Muscle atrophy induced by mechanical unloading: Mechanisms and potential countermeasures

Frontiers in Physiology

Volumn 9, Issue MAR, 2018, Pages

  Gao, Yunfang ^a   Arfat, Yasir ^a   Wang, Huiping ^a   Goswami, Nandu ^b  

^a NORTHWEST UNIVERSITY   (China)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Disuse muscle atrophy; Mechanical unloading; Molecular and cellular pathways; Protein degradation; Protein synthesis; Therapeutic countermeasures

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; ATROGIN 1; CALCIUM; CATECHIN; CURCUMIN; ELAMIPRETIDE; HERBACEOUS AGENT; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE RING FINGER 1 PROTEIN; POLYPHENOL; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; RESVERATROL; SOMATOMEDIN C; TETRAMETHYLPYRAZINE; TRANSCRIPTION FACTOR FOXO;

ADAPTATION; EXERCISE; HUMAN; INFLAMMATION; MECHANICAL UNLOADING; MECHANICS; MUSCLE ATROPHY; MUSCLE CONTRACTION; NONHUMAN; NUTRITION; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SUPPLEMENTATION; TRAINING;

EID: 85044130800     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2018.00235     Document Type: Review

References (252)

1. Abadi, A., Glover, E. I., Isfort, R. J., Raha, S., Safdar, A., Yasuda, N., et al. (2009). Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS ONE 4:e6518. doi: 10.1371/journal.pone.0006518
2. Adams, C. M., Ebert, S. M., and Dyle, M. C. (2017). Role of ATF4 in skeletal muscle atrophy. Curr. Opin. Clin. Nutr. Metab. Care 20, 164-168. doi: 10.1097/MCO.0000000000000362
3. Adams, G. R., Caiozzo, V. J., and Baldwin, K. M. (2003). Skeletal muscle unweighting: spaceflight and ground-based models. J. Appl. Physiol. (1985) 95, 2185-2201. doi: 10.1152/japplphysiol.00346.2003
4. Adams, G. R., Haddad, F., Bodell, P. W., Tran, P. D., and Baldwin, K. M. (2007). Combined isometric, concentric, and eccentric resistance exercise prevents unloading-induced muscle atrophy in rats. J. Appl. Physiol. (1985) 103, 1644-1654. doi: 10.1152/japplphysiol.00669.2007
5. Agten, A., Maes, K., Smuder, A., Powers, S. K., Decramer, M., and Gayan-Ramirez, G. (2011). N-Acetylcysteine protects the rat diaphragm from the decreased contractility associated with controlled mechanical ventilation. Crit. Care Med. 39, 777-782. doi: 10.1097/CCM.0b013e318206cca9
6. Akima, H., Kawakami, Y., Kubo, K., Sekiguchi, C., Ohshima, H., Miyamoto, A., et al. (2000). Effect of short-duration spaceflight on thigh and leg muscle volume. Med. Sci. Sports Exerc. 32, 1743-1747. doi: 10.1097/00005768-200010000-00013
7. Akima, H., Kubo, K., Imai, M., Kanehisa, H., Suzuki, Y., Gunji, A., et al. (2001). Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol. Scand. 172, 269-278. doi: 10.1046/j.1365-201x.2001.00869.x
8. Akima, H., Kuno, S., Suzuki, Y., Gunji, A., and Fukunaga, T. (1997). Effects of 20 days of bed rest on physiological cross-sectional area of human thigh and leg muscles evaluated by magnetic resonance imaging. J. Gravit. Physiol. 4, S15-21.
9. Allen, D. L., Bandstra, E. R., Harrison, B. C., Thorng, S., Stodieck, L. S., Kostenuik, P. J., et al. (2009). Effects of spaceflight on murine skeletal muscle gene expression. J. Appl. Physiol. 106, 582-595. doi: 10.1152/japplphysiol.90780.2008
10. 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. (1985) 83, 1857-1861. doi: 10.1152/jappl.1997.83.6.1857
11. Anastasi, G., Cutroneo, G., Santoro, G., Arco, A., Rizzo, G., Bramanti, P., et al. (2008). Costameric proteins in human skeletal muscle during muscular inactivity. J. Anat. 213, 284-295. doi: 10.1111/j.1469-7580.2008.00921.x
12. Anthony, J. C., Anthony, T. G., Kimball, S. R., Vary, T. C., and Jefferson, L. S. (2000a). Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased elF4F formation. J. Nutr. 130, 139-145. doi: 10.1093/jn/130.2.139
13. Anthony, J. C., Yoshizawa, F., Anthony, T. G., Vary, T. C., Jefferson, L. S., and Kimball, S. R. (2000b). Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J. Nutr. 130, 2413-2419. doi: 10.1093/jn/130.10.2413
14. Antonsson, B., Conti, F., Ciavatta, A., Montessuit, S., Lewis, S., Martinou, I., et al. (1997). Inhibition of Bax channel-forming activity by Bcl-2. Science 277, 370-372. doi: 10.1126/science.277.5324.370
15. Atherton, P. J., Greenhaff, P. L., Phillips, S. M., Bodine, S. C., Adams, C. M., and Lang, C. H. (2016). Control of skeletal muscle atrophy in response to disuse: clinical/preclinical contentions and fallacies of evidence. Am. J. Physiol. Endocrinol. Metab. 311, E594-E604. doi: 10.1152/ajpendo.00257.2016
16. Baehr, L. M., West, D. W. D., Marshall, A. G., Marcotte, G. R., Baar, K., and Bodine, S. C. (2017). Muscle-specific and age-related changes in protein synthesis and protein degradation in response to hindlimb unloading in rats. J. Appl. Physiol. 122, 1336-1350. doi: 10.1152/japplphysiol.00703.2016
17. Baehr, L. M., West, D. W., Marcotte, G., Marshall, A. G., De Sousa, L. G., Baar, K., et al. (2016). Age-related deficits in skeletal muscle recovery following disuse are associated with neuromuscular junction instability and ER stress, not impaired protein synthesis. Aging (Albany. NY). 8, 127-146. doi: 10.18632/aging.100879
18. Bajotto, G., Sato, Y., Kitaura, Y., and Shimomura, Y. (2011). Effect of branched-chain amino acid supplementation during unloading on regulatory components of protein synthesis in atrophied soleus muscles. Eur. J. Appl. Physiol. 111, 1815-1828. doi: 10.1007/s00421-010-1825-8
