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Journal of Nutrition and Metabolism
Volume 2011 (2011), Article ID 539690, 9 pages
http://dx.doi.org/10.1155/2011/539690
Research Article

Protein and Amino Acid Supplementation Does Not Alter Proteolytic Gene Expression following Immobilization

1Exercise and Biochemical Nutritional Laboratory, Department of Health, Human Performance, and Recreation, Baylor University, Waco, TX 76798, USA
2University of Florida College of Medicine, Gainesville, FL 32611, USA
3Education and Clinical Center of the Baltimore Veterans Affairs Medical Center, University of Maryland School of Medicine and the Geriatric Research, Baltimore, MD 21201, USA
4Texas A & M University, College Station, TX 77843, USA

Received 1 November 2010; Revised 28 January 2011; Accepted 13 June 2011

Academic Editor: Maurizio Muscaritoli

Copyright © 2011 Jennifer A. Bunn et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. W. Jones, R. J. Hill, P. A. Krasney, B. O'Conner, N. Peirce, and P. L. Greenhaff, “Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass,” The FASEB Journal, vol. 18, no. 9, pp. 1025–1027, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. G. E. Bettany, B. C. Ang, S. N. Georgiannos, D. Halliday, and J. Powell-Tuck, “Bed rest decreases whole-body protein turnover in post-absorptive man,” Clinical Science, vol. 90, no. 1, pp. 73–75, 1996. View at Google Scholar · View at Scopus
  3. D. Paddon-Jones, “Interplay of stress and physical inactivity on muscle loss: nutritional countermeasures,” Journal of Nutrition, vol. 136, no. 8, pp. 2123–2126, 2006. View at Google Scholar · View at Scopus
  4. D. Paddon-Jones, M. Sheffield-Moore, M. G. Cree et al., “Atrophy and impaired muscle protein synthesis during prolonged inactivity and stress,” Journal of Clinical Endocrinology & Metabolism, vol. 91, no. 12, pp. 4836–4841, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. R. W. Jackman and S. C. Kandarian, “The molecular basis of skeletal muscle atrophy,” American Journal of Physiology, vol. 287, no. 4, pp. C834–C843, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Féasson, D. Stockholm, D. Freyssenet et al., “Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle,” Journal of Physiology, vol. 543, no. 1, part 1, pp. 297–306, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Medina, S. S. Wing, and A. L. Goldberg, “Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy,” Biochemical Journal, vol. 307, part3, pp. 631–637, 1995. View at Google Scholar · View at Scopus
  8. R. Medina, S. S. Wing, A. Haas, and A. L. Goldberg, “Activation of the ubiquitin-ATP-dependent proteolytic system in skeletal muscle during fasting and denervation atrophy,” Biomedica Biochimica Acta, vol. 50, no. 4–6, pp. 347–356, 1991. View at Google Scholar · View at Scopus
  9. W. E. Mitch and A. L. Goldberg, “Mechanisms of disease: mechanisms of muscle wasting: the role of the ubiquitin-proteasome pathway,” The New England Journal of Medicine, vol. 335, no. 25, pp. 1897–1905, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. S. S. Wing, A. L. Haas, and A. L. Goldberg, “Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation,” Biochemical Journal, vol. 307, part 3, pp. 639–645, 1995. View at Google Scholar · View at Scopus
  11. N. E. Tawa Jr., I. C. Kettelhut, and A. L. Goldberg, “Dietary protein deficiency reduces lysosomal and nonlysosomal ATP-dependent proteolysis in muscle,” American Journal of Physiology, vol. 263, no. 2, part1, pp. E326–E334, 1992. View at Google Scholar · View at Scopus
  12. D. C. Guttridge, M. W. Mayo, L. V. Madrid, C. Y. Wang, and A. S. Baldwin, “NF-κB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia,” Science, vol. 289, no. 5488, pp. 2363–2365, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. M. B. Reid and Y. P. Li, “Tumor necrosis factor-α and muscle wasting: a cellular perspective,” Respiratory Research, vol. 2, no. 5, pp. 269–272, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. S. C. Kandarian and R. W. Jackman, “Intracellular signaling during skeletal muscle atrophy,” Muscle & Nerve, vol. 33, no. 2, pp. 155–165, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. J. M. Argiles and F. J. Lopez-Soriano, “The ubiquitin-dependent proteolytic pathway in skeletal muscle: its role in pathological states,” Trends in Pharmacological Sciences, vol. 17, no. 6, pp. 223–226, 1996. View at Google Scholar
