  45. Müller, R., Hahn, M., Vogel, M., Delling, G., and Rüegsegger, P., “Morphometric Analysis of Noninvasively Assessed Bone Biopsies: Comparison of High-Resolution Computed Tomography and Histologic Sections,” Bone, Vol. 18, No. 3, pp. 215–220, 1996.

    Article  Google Scholar 

  46. Rüegsegger, P., Koller, B., and Müller, R., “A Microtomographic System for the Nondestructive Evaluation of Bone Architecture,” Calcified Tissue International, Vol. 58, No. 1, pp. 24–29, 1996.

    Article  Google Scholar 

  47. Haddad, F., Adams, G., Bodell, P., and Baldwin, K., “Isometric Resistance Exercise Fails to Counteract Skeletal Muscle Atrophy Processes during the Initial Stages of Unloading,” Journal of Applied Physiology, Vol. 100, No. 2, pp. 433–441, 2006.

    Article  Google Scholar 

  48. BiBodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., et al., “Akt/mTOR Pathway is a Crucial Regulator of Skeletal Muscle Hypertrophy and Can Prevent Muscle Atrophy in Vivo,” Nature Cell Biology, Vol. 3, No. 11, pp. 1014–1019, 2001.

    Article  Google Scholar 

  49. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., et al., “Foxo Transcription Factors Induce the Atrophy-Related Ubiquitin Ligase Atrogin-1 and Cause Skeletal Muscle Atrophy,” Cell, Vol. 117, No. 3, pp. 399–412, 2004.

    Article  Google Scholar 

  50. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., et al., “Foxo3 Coordinately Activates Protein Degradation by the Autophagic/ Lysosomal and proteasomal Pathways in Atrophying Muscle Cells,” Cell Metabolism, Vol. 6, No. 6, pp. 472–483, 2007.

    Article  Google Scholar 

  51. Mammucari, C., Schiaffino, S., and Sandri, M., “Downstream of Akt: FoxO3 and mTOR in the Regulation of Autophagy in Skeletal Muscle,” Autophagy, Vol. 4, No. 4, pp. 524–526, 2008.

    Article  Google Scholar 

  52. Zhao, J., Brault, J. J., Schild, A., and Goldberg, A. L., “Coordinate Activation of Autophagy and the Proteasome Pathway by Foxo Transcription Factor,” Autophagy, Vol. 4, No. 3, pp. 378–380, 2008.

    Article  Google Scholar 

  53. Risson, V., Mazelin, L., Roceri, M., Sanchez, H., Moncollin, V., et al., “Muscle Inactivation of mTOR Causes Metabolic and Dystrophin Defects Leading to Severe Myopathy,” The Journal of Cell Biology, Vol. 187, No. 6, pp. 859–874, 2009.

    Article  Google Scholar 

  54. Bentzinger, C. F., Romanino, K., Cloëtta, D., Lin, S., Mascarenhas, J. B., et al., “Skeletal Muscle-Specific Ablation of Raptor, but Not of Rictor, Causes Metabolic Changes and Results in Muscle Dystrophy,” Cell Metabolism, Vol. 8, No. 5, pp. 411–424, 2008.

    Article  Google Scholar 

  55. Ohanna, M., Sobering, A. K., Lapointe, T., Lorenzo, L., Praud, C., et al., “Atrophy of S6k1/Skeletal Muscle Cells Reveals Distinct mTOR Effectors for Cell Cycle and Size Control,” Nature Cell Biology, Vol. 7, No. 3, pp. 286–294, 2005.

    Article  Google Scholar 

  56. Park, I. H., Erbay, E., Nuzzi, P., and Chen, J., “Skeletal Myocyte Hypertrophy Requires mTOR Kinase Activity and S6k1,” Experimental Cell Research, Vol. 309, No. 1, pp. 211–219, 2005.

    Article  Google Scholar 

  57. Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., et al., “Mediation of IGF-1-Induced Skeletal Myotube Hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 Pathways,” Nature Cell Biology, Vol. 3, No. 11, pp. 1009–1013, 2001.

    Article  Google Scholar 

  58. Kumar, A., Harris, T. E., Keller, S. R., Choi, K. M., Magnuson, M. A., and Lawrence, J. C., “Muscle-Specific Deletion of Rictor Impairs Insulin-Stimulated Glucose Transport and Enhances Basal Glycogen Synthase Activity,” Molecular and Cellular Biology, Vol. 28, No. 1, pp. 61–70, 2008.

    Article  Google Scholar 

  59. Shu, L. and Houghton, P. J., “The mTORC2 Complex Regulates Terminal Differentiation of C2C12 Myoblasts,” Molecular and Cellular Biology, Vol. 29, No. 17, pp. 4691–4700, 2009.

    Article  Google Scholar 

  60. Gorres, B. K., Bomhoff, G. L., Morris, J. K., and Geiger, P. C., “In Vivo Stimulation of Oestrogen Receptor a Increases Insulin Stimulated Skeletal Muscle Glucose Uptake,” The Journal of Physiology, Vol. 589, No. 8, pp. 2041–2054, 2011.

    Article  Google Scholar 

  61. Velders, M., Schleipen, B., Fritzemeier, K. H., Zierau, O., and Diel, P., “Selective Estrogen Receptor-B Activation Stimulates Skeletal Muscle Growth and Regeneration,” The FASEB Journal, Vol. 26, No. 5, pp. 1909–1920, 2012.

    Article  Google Scholar 

  62. Johnson, B., White, M., Hathaway, M., Christians, C., and Dayton, W., “Effect of a Combined Trenbolone Acetate and Estradiol Implant on Steady-State IGF-I Mrna Concentrations in the Liver Of Wethers and the Longissimus Muscle of Steers,” Journal of Animal Science-Menasha Then Albany Then Champaign IllinoiS-, Vol. 76, No. pp. 491–497, 1998.

    Google Scholar 

  63. Tsai, W. J. A., McCormick, K. M., Brazeau, D. A., and Brazeau, G. A., “Estrogen Effects on Skeletal Muscle Insulin-Like Growth Factor-1 and Myostatin in Ovariectomized Rats,” Experimental Biology and Medicine, Vol. 232, No. 10, pp. 1314–1325, 2007.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biomedical Engineering, College of Health Science, Yonsei University, 1, Yeonsedae-gil, Heungeop-myeon, Wonju-si, Gangwon-do, 220-710, South Korea

    Yeong-Min Yoo, Ji Hyung Park, Dong-Hyun Seo, Sinae Eom, Young Jin Jung & Han Sung Kim

  2. Division of Biological Science and Technology, College of Science and Technology, Yonsei University, 1, Yeonsedae-gil, Heungeop-myeon, Wonju-si, Gangwon-do, 220-710, South Korea

    Tack-Joong Kim

  3. Fraunhofer Institute IKTS-MD, Maria-Reiche-Str.2, 01109, Dresden, Germany

    Tae-Young Han

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  1. Yeong-Min Yoo
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Yeong-Min Yoo and Ji Hyung Park contributed equally to this work

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Yoo, YM., Park, J.H., Seo, DH. et al. Activation of mTOR for the loss of skeletal muscle in a hindlimb-suspended rat model. Int. J. Precis. Eng. Manuf. 16, 1003–1010 (2015). https://doi.org/10.1007/s12541-015-0130-1

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