19. Baldwin, K. M. (1996). Effect of spaceflight on the functional, biochemical, and metabolic properties of skeletal muscle. Med. Sci. Sports Exerc. 28, 983-987. doi: 10.1097/00005768-199608000-00008
20. Baldwin, K. M., and Haddad, F. (2001). Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J. Appl. Physiol. (1985) 90, 345-357. doi: 10.1152/jappl.2001.90.1.345
21. Bashan, N., Kovsan, J., Kachko, I., Ovadia, H., and Rudich, A. (2009). Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol. Rev. 89, 27-71. doi: 10.1152/physrev.00014.2008
22. Baumgartner, R. N., Koehler, K. M., Gallagher, D., Romero, L., Heymsfield, S. B., Ross, R. R., et al. (1998). Epidemiology of sarcopenia among the elderly in New Mexico. Am. J. Epidemiol. 147, 755-763. doi: 10.1093/oxfordjournals.aje.a009520
23. Bechshøft, R. L., Malmgaard-Clausen, N. M., Gliese, B., Beyer, N., Mackey, A. L., Andersen, J. L., et al. (2017). Improved skeletal muscle mass and strength after heavy strength training in very old individuals. Exp. Gerontol. 92, 96-105. doi: 10.1016/j.exger.2017.03.014
24. Bialek, P., Morris, C., Parkington, J., St Andre, M., Owens, J., Yaworsky, P., et al. (2011). Distinct protein degradation profiles are induced by different disuse models of skeletal muscle atrophy. Physiol. Genomics 43, 1075-1086. doi: 10.1152/physiolgenomics.00247.2010
25. Bickel, C. S., Slade, J., Mahoney, E., Haddad, F., Dudley, G. A., and Adams, G. R. (2005). Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J. Appl. Physiol. (1985) 98, 482-488. doi: 10.1152/japplphysiol.00895.2004
26. Biolo, G., Tipton, K. D., Klein, S., and Wolfe, R. R. (1997). An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am. J. Physiol. 273(1 Pt 1), E122-129. doi: 10.1152/ajpendo.1997.273.1.E122
27. Bloch, R. J., and Gonzalez-Serratos, H. (2003). Lateral force transmission across costameres in skeletal muscle. Exerc. Sport Sci. Rev. 31, 73-78. doi: 10.1097/00003677-200304000-00004
28. Bodine, S. C. (2013). Disuse-induced muscle wasting. Int. J. Biochem. Cell Biol. 45, 2200-2208. doi: 10.1016/j.biocel.2013.06.011
29. Bodine, S. C., and Baehr, L. M. (2014). Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1. Am. J. Physiol. Endocrinol. Metab. 307, E469-E484. doi: 10.1152/ajpendo.00204.2014
30. 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
31. 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
32. Bogdanis, G. C. (2012). Effects of physical activity and inactivity on muscle fatigue. Front. Physiol. 3:142. doi: 10.3389/fphys.2012.00142
33. Bohé, J., Low, J. F., Wolfe, R. R., and Rennie, M. J. (2001). Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J. Physiol. 532(Pt 2), 575-579. doi: 10.1111/j.1469-7793.2001.0575f.x
34. Bonaldo, P., and Sandri, M. (2013). Cellular and molecular mechanisms of muscle atrophy. Dis. Model. Mech. 6, 25-39. doi: 10.1242/dmm.010389
35. Boonyarom, O., and Inui, K. (2006). Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol. (Oxf). 188, 77-89. doi: 10.1111/j.1748-1716.2006.01613.x
36. Booth, F. W., and Gollnick, P. D. (1983). Effects of disuse on the structure and function of skeletal muscle. Med. Sci. Sports Exerc. 15, 415-420. doi: 10.1249/00005768-198315050-00013
37. Booth, F. W., and Kelso, J. R. (1973). Effect of hind-limb immobilization on contractile and histochemical properties of skeletal muscle. Pflugers Arch. 342, 231-238. doi: 10.1007/BF00591371
38. Booth, F. W., and Seider, M. J. (1979). Early change in skeletal muscle protein synthesis after limb immobilization of rats. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 47, 974-977. doi: 10.1152/jappl.1979.47.5.974
39. Breen, L., Stokes, K. A., Churchward-Venne, T. A., Moore, D. R., Baker, S. K., Smith, K., et al. (2013). Two weeks of reduced activity decreases leg lean mass and induces "anabolic resistance" of myofibrillar protein synthesis in healthy elderly. J. Clin. Endocrinol. Metab. 98, 2604-2612. doi: 10.1210/jc.2013-1502
40. Brito, P. M., Simões, N. F., Almeida, L. M., and Dinis, T. C. (2008). Resveratrol disrupts peroxynitrite-triggered mitochondrial apoptotic pathway: a role for Bcl-2. Apoptosis 13, 1043-1053. doi: 10.1007/s10495-008-0235-4
41. Brocca, L., Cannavino, J., Coletto, L., Biolo, G., Sandri, M., Bottinelli, R., et al. (2012). The time course of the adaptations of human muscle proteome to bed rest and the underlying mechanisms. J. Physiol. (Lond). 590, 5211-5230. doi: 10.1113/jphysiol.2012.240267
42. Brocca, L., Toniolo, L., Reggiani, C., Bottinelli, R., Sandri, M., and Pellegrino, M. A. (2017). FoxO-dependent atrogenes vary among catabolic conditions and play a key role in muscle atrophy induced by hindlimb suspension. J. Physiol. (Lond). 595, 1143-1158. doi: 10.1113/JP273097
43. Brooks, N., Cloutier, G. J., Cadena, S. M., Layne, J. E., Nelsen, C. A., Freed, A. M., et al. (2008). Resistance training and timed essential amino acids protect against the loss of muscle mass and strength during 28 days of bed rest and energy deficit. J. Appl. Physiol. (1985) 105, 241-248. doi: 10.1152/japplphysiol.01346.2007
44. Brooks, N. E., and Myburgh, K. H. (2014). Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways. Front. Physiol. 5:99. doi: 10.3389/fphys.2014.00099
45. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., et al. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868. doi: 10.1016/S0092-8674(00)80595-4