  16. M. Llovera, C. Garcia-Martinez, N. Agell, F. J. Lopez-Soriano, and J. M. Argiles, “Muscle wasting associated with cancer cachexia is linked to an important activation of the ATP-dependent ubiquitin-mediated proteolysis,” International Journal of Cancer, vol. 61, no. 1, pp. 138–141, 1995. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Tessitore, G. Bonelli, and F. M. Baccino, “Early development of protein metabolic perturbations in the liver and skeletal muscle of tumour-bearing rats. A model system for cancer cachexia,” Biochemical Journal, vol. 241, no. 1, pp. 153–159, 1987. View at Google Scholar · View at Scopus
  18. V. E. Baracos, C. DeVivo, D. H. R. Hoyle, and A. L. Goldberg, “Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma,” American Journal of Physiology, vol. 268, no. 5, part 1, pp. E996–E1006, 1995. View at Google Scholar · View at Scopus
  19. R. C. May, Y. Hara, and R. A. Kelly, “Branched-chain amino acid metabolism in rat muscle: abnormal regulation in acidosis,” American Journal of Physiology, vol. 252, no. 6, part 1, pp. E712–E718, 1987. View at Google Scholar · View at Scopus
  20. W. E. Mitch, R. Medina, S. Grieber et al., “Metabolic acidosis stimulates muscle protein degradation by activating the adenosine triphosphate-dependent pathway involving ubiquitin and proteasomes,” Journal of Clinical Investigation, vol. 93, no. 5, pp. 2127–2133, 1994. View at Google Scholar · View at Scopus
  21. S. R. Price, B. K. England, J. L. Bailey, K. van Vreede, and W. E. Mitch, “Acidosis and glucocorticoids concomitantly increase ubiquitin andd proteasome subunit mRNAs in rat muscle,” American Journal of Physiology, vol. 267, no. 4, part 1, pp. C955–C960, 1994. View at Google Scholar · View at Scopus
  22. D. S. Willoughby, S. Sultemeire, and M. Brown, “Human muscle disuse atrophy after 28 days of immobilization in alower-limbwalking boot: a case study,” Journal of Exercise Physiology Online, vol. 6, no. 2, pp. 88–95, 2003. View at Google Scholar · View at Scopus
  23. R. Lalani, S. Bhasin, F. Byhower et al., “Myostatin and insulin-like growth factor-I and -II expression in the muscle of rats exposed to the microgravity environment of the Neurolab space shuttle flight,” Journal of Endocrinology, vol. 167, no. 3, pp. 417–428, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Ma, C. Mallidis, S. Bhasin et al., “Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression,” American Journal of Physiology, vol. 285, no. 2, pp. E363–E371, 2003. View at Google Scholar
  25. C. J. Carlson, F. W. Booth, and S. E. Gordon, “Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading,” American Journal of Physiology, vol. 277, no. 2, part 2, pp. R601–R606, 1999. View at Google Scholar · View at Scopus
  26. K. A. Reardon, J. Davis, and R. M. I. Kapsa, “Myostatin, insulin-like growth factor-1, and leukemia inhibitory factor mRNAs are upregulated in chronic human disuse muscle atrophy,” Muscle & Nerve, vol. 24, no. 7, pp. 893–899, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. C. H. Fang, G. Tiao, H. James, C. Ogle, J. E. Fischer, and P. O. Hasselgren, “Burn injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy-dependent pathway,” Journal of the American College of Surgeons, vol. 180, no. 2, pp. 161–170, 1995. View at Google Scholar · View at Scopus
  28. K. Baar, G. Nader, and S. Bodine, “Resistance exercise, muscle loading/unloading and the control of muscle mass,” Essays in Biochemistry, vol. 42, pp. 61–74, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. A. A. Ferrando, H. W. Lane, C. A. Stuart, J. Davis-Street, and R. R. Wolfe, “Prolonged bed rest decreases skeletal muscle and whole body protein synthesis,” American Journal of Physiology, vol. 270, no. 4, part 1, pp. E627–E633, 1996. View at Google Scholar · View at Scopus
  30. D. F. Goldspink, A. J. Morton, P. Loughna, and G. Goldspink, “The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat,” Pflügers Archiv—European Journal of Physiology, vol. 407, no. 3, pp. 333–340, 1986. View at Google Scholar · View at Scopus