46. Bullard, S. A., Seo, S., Schilling, B., Dyle, M. C., Dierdorff, J. M., Ebert, S. M., et al. (2016). Gadd45a Protein Promotes Skeletal Muscle Atrophy by Forming a Complex with the Protein Kinase MEKK4. J. Biol. Chem. 291, 17496-17509. doi: 10.1074/jbc.M116.740308
47. Caron, A. Z., Drouin, G., Desrosiers, J., Trensz, F., and Grenier, G. (2009). A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. J. Appl. Physiol. (1985) 106, 2049-2059. doi: 10.1152/japplphysiol.91505.2008
48. Carroll, C. C., Fluckey, J. D., Williams, R. H., Sullivan, D. H., and Trappe, T. A. (2005). Human soleus and vastus lateralis muscle protein metabolism with an amino acid infusion. Am. J. Physiol. Endocrinol. Metab. 288, E479-E485. doi: 10.1152/ajpendo.00393.2004
49. Chaillou, T., Kirby, T. J., and McCarthy, J. J. (2014). Ribosome biogenesis: emerging evidence for a central role in the regulation of skeletal muscle mass. J. Cell. Physiol. 229, 1584-1594. doi: 10.1002/jcp.24604
50. Chen, H. C., Appeddu, P. A., Isoda, H., and Guan, J. L. (1996). Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J. Biol. Chem. 271, 26329-26334. doi: 10.1074/jbc.271.42.26329
51. Chen, M., Won, D. J., Krajewski, S., and Gottlieb, R. A. (2002). Calpain and mitochondria in ischemia/reperfusion injury. J. Biol. Chem. 277, 29181-29186. doi: 10.1074/jbc.M204951200
52. 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. (1985) 73, 1383-1388. doi: 10.1152/jappl.1992.73.4.1383
53. Chopard, A., Arrighi, N., Carnino, A., and Marini, J. F. (2005). Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long-term bedrest with or without exercise. FASEB J. 19, 1722-1724. doi: 10.1096/fj.04-3336fje
54. Cornetti, U. (2009). Antioxidant use in nutraceuticals. Clin. Dermatol. 27, 175-194. doi: 10.1016/j.clindermatol.2008.01.010
55. Dani, C., Bonatto, D., Salvador, M., Pereira, M. D., Henriques, J. A., and Eleutherio, E. (2008). Antioxidant protection of resveratrol and catechin in Saccharomyces cerevisiae. J. Agric. Food Chem. 56, 4268-4272. doi: 10.1021/jf800752s
56. Das, S., Khan, N., Mukherjee, S., Bagchi, D., Gurusamy, N., Swartz, H., et al. (2008). Redox regulation of resveratrol-mediated switching of death signal into survival signal. Free Radic. Biol. Med. 44, 82-90. doi: 10.1016/j.freeradbiomed.2007.09.008
57. Dayton, W. R., Goll, D. E., Zeece, M. G., Robson, R. M., and Reville, W. J. (1976). A Ca2+-activated protease possibly involved in myofibrillar protein turnover. Purification from porcine muscle. Biochemistry 15, 2150-2158. doi: 10.1021/bi00655a019
58. de Boer, M. D., Selby, A., Atherton, P., Smith, K., Seynnes, O. R., Maganaris, C. N., et al. (2007). The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J. Physiol. 585(Pt 1), 241-251. doi: 10.1113/jphysiol.2007.142828
59. Degens, H., and Korhonen, M. T. (2012). Factors contributing to the variability in muscle ageing. Maturitas 73, 197-201. doi: 10.1016/j.maturitas.2012.07.015
60. Desaphy, J. F., Pierno, S., Liantonio, A., Giannuzzi, V., Digennaro, C., Dinardo, M. M., et al. (2010). Antioxidant treatment of hindlimb-unloaded mouse counteracts fiber type transition but not atrophy of disused muscles. Pharmacol. Res. 61, 553-563. doi: 10.1016/j.phrs.2010.01.012
61. Deschenes, M. R., Giles, J. A., McCoy, R. W., Volek, J. S., Gomez, A. L., and Kraemer, W. J. (2002). Neural factors account for strength decrements observed after short-term muscle unloading. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R578-R583. doi: 10.1152/ajpregu.00386.2001
62. Dillon, E. L., Sheffield-Moore, M., Paddon-Jones, D., Gilkison, C., Sanford, A. P., Casperson, S. L., et al. (2009). Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J. Clin. Endocrinol. Metab. 94, 1630-1637. doi: 10.1210/jc.2008-1564
63. Di Meo, S., Iossa, S., and Venditti, P. (2017). Skeletal muscle insulin resistance: role of mitochondria and other ROS sources. J. Endocrinol. 233, R15-R42. doi: 10.1530/JOE-16-0598
64. Dirks, M. L., Wall, B. T., Snijders, T., Ottenbros, C. L., Verdijk, L. B., and van Loon, L. J. (2014). Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol. (Oxf). 210, 628-641. doi: 10.1111/apha.12200
65. Dodd, S. L., Gagnon, B. J., Senf, S. M., Hain, B. A., and Judge, A. R. (2010). Ros-mediated activation of NF-kappaB and Foxo during muscle disuse. Muscle Nerve 41, 110-113. doi: 10.1002/mus.21526
66. Dong, F., Hua, Y., Zhao, P., Ren, J., Du, M., and Sreejayan, N. (2009). Chromium supplement inhibits skeletal muscle atrophy in hindlimb-suspended mice. J. Nutr. Biochem. 20, 992-999. doi: 10.1016/j.jnutbio.2008.09.006
67. Drew, B., Phaneuf, S., Dirks, A., Selman, C., Gredilla, R., Lezza, A., et al. (2003). Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R474-R480. doi: 10.1152/ajpregu.00455.2002
68. Dreyer, H. C., Drummond, M. J., Pennings, B., Fujita, S., Glynn, E. L., Chinkes, D. L., et al. (2008). Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am. J. Physiol. Endocrinol. Metab. 294, E392-E400. doi: 10.1152/ajpendo.00582.2007
69. Drummond, M. J., Dickinson, J. M., Fry, C. S., Walker, D. K., Gundermann, D. M., Reidy, P. T., et al. (2012). Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults. Am. J. Physiol. Endocrinol. Metab. 302, E1113-E1122. doi: 10.1152/ajpendo.00603.2011
70. Drummond, M. J., Reidy, P. T., Baird, L. M., Dalley, B. K., and Howard, M. T. (2017). Leucine differentially regulates gene-specific translation in mouse skeletal muscle. J. Nutr. 147, 1616-1623. doi: 10.3945/jn.117.251181
71. Du, B., and Gao, Y. (2014). Angelica and the contractile properties of soleus muscle in tail-suspended rats. J. Northwest Univ. 44, 588-594. doi: 10.16152/j.cnki.xdxbzr.2014.04.063
72. Du, F., Wang, J., Gao, Y., Wang, H., Wang, Q., Jiang, S., et al. (2011). A hind limb disuse model inducing extensor digitorum longus atrophy in rats: tail suspension-immobilization. Aviat. Space Environ. Med. 82, 689-693. doi: 10.3357/ASEM.2984.2011
73. Dupont-Versteegden, E. E., Fluckey, J. D., Knox, M., Gaddy, D., and Peterson, C. A. (2006). Effect of flywheel-based resistance exercise on processes contributing to muscle atrophy during unloading in adult rats. J. Appl. Physiol. (1985) 101, 202-212. doi: 10.1152/japplphysiol.01540.2005
74. Ebert, S. M., Dyle, M. C., Kunkel, S. D., Bullard, S. A., Bongers, K. S., Fox, D. K., et al. (2012). Stress-induced skeletal muscle Gadd45a expression reprograms myonuclei and causes muscle atrophy. J. Biol. Chem. 287, 27290-27301. doi: 10.1074/jbc.M112.374777
75. 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. (1985) 78, 1733-1739. doi: 10.1152/jappl.1995.78.5.1733
76. Erbay, E., Park, I. H., Nuzzi, P. D., Schoenherr, C. J., and Chen, J. (2003). IGF-II transcription in skeletal myogenesis is controlled by mTOR and nutrients. J. Cell Biol. 163, 931-936. doi: 10.1083/jcb.200307158
77. Evans, W. J. (2010). Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am. J. Clin. Nutr. 91, 1123S-1127S. doi: 10.3945/ajcn.2010.28608A
78. Farid, M., Reid, M. B., Li, Y. P., Gerken, E., and Durham, W. J. (2005). Effects of dietary curcumin or N-acetylcysteine on NF-kappaB activity and contractile performance in ambulatory and unloaded murine soleus. Nutr. Metab. (Lond). 2:20. doi: 10.1186/1743-7075-2-20
79. Ferrando, A. A., Tipton, K. D., Bamman, M. M., and Wolfe, R. R. (1997). Resistance exercise maintains skeletal muscle protein synthesis during bed rest. J. Appl. Physiol. (1985) 82, 807-810. doi: 10.1152/jappl.1997.82.3.807
80. Fetterman, J. W. Jr., and Zdanowicz, M. M. (2009). Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am. J. Health Syst. Pharm. 66, 1169-1179. doi: 10.2146/ajhp080411
81. Fitts, R. H., Brimmer, C. J., Heywood-Cooksey, A., and Timmerman, R. J. (1989). Single muscle fiber enzyme shifts with hindlimb suspension and immobilization. Am. J. Physiol. 256(5 Pt 1), C1082-C1091. doi: 10.1152/ajpcell.1989.256.5.C1082
82. Fitts, R. H., Riley, D. R., and Widrick, J. J. (2001). Functional and structural adaptations of skeletal muscle to microgravity. J. Exp. Biol. 204(Pt 18), 3201-3208.
83. Fitts, R. H., Trappe, S. W., Costill, D. L., Gallagher, P. M., Creer, A. C., Colloton, P. A., et al. (2010). Prolonged space flight-induced alterations in the structure and function of human skeletal muscle fibres. J. Physiol. 588(Pt 18), 3567-3592. doi: 10.1113/jphysiol.2010.188508
84. Fluckey, J. D., Dupont-Versteegden, E. E., Knox, M., Gaddy, D., Tesch, P. A., and Peterson, C. A. (2004). Insulin facilitation of muscle protein synthesis following resistance exercise in hindlimb-suspended rats is independent of a rapamycin-sensitive pathway. Am. J. Physiol. Endocrinol. Metab. 287, E1070-E1075. doi: 10.1152/ajpendo.00329.2004
85. Foletta, V. C., White, L. J., Larsen, A. E., Léger, B., and Russell, A. P. (2011). The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pflugers Arch. 461, 325-335. doi: 10.1007/s00424-010-0919-9
86. Fox, D. K., Ebert, S. M., Bongers, K. S., Dyle, M. C., Bullard, S. A., Dierdorff, J. M., et al. (2014). p53 and ATF4 mediate distinct and additive pathways to skeletal muscle atrophy during limb immobilization. Am. J. Physiol. Endocrinol. Metab. 307, E245-E261. doi: 10.1152/ajpendo.00010.2014
87. Gabriel, B. M., Hamilton, D. L., Tremblay, A. M., and Wackerhage, H. (2016). The Hippo signal transduction network for exercise physiologists. J. Appl. Physiol. (1985) 120, 1105-1117. doi: 10.1152/japplphysiol.01076.2015
88. Gambara, G., Salanova, M., Ciciliot, S., Furlan, S., Gutsmann, M., Schiffl, G., et al. (2017). Microgravity-induced transcriptome adaptation in mouse paraspinal longissimus dorsi muscle highlights insulin resistance-linked genes. Front. Physiol. 8:279. doi: 10.3389/fphys.2017.00279
89. Gao, Y. F., Fan, X. L., He, Z. X., Wu, S. D., and Song, X. A. (2005). [Effects of Ligustrazine and Radix Astragali on activities of myosin adenosine triphosphatase of soleus muscle and muscle atrophy in tail-suspended rats]. Space Med. Med. Eng. (Beijing). 18, 262-266. doi: 10.16289/j.cnki.1002-0837.2005.04.007
90. Gao, Y., Goswami, N., Grasser, E., Rössler, A., Stöger, E., Schwaberger, G., et al. (2008). Radix astragali and orthostatic response: a double-masked crossover study. Aviat. Space Environ. Med. 79, 94-98. doi: 10.3357/ASEM.2193.2008
91. Garrido, C., Galluzzi, L., Brunet, M., Puig, P. E., Didelot, C., and Kroemer, G. (2006). Mechanisms of cytochrome c release from mitochondria. Cell Death Differ. 13, 1423-1433. doi: 10.1038/sj.cdd.4401950
92. Gingras, A. A., White, P. J., Chouinard, P. Y., Julien, P., Davis, T. A., Dombrowski, L., et al. (2007). Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signalling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. J. Physiol. 579(Pt 1), 269-284. doi: 10.1113/jphysiol.2006.121079
93. Giresi, P. G., Stevenson, E. J., Theilhaber, J., Koncarevic, A., Parkington, J., Fielding, R. A., et al. (2005). Identification of a molecular signature of sarcopenia. Physiol. Genomics 21, 253-263. doi: 10.1152/physiolgenomics.00249.2004