  31. A. Ciechanover and A. L. Schwartz, “The ubiquitin system: pathogenesis of human diseases and drug targeting,” Biochimica et Biophysica Acta, vol. 1695, no. 1–3, pp. 3–17, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. S. H. Lecker, V. Solomon, W. E. Mitch, and A. L. Goldberg, “Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states,” Journal of Nutrition, vol. 129, no. 1, supplement 1, pp. 227S–237S, 1999. View at Google Scholar · View at Scopus
  33. J. Huang and N. E. Forsberg, “Role of calpain in skeletal-muscle protein degradation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 21, pp. 12100–12105, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Ishiura, H. Murofushi, K. Suzuki, and K. Imahori, “Studies of a calcium activated neutral protease from chicken skeletal muscle. I. Purification and characterization,” Journal of Biochemistry, vol. 84, no. 1, pp. 225–230, 1978. View at Google Scholar · View at Scopus
  35. M. Koohmaraie, “Ovine skeletal muscle multicatalytic proteinase complex (proteasome): purification, characterization, and comparison of its effects on myofibrils with mu-calpains,” Journal of Animal Science, vol. 70, no. 12, pp. 3697–3708, 1992. View at Google Scholar · View at Scopus
  36. F. C. Tan, D. E. Goll, and Y. Otsuka, “Some properties of the millimolar Ca2+-dependent proteinase from bovine cardiac muscle,” Journal of Molecular and Cellular Cardiology, vol. 20, no. 11, pp. 983–997, 1988. View at Google Scholar · View at Scopus
  37. W. A. Busch, M. H. Stromer, D. E. Goll, and A. Suzuki, “Ca2+ -specific removal of Z lines from rabbit skeletal muscle,” Journal of Cell Biology, vol. 52, no. 2, pp. 367–381, 1972. View at Google Scholar · View at Scopus
  38. E. Carafoli and M. Molinari, “Calpain: a protease in search of a function?” Biochemical and Biophysical Research Communications, vol. 247, no. 2, pp. 193–203, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Plomgaard, M. Penkowa, and B. K. Pedersen, “Fiber type specific expression of TNF-α, IL-6 and IL-18 in human skeletal muscles,” Exercise Immunology Review, vol. 11, pp. 53–63, 2005. View at Google Scholar · View at Scopus
  40. Y. P. Li and M. B. Reid, “NF-κB mediates the protein loss induced by TNF-αin differentiated skeletal muscle myotubes,” American Journal of Physiology, vol. 279, no. 4, pp. R1165–R1170, 2000. View at Google Scholar · View at Scopus
  41. L. Combaret, T. Tilignac, A. Claustre et al., “Torbafylline (HWA 448) inhibits enhanced skeletal muscle ubiquitin-proteasome-dependent proteolysis in cancer and septic rats,” Biochemical Journal, vol. 361, part 2, pp. 185–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. R. B. Hunter, E. J. Stevenson, C. Alan Koncarevi, H. Mitchell-Felton, D. A. Essig, and S. C. Kandarian, “Activation of an alternative NF-κB pathway in skeletal muscle during disuse atrophy,” The FASEB Journal, vol. 16, no. 6, pp. 529–538, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. P. Li, Y. Chen, A. S. Li, and M. B. Reid, “Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes,” American Journal of Physiology, vol. 285, no. 4, pp. C806–C812, 2003. View at Google Scholar · View at Scopus
  44. K. J. Ladner, M. A. Caligiuri, and D. C. Guttridge, “Tumor necrosis factor-regulated biphasic activation of NF-κB is required for cytokine-induced loss of skeletal muscle gene products,” Journal of Biological Chemistry, vol. 278, no. 4, pp. 2294–2303, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. P. Li, R. J. Schwartz, I. D. Waddell, B. R. Holloway, and M. B. Reid, “Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-κB activation in response to tumor necrosis factor α,” The FASEB Journal, vol. 12, no. 10, pp. 871–880, 1998. View at Google Scholar · View at Scopus
  46. D. Attaix, S. Ventadour, A. Codran, D. Béchet, D. Taillandier, and L. Combaret, “The ubiquitin-proteasome system and skeletal muscle wasting,” Essays in Biochemistry, vol. 41, pp. 173–186, 2005. View at Google Scholar · View at Scopus
  47. S. M. Wyke and M. J. Tisdale, “NF-κB mediates proteolysis-inducing factor induced protein degradation and expression of the ubiquitin-proteasome system in skeletal muscle,” British Journal of Cancer, vol. 92, no. 4, pp. 711–721, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Bar-Shai, E. Carmeli, and A. Z. Reznick, “The role of NF-κB in protein breakdown in immobilization, aging, and exercise: from basic processes to promotion of health,” Annals of the New York Academy of Sciences, vol. 1057, pp. 431–447, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Børsheim, A. Aarsland, and R. R. Wolfe, “Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise,” International Journal of Sport Nutrition and Exercise Metabolism, vol. 14, no. 3, pp. 255–271, 2004. View at Google Scholar