94. Glover, E. I., Phillips, S. M., Oates, B. R., Tang, J. E., Tarnopolsky, M. A., Selby, A., et al. (2008). Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J. Physiol. (Lond). 586, 6049-6061. doi: 10.1113/jphysiol.2008.160333
95. Goldspink, D. F. (1977). The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J. Physiol. (Lond). 264, 267-282. doi: 10.1113/jphysiol.1977.sp011667
96. Goodman, C. A., Miu, M. H., Frey, J. W., Mabrey, D. M., Lincoln, H. C., Ge, Y., et al. (2010). A phosphatidylinositol 3-kinase/protein kinase B-independent activation of mammalian target of rapamycin signaling is sufficient to induce skeletal muscle hypertrophy. Mol. Biol. Cell 21, 3258-3268. doi: 10.1091/mbc.E10-05-0454
97. Gordon, B. S., Kelleher, A. R., and Kimball, S. R. (2013). Regulation of muscle protein synthesis and the effects of catabolic states. Int. J. Biochem. Cell Biol. 45, 2147-2157. doi: 10.1016/j.biocel.2013.05.039
98. Goswami, N. (2017). Falls and fall-prevention in older persons: geriatrics meets spaceflight! Front Physiol. 8:603. doi: 10.3389/fphys.2017.00603
99. Graham, Z. A., Gallagher, P. M., and Cardozo, C. P. (2015). Focal adhesion kinase and its role in skeletal muscle. J. Muscle Res. Cell Motil. 36, 305-315. doi: 10.1007/s10974-015-9415-3
100. Greig, C. A., Gray, C., Rankin, D., Young, A., Mann, V., Noble, B., et al. (2011). Blunting of adaptive responses to resistance exercise training in women over 75y. Exp. Gerontol. 46, 884-890. doi: 10.1016/j.exger.2011.07.010
101. Gustafsson, T., Osterlund, T., Flanagan, J. N., von Waldén, F., Trappe, T. A., Linnehan, R. M., et al. (2010). Effects of 3 days unloading on molecular regulators of muscle size in humans. J. Appl. Physiol. (1985) 109, 721-727. doi: 10.1152/japplphysiol.00110.2009
102. 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. (1985) 100, 433-441. doi: 10.1152/japplphysiol.01203.2005
103. Hamburg, N. M., McMackin, C. J., Huang, A. L., Shenouda, S. M., Widlansky, M. E., Schulz, E., et al. (2007). Physical inactivity rapidly induces insulin resistance and microvascular dysfunction in healthy volunteers. Arterioscler. Thromb. Vasc. Biol. 27, 2650-2656. doi: 10.1161/ATVBAHA.107.153288
104. Hamilton, D. L., Philp, A., MacKenzie, M. G., and Baar, K. (2010). A limited role for PI(3,4,5)P3 regulation in controlling skeletal muscle mass in response to resistance exercise. PLoS ONE 5:e11624. doi: 10.1371/journal.pone.0011624
105. Han, B., Tong, J., Zhu, M. J., Ma, C., and Du, M. (2008). Insulin-like growth factor-1 (IGF-1) and leucine activate pig myogenic satellite cells through mammalian target of rapamycin (mTOR) pathway. Mol. Reprod. Dev. 75, 810-817. doi: 10.1002/mrd.20832
106. Helliwell, T. R., Wilkinson, A., Griffiths, R. D., McClelland, P., Palmer, T. E., and Bone, J. M. (1998). Muscle fibre atrophy in critically ill patients is associated with the loss of myosin filaments and the presence of lysosomal enzymes and ubiquitin. Neuropathol. Appl. Neurobiol. 24, 507-517. doi: 10.1046/j.1365-2990.1998.00144.x
107. Herbert, M. E., Roy, R. R., and Edgerton, V. R. (1988). Influence of one-week hindlimb suspension and intermittent high load exercise on rat muscles. Exp. Neurol. 102, 190-198. doi: 10.1016/0014-4886(88)90093-3
108. Hornberger, T. A., Hunter, R. B., Kandarian, S. C., and Esser, K. A. (2001). Regulation of translation factors during hindlimb unloading and denervation of skeletal muscle in rats. Am. J. Physiol. Cell Physiol. 281, C179-C187. doi: 10.1152/ajpcell.2001.281.1.C179
109. Hornberger, T. A., Stuppard, R., Conley, K. E., Fedele, M. J., Fiorotto, M. L., Chin, E. R., et al. (2004). Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism. Biochem. J. 380(Pt 3), 795-804. doi: 10.1042/bj20040274
110. Hornberger, T. A., Sukhija, K. B., and Chien, S. (2006). Regulation of mTOR by mechanically induced signaling events in skeletal muscle. Cell Cycle 5, 1391-1396. doi: 10.4161/cc.5.13.2921
111. Hu, N. F., Chang, H., Du, B., Zhang, Q. W., Arfat, Y., Dang, K., et al. (2017). Tetramethylpyrazine ameliorated disuse-induced gastrocnemius muscle atrophy in hindlimb unloading rats through suppression of Ca2+/ROS-mediated apoptosis. Appl. Physiol. Nutr. Metab. 42, 117-127. doi: 10.1139/apnm-2016-0363
112. Hu, Q., Gao, Y., and Cao, J. (2009). Effects of different doses of Sijunzi Decoction on soleus atrophy in tail-suspmended rats. Space Med. Med. Eng. 22, 9-12. doi: 10.16289/j.cnki.1002-0837.2009.01.006
113. Huang, J., and Zhu, X. (2016). The molecular mechanisms of calpains action on skeletal muscle atrophy. Physiol. Res. 65, 547-560.
114. Hughes, D. C., Marcotte, G. R., Marshall, A. G., West, D. W. D., Baehr, L. M., Wallace, M. A., et al. (2017). Age-related differences in dystrophin: impact on force transfer proteins, membrane integrity, and neuromuscular junction stability. J. Gerontol. A Biol. Sci. Med. Sci. 72, 640-648. doi: 10.1093/gerona/glw109
115. Hvid, L., Aagaard, P., Justesen, L., Bayer, M. L., Andersen, J. L., Ørtenblad, N., et al. (2010). Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J. Appl. Physiol. (1985) 109, 1628-1634. doi: 10.1152/japplphysiol.00637.2010
116. Hvid, L. G., Suetta, C., Nielsen, J. H., Jensen, M. M., Frandsen, U., Ørtenblad, N., et al. (2014). Aging impairs the recovery in mechanical muscle function following 4 days of disuse. Exp. Gerontol. 52, 1-8. doi: 10.1016/j.exger.2014.01.012
117. Ingalls, C. P., Wenke, J. C., and Armstrong, R. B. (2001). Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles. Aviat. Space Environ. Med. 72, 471-476.
118. Inoki, K., Li, Y., Zhu, T. Q., Wu, J., and Guan, K. L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648-657. doi: 10.1038/ncb839
119. Jackson, J. R., Ryan, M. J., Hao, Y., and Alway, S. E. (2010). Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R1572-R1581. doi: 10.1152/ajpregu.00489.2010
120. Janssen, I., Heymsfield, S. B., Wang, Z. M., and Ross, R. (2000). Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J. Appl. Physiol. (1985) 89, 81-88. doi: 10.1152/jappl.2000.89.1.81
121. Jheng, H. F., Tsai, P. J., Guo, S. M., Kuo, L. H., Chang, C. S., Su, I. J., et al. (2012). Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol. Cell. Biol. 32, 309-319. doi: 10.1128/MCB.05603-11
122. Jones, S. W., Hill, R. J., Krasney, P. A., O'Conner, B., Peirce, N., and Greenhaff, P. L. (2004). Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J. 18, 1025-1027. doi: 10.1096/fj.03-1228fje
123. Jozsa, L., Thöring, J., Järvinen, M., Kannus, P., Lehto, M., and Kvist, M. (1988). Quantitative alterations in intramuscular connective tissue following immobilization: an experimental study in the rat calf muscles. Exp. Mol. Pathol. 49, 267-278. doi: 10.1016/0014-4800(88)90039-1
124. Katsanos, C. S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A., and Wolfe, R. R. (2006). A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am. J. Physiol. Endocrinol. Metab. 291, E381-E387. doi: 10.1152/ajpendo.00488.2005
125. Kelleher, A. R., Kimball, S. R., Dennis, M. D., Schilder, R. J., and Jefferson, L. S. (2013). 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. Am. J. Physiol. Endocrinol. Metab. 304, E229-E236. doi: 10.1152/ajpendo.00409.2012
126. Kelleher, A. R., Pereira, S. L., Jefferson, L. S., and Kimball, S. R. (2015). REDD2 expression in rat skeletal muscle correlates with nutrient-induced activation of mTORC1: responses to aging, immobilization, and remobilization. Am. J. Physiol. Endocrinol. Metab. 308, E122-E129. doi: 10.1152/ajpendo.00341.2014
127. Keller, K., and Engelhardt, M. (2013). Strength and muscle mass loss with aging process. Age and strength loss. Muscles Ligaments Tendons J. 3, 346-350.
128. Kimball, S. R., Shantz, L. M., Horetsky, R. L., and Jefferson, L. S. (1999). Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J. Biol. Chem. 274, 11647-11652. doi: 10.1074/jbc.274.17.11647
129. Knudsen, S. H., Hansen, L. S., Pedersen, M., Dejgaard, T., Hansen, J., Hall, G. V., et al. (2012). Changes in insulin sensitivity precede changes in body composition during 14 days of step reduction combined with overfeeding in healthy young men. J. Appl. Physiol. (1985) 113, 7-15. doi: 10.1152/japplphysiol.00189.2011
130. Kode, A., Rajendrasozhan, S., Caito, S., Yang, S. R., Megson, I. L., and Rahman, I. (2008). Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L478-L488. doi: 10.1152/ajplung.00361.2007
131. Koesterer, T. J., Dodd, S. L., and Powers, S. (2002). Increased antioxidant capacity does not attenuate muscle atrophy caused by unweighting. J. Appl. Physiol. (1985) 93, 1959-1965. doi: 10.1152/japplphysiol.00511.2002
132. Kortebein, P., Paddon-Jones, D., Ronsen, O., Trappe, T., Lombeida, J., Ferrando, A., et al. (2006). Effects of 10 days of bedrest on body composition and the rate of muscle protein synthesis in older men and women. FASEB J. 20, A159-A159.
133. Koryak, Y. U. (2001). Electrically evoked and voluntary properties of the human triceps surae muscle: effects of long-term spaceflights. Acta Physiol. Pharmacol. Bulg. 26, 21-27.
134. Kozlovskaya, I. B., Kreidich Yu, V., Oganov, V. S., and Koserenko, O. P. (1981). Pathophysiology of motor functions in prolonged manned space flights. Acta Astronaut. 8, 1059-1072. doi: 10.1016/0094-5765(81)90079-5
135. Krogh-Madsen, R., Thyfault, J. P., Broholm, C., Mortensen, O. H., Olsen, R. H., Mounier, R., et al. (2010). A 2-wk reduction of ambulatory activity attenuates peripheral insulin sensitivity. J. Appl. Physiol. (1985) 108, 1034-1040. doi: 10.1152/japplphysiol.00977.2009
136. Kumar, V., Atherton, P. J., Selby, A., Rankin, D., Williams, J., Smith, K., et al. (2012). Muscle protein synthetic responses to exercise: effects of age, volume, and intensity. J. Gerontol. A Biol. Sci. Med. Sci. 67, 1170-1177. doi: 10.1093/gerona/gls141
137. Kyparos, A., Feeback, D. L., Layne, C. S., Martinez, D. A., and Clarke, M. S. (2005). Mechanical stimulation of the plantar foot surface attenuates soleus muscle atrophy induced by hindlimb unloading in rats. J. Appl. Physiol. (1985) 99, 739-746. doi: 10.1152/japplphysiol.00771.2004
138. Labeit, S., Kohl, C. H., Witt, C. C., Labeit, D., Jung, J., and Granzier, H. (2010). Modulation of muscle atrophy, fatigue and MLC phosphorylation by MuRF1 as indicated by hindlimb suspension studies on MuRF1-KO mice. J. Biomed. Biotechnol. 2010:693741. doi: 10.1155/2010/693741
139. Lawler, J. M., Song, W., and Demaree, S. R. (2003). Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic. Biol. Med. 35, 9-16. doi: 10.1016/S0891-5849(03)00186-2
140. 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. (1985) 89, 2158-2164. doi: 10.1152/jappl.2000.89.6.2158
141. Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., et al. (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39-51. doi: 10.1096/fj.03-0610com
142. Levine, S., Biswas, C., Dierov, J., Barsotti, R., Shrager, J. B., Nguyen, T., et al. (2011). Increased proteolysis, myosin depletion, and atrophic AKT-FOXO signaling in human diaphragm disuse. Am. J. Respir. Crit. Care Med. 183, 483-490. doi: 10.1164/rccm.200910-1487OC
143. Li, S., Yang, Z., Gao, Y., Li, G., Wang, H., and Hinghofer-Szalkay, H. G. (2012). Ligustrazine and the contractile properties of soleus muscle in hindlimb-unloaded rats. Aviat. Space Environ. Med. 83, 1049-1054. doi: 10.3357/ASEM.3249.2012
144. Liu, H., Blough, E. R., Arvapalli, R., Wang, Y., Reiser, P. J., Paturi, S., et al. (2012). Regulation of contractile proteins and protein translational signaling in disused muscle. Cell. Physiol. Biochem. 30, 1202-1214. doi: 10.1159/000343310
145. Lomonosova, Y. N., Belova, S. P., Mirzoev, T. M., Kozlovskaya, I. B., and Shenkman, B. S. (2017). Eukaryotic elongation factor 2 kinase activation in M. soleus under 14-day hindlimb unloading of rats. Dokl. Biochem. Biophys. 474, 165-167. doi: 10.1134/S1607672917030048
146. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., et al. (2007). FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6, 458-471. doi: 10.1016/j.cmet.2007.11.001
147. Marimuthu, K., Murton, A. J., and Greenhaff, P. L. (2011). Mechanisms regulating muscle mass during disuse atrophy and rehabilitation in humans. J. Appl. Physiol. (1985) 110, 555-560. doi: 10.1152/japplphysiol.00962.2010
148. Matsumoto, A., Fujita, N., Arakawa, T., Fujino, H., and Miki, A. (2014). Influence of electrical stimulation on calpain and ubiquitin-proteasome systems in the denervated and unloaded rat tibialis anterior muscles. Acta Histochem. 116, 936-942. doi: 10.1016/j.acthis.2014.03.006
149. McCarthy, J. J., and Esser, K. A. (2010). Anabolic and catabolic pathways regulating skeletal muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 230-235. doi: 10.1097/MCO.0b013e32833781b5
150. McGlory, C., von Allmen, M. T., Stokes, T., Morton, R. G., Hector, A. J., Lago, B. A., et al. (2017). Failed recovery of glycemic control and myofibrillar protein synthesis with two weeks of physical inactivity in overweight, pre-diabetic older adults. J. Gerontol. A Biol. Sci. Med. Sci. doi: 10.1093/gerona/glx203. [Epub ahead of print].