  50. C. C. Carroll, J. D. Fluckey, R. H. Williams, D. H. Sullivan, and T. A. Trappe, “Human soleus and vastus lateralis muscle protein metabolism with an amino acid infusion,” American Journal of Physiology, vol. 288, no. 3, pp. E479–E485, 2005. View at Publisher · View at Google Scholar
  51. B. B. Rasmussen, K. D. Tipton, S. L. Miller, S. E. Wolf, and R. R. Wolfe, “An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise,” Journal of Applied Physiology, vol. 88, no. 2, pp. 386–392, 2000. View at Google Scholar · View at Scopus
  52. K. D. Tipton, T. A. Elliott, M. G. Cree, S. E. Wolf, A. P. Sanford, and R. R. Wolfe, “Ingestion of casein and whey prosteins result in muscle anabolism after resistance exercise,” Medicine and Science in Sports and Exercise, vol. 36, no. 12, pp. 2073–2081, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. D. S. Willoughby, J. R. Stout, and C. D. Wilborn, “Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength,” Amino Acids, vol. 32, no. 4, pp. 467–477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Yokogoshi, S. Takase, T. Goda, and T. Hoshi, “Effects of suspension hypokinesia/hypodynamia on the body weight and nitrogen balance in rats fed with various protein concentrations,” Agricultural and Biological Chemistry, vol. 54, no. 3, pp. 779–789, 1990. View at Google Scholar
  55. L. L. Andersen, G. Tufekovic, M. K. Zebis et al., “The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength,” Metabolism, vol. 54, no. 2, pp. 151–156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Biolo, K. D. Tipton, S. Klein, and R. R. Wolfe, “An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein,” American Journal of Physiology, vol. 273, no. 1, part 1, pp. E122–E129, 1997. View at Google Scholar · View at Scopus
  57. K. Matsumoto, M. Mizuno, T. Mizuno et al., “Branched-chain amino acids and arginine supplementation attenuates skeletal muscle proteolysis induced by moderate exercise in young individuals,” International Journal of Sports Medicine, vol. 28, no. 6, pp. 531–538, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. C. M. Op den Kamp, R. C. Langen, A. Haegens, and A. M. Schols, “Muscle atrophy in cachexia: dan dietary protein tip the balance?” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 12, no. 6, pp. 611–616, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Paddon-Jones, M. Sheffield-Moore, R. J. Urban et al., “Essential amino acid and carbohydrate supplementation ameliorates muscle protein loss in humans during 28 days bedrest,” Journal of Clinical Endocrinology & Metabolism, vol. 89, no. 9, pp. 4351–4358, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Paddon-Jones, M. Sheffield-Moore, R. J. Urban, A. Aarsland, R. R. Wolfe, and A. A. Ferrando, “The catabolic effects of prolonged inactivity and acute hypercortisolemia are offset by dietary supplementation,” Journal of Clinical Endocrinology & Metabolism, vol. 90, no. 3, pp. 1453–1459, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Aquilani, C. Opasich, A. Gualco et al., “Adequate energy-protein intake is not enough to improve nutritional and metabolic status in muscle-depleted patients with chronic heart failure,” European Journal of Heart Failure, vol. 10, no. 11, pp. 1127–1135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. P. Engelen, E. P. Rutten, C. L. De Castro, E. F. Wouters, A. M. Schols, and N. E. Deutz, “Supplementation of soy protein with branched-chain amino acids alters protein metabolism in healthy elderly and even more in patients with chronic obstructive pulmonary disease,” American Journal of Clinical Nutrition, vol. 85, no. 2, pp. 431–439, 2007. View at Google Scholar · View at Scopus
  63. D. S. Willoughby and C. D. Wilborn, “Estradiol in females may negate skeletal muscle myostatin mRNA expression and serum myostatin propeptide levels after eccentric muscle contractions,” Journal of Sports Science and Medicine, vol. 5, no. 4, pp. 672–681, 2006. View at Google Scholar · View at Scopus
  64. “Current protocols in molecular biology,” in Short Protocols in Molecular Biology, A3, pp. 10–11, John Wiley & Sons, New York, NY, USA, 1999.
  65. T. W. Buford, M. B. Cooke, T. M. Manini, C. Leeuwenburgh, and D. S. Willoughby, “Effects of age and sedentary lifestyle on skeletal muscle NF-κB signaling in men,” The Journals of Gerontology. Series A, vol. 65, no. 5, pp. 532–537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Ogawa, H. Furochi, M. Mameoka et al., “Ubiquitin ligase gene expression in healthy volunteers with 20-day bedrest,” Muscle & Nerve, vol. 34, no. 4, pp. 463–469, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. D. A. Riley, J. L. W. Bain, and A. L. Haas, “Increased ubiquitin, conjugation of proteins during skeletal muscle atrophy,” Cell Biology, vol. 103, p. 401a, 1986. View at Google Scholar
  69. P. W. Vanderklish and B. A. Bahr, “The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states,” International Journal of Experimental Pathology, vol. 81, no. 5, pp. 323–339, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. N. Stupka, M. A. Tarnopolsky, N. J. Yardley, and S. M. Phillips, “Cellular adaptation to repeated eccentric exercise-induced muscle damage,” Journal of Applied Physiology, vol. 91, no. 4, pp. 1669–1678, 2001. View at Google Scholar · View at Scopus
  71. C. Garcia-Martinez, N. Agell, M. Llovera, F. J. Lopez-Soriano, and J. M. Argiles, “Tumour necrosis factor-α increases the ubiquitinization of rat skeletal muscle proteins,” FEBS Letters, vol. 323, no. 3, pp. 211–214, 1993. View at Publisher · View at Google Scholar · View at Scopus
  72. N. F. Gonzalez-Cadavid, W. E. Taylor, K. Yarasheski et al., “Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 25, pp. 14938–14943, 1998. View at Publisher · View at Google Scholar · View at Scopus
  73. C. D. McMahon, L. Popovic, J. M. Oldham et al., “Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension,” American Journal of Physiology, vol. 285, no. 1, pp. E82–E87, 2003. View at Google Scholar
  74. V. R. Edgerton, J. L. Smith, and D. R. Simpson, “Muscle fibre type populations of human leg muscles,” Histochemical Journal, vol. 7, no. 3, pp. 259–266, 1975. View at Google Scholar · View at Scopus
  75. D. Paddon-Jones, M. Sheffield-Moore, C. S. Katsanos, X. J. Zhang, and R. R. Wolfe, “Differential stimulation of muscle protein synthesis in elderly humans following isocaloric ingestion of amino acids or whey protein,” Experimental Gerontology, vol. 41, no. 2, pp. 215–219, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. R. R. Wolfe, S. L. Miller, and K. B. Miller, “Optimal protein intake in the elderly,” Clinical Nutrition, vol. 27, no. 5, pp. 675–684, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. I. Mujika and S. Padilla, “Detraining: loss of training-induced physiological and performance adaptations. Part II: long term insufficient training stimulus,” Sports Medicine, vol. 30, no. 3, pp. 145–154, 2000. View at Google Scholar · View at Scopus
  78. C. Lundby, N. Nordsborg, K. Kusuhara, K. M. Kristensen, P. D. Neufer, and H. Pilegaard, “Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies,” European Journal of Applied Physiology, vol. 95, no. 4, pp. 351–360, 2005. View at Publisher · View at Google Scholar · View at Scopus