151. Min, K., Smuder, A. J., Kwon, O. S., Kavazis, A. N., Szeto, H. H., and Powers, S. K. (2011). Mitochondrial-targeted antioxidants protect skeletal muscle against immobilization-induced muscle atrophy. J. Appl. Physiol. (1985) 111, 1459-1466. doi: 10.1152/japplphysiol.00591.2011
152. Miokovic, T., Armbrecht, G., Felsenberg, D., and Belavỳ, D. L. (2012). Heterogeneous atrophy occurs within individual lower limb muscles during 60 days of bed rest. J. Appl. Physiol. 113, 1545-1559. doi: 10.1152/japplphysiol.00611.2012
153. Mirzoev, T., Tyganov, S., Vilchinskaya, N., Lomonosova, Y., and Shenkman, B. (2016). Key markers of mTORC1-dependent and mTORC1-independent signaling pathways regulating protein synthesis in rat soleus muscle during early stages of hindlimb unloading. Cell Physiol. Biochem. 39, 1011-1020. doi: 10.1159/000447808
154. Mitch, W. E., and Goldberg, A. L. (1996). Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335, 1897-1905. doi: 10.1056/NEJM199612193352507
155. Miyazaki, M., McCarthy, J. J., Fedele, M. J., and Esser, K. A. (2011). Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J. Physiol. 589(Pt 7), 1831-1846. doi: 10.1113/jphysiol.2011.205658
156. Momken, I., Stevens, L., Bergouignan, A., Desplanches, D., Rudwill, F., Chery, I., et al. (2011). Resveratrol prevents the wasting disorders of mechanical unloading by acting as a physical exercise mimetic in the rat. FASEB J. 25, 3646-3660. doi: 10.1096/fj.10-177295
157. Morey-Holton, E. R., and Globus, R. K. (2002). Hindlimb unloading rodent model: technical aspects. J. Appl. Physiol. (1985) 92, 1367-1377. doi: 10.1152/japplphysiol.00969.2001
158. Moylan, J. S., and Reid, M. B. (2007). Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35, 411-429. doi: 10.1002/mus.20743
159. Murton, A. J., Constantin, D., and Greenhaff, P. L. (2008). The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim. Biophys. Acta 1782, 730-743. doi: 10.1016/j.bbadis.2008.10.011
160. Narici, M. V., and Maffulli, N. (2010). Sarcopenia: characteristics, mechanisms and functional significance. Br. Med. Bull. 95, 139-159. doi: 10.1093/bmb/ldq008
161. Nilwik, R., Snijders, T., Leenders, M., Groen, B. B., van Kranenburg, J., Verdijk, L. B., et al. (2013). The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp. Gerontol. 48, 492-498. doi: 10.1016/j.exger.2013.02.012
162. Oates, B. R., Glover, E. I., West, D. W., Fry, J. L., Tarnopolsky, M. A., and Phillips, S. M. (2010). Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve 42, 539-546. doi: 10.1002/mus.21721
163. Ogawa, T., Furochi, H., Mameoka, M., Hirasaka, K., Onishi, Y., Suzue, N., et al. (2006). Ubiquitin ligase gene expression in healthy volunteers with 20-day bedrest. Muscle Nerve 34, 463-469. doi: 10.1002/mus.20611
164. Ohira, T., Kawano, F., Ohira, T., Goto, K., and Ohira, Y. (2015). Responses of skeletal muscles to gravitational unloading and/or reloading. J. Physiol. Sci. 65, 293-310. doi: 10.1007/s12576-015-0375-6
165. Ohira, Y., Jiang, B., Roy, R. R., Oganov, V., Ilyina-Kakueva, E., Marini, J. F., et al. (1992). Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J. Appl. Physiol. (1985) 73(2 Suppl), 51S-57S. doi: 10.1152/jappl.1992.73.2.S51
166. Ohira, Y., Yoshinaga, T., Nomura, T., Kawano, F., Ishihara, A., Nonaka, I., et al. (2002). Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Adv. Space Res. 30, 777-781. doi: 10.1016/S0273-1177(02)00395-2
167. Ohira, Y., Yoshinaga, T., Ohara, M., Kawano, F., Wang, X. D., Higo, Y., et al. (2006). The role of neural and mechanical influences in maintaining normal fast and slow muscle properties. Cells Tissues Organs (Print). 182, 129-142. doi: 10.1159/000093963
168. Okamoto, T., and Machida, S. (2017). Changes in FOXO and proinflammatory cytokines in the late stage of immobilized fast and slow muscle atrophy. Biomed. Res. 38, 331-342. doi: 10.2220/biomedres.38.331
169. Okita, M., Yoshimura, T., Nakano, J., Saeki, A., Uehara, A., Mineshita, A., et al. (2001). Effects of short duration stretching on disuse muscle atrophy in immobilized rat soleus muscles. J. Jpn. Phys. Ther. Assoc. 4, 1-5. doi: 10.1298/jjpta.4.1
170. Olsen, R. H., Krogh-Madsen, R., Thomsen, C., Booth, F. W., and Pedersen, B. K. (2008). Metabolic responses to reduced daily steps in healthy nonexercising men. JAMA 299, 1261-1263. doi: 10.1001/jama.299.11.1259
171. Onda, A., Kono, H., Jiao, Q. B., Akimoto, T., Miyamoto, T., Sawada, Y., et al. (2016). New mouse model of skeletal muscle atrophy using spiral wire immobilization. Muscle Nerve 54, 788-791. doi: 10.1002/mus.25202
172. Ota, N., Soga, S., Haramizu, S., Yokoi, Y., Hase, T., and Murase, T. (2011). Tea catechins prevent contractile dysfunction in unloaded murine soleus muscle: a pilot study. Nutrition 27, 955-959. doi: 10.1016/j.nut.2010.10.008
173. Paddon-Jones, D. (2006). Interplay of stress and physical inactivity on muscle loss: nutritional countermeasures. J. Nutr. 136, 2123-2126. doi: 10.1093/jn/136.8.2123
174. Pasiakos, S. M., McClung, H. L., McClung, J. P., Margolis, L. M., Andersen, N. E., Cloutier, G. J., et al. (2011). Leucine-enriched essential amino acid supplementation during moderate steady state exercise enhances postexercise muscle protein synthesis. Am. J. Clin. Nutr. 94, 809-818. doi: 10.3945/ajcn.111.017061
175. Pavy-Le Traon, A., Heer, M., Narici, M. V., Rittweger, J., and Vernikos, J. (2007). From space to Earth: advances in human physiology from 20 years of bed rest studies (1986-2006). Eur. J. Appl. Physiol. 101, 143-194. doi: 10.1007/s00421-007-0474-z
176. Peng, X. D., Xu, P. Z., Chen, M. L., Hahn-Windgassen, A., Skeen, J., Jacobs, J., et al. (2003). Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17, 1352-1365. doi: 10.1101/gad.1089403
177. Peterson, J. M., Bakkar, N., and Guttridge, D. C. (2011). NF-kappaB signaling in skeletal muscle health and disease. Curr. Top. Dev. Biol. 96, 85-119. doi: 10.1016/B978-0-12-385940-2.00004-8
178. Phillips, S. M., Glover, E. I., and Rennie, M. J. (2009). Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J. Appl. Physiol. (1985) 107, 645-654. doi: 10.1152/japplphysiol.00452.2009
179. Philp, A., Hamilton, D. L., and Baar, K. (2011). Signals mediating skeletal muscle remodeling by resistance exercise: PI3-kinase independent activation of mTORC1. J. Appl. Physiol. (1985) 110, 561-568. doi: 10.1152/japplphysiol.00941.2010
180. Powers, S. K. (2014). Can antioxidants protect against disuse muscle atrophy? Sports Med. 44 (Suppl 2), S155-S165. doi: 10.1007/s40279-014-0255-x
181. Powers, S. K., Kavazis, A. N., and DeRuisseau, K. C. (2005). Mechanisms of disuse muscle atrophy: role of oxidative stress. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R337-R344. doi: 10.1152/ajpregu.00469.2004
182. Powers, S. K., Kavazis, A. N., and McClung, J. M. (2007). Oxidative stress and disuse muscle atrophy. J. Appl. Physiol. (1985) 102, 2389-2397. doi: 10.1152/japplphysiol.01202.2006
183. Powers, S. K., Smuder, A. J., and Judge, A. R. (2012). Oxidative stress and disuse muscle atrophy: cause or consequence? Curr. Opin. Clin. Nutr. Metab. Care 15, 240-245. doi: 10.1097/MCO.0b013e328352b4c2
184. Primeau, A. J., Adhihetty, P. J., and Hood, D. A. (2002). Apoptosis in heart and skeletal muscle. Can. J. Appl. Physiol. 27, 349-395. doi: 10.1139/h02-020
185. Qin, W. X., Gao, Y., Xue, W., Zhang, H., and Wang, H. (2009). Effects of two chinese herbs on muscle composition after 14 d of hind-limb unloading in rats. Space Med. Med. Eng. 22, 235-239. doi: 10.16289/j.cnki.1002-0837.2009.04.004
186. Redpath, N. T., Foulstone, E. J., and Proud, C. G. (1996). Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signalling pathway. EMBO J. 15, 2291-2297.
187. Reed, S. A., Sandesara, P. B., Senf, S. M., and Judge, A. R. (2012). Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J. 26, 987-1000. doi: 10.1096/fj.11-189977
188. Rennie, M. J. (2009). Anabolic resistance: the effects of aging, sexual dimorphism, and immobilization on human muscle protein turnover. Appl. Physiol. Nutr. Metab. 34, 377-381. doi: 10.1139/H09-012
189. 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
190. Richter, E. A., Kiens, B., Mizuno, M., and Strange, S. (1989). Insulin action in human thighs after one-legged immobilization. J. Appl. Physiol. (1985) 67, 19-23. doi: 10.1152/jappl.1989.67.1.19
191. Rieu, I., Magne, H., Savary-Auzeloux, I., Averous, J., Bos, C., Peyron, M. A., et al. (2009). Reduction of low grade inflammation restores blunting of postprandial muscle anabolism and limits sarcopenia in old rats. J. Physiol. 587(Pt 22), 5483-5492. doi: 10.1113/jphysiol.2009.178319
192. Risson, V., Mazelin, L., Roceri, M., Sanchez, H., Moncollin, V., Corneloup, C., et al. (2009). Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J. Cell Biol. 187, 859-874. doi: 10.1083/jcb.200903131
193. Rittweger, J., Frost, H. M., Schiessl, H., Ohshima, H., Alkner, B., Tesch, P., et al. (2005). Muscle atrophy and bone loss after 90 days' bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. Bone 36, 1019-1029. doi: 10.1016/j.bone.2004.11.014
194. Robb, E. L., Winkelmolen, L., Visanji, N., Brotchie, J., and Stuart, J. A. (2008). Dietary resveratrol administration increases MnSOD expression and activity in mouse brain. Biochem. Biophys. Res. Commun. 372, 254-259. doi: 10.1016/j.bbrc.2008.05.028
195. Roy, R. R., Baldwin, K. M., and Edgerton, V. R. (1991). The plasticity of skeletal muscle: effects of neuromuscular activity. Exerc. Sport Sci. Rev. 19, 269-312. doi: 10.1249/00003677-199101000-00008
196. Rudrappa, S. S., Wilkinson, D. J., Greenhaff, P. L., Smith, K., Idris, I., and Atherton, P. J. (2016). Human skeletal muscle disuse atrophy: effects on muscle protein synthesis, breakdown, and insulin resistance-a qualitative review. Front. Physiol. 7:361. doi: 10.3389/fphys.2016.00361
197. Ryan, M. J., Jackson, J. R., Hao, Y. L., Williamson, C. L., Dabkowski, E. R., Hollander, J. M., et al. (2010). Suppression of oxidative stress by resveratrol after isometric contractions in gastrocnemius muscles of aged mice. J. Gerontol. A Biol. Sci. Med. Sci. 65, 815-831. doi: 10.1093/gerona/glq080
198. Sacheck, J. M., Hyatt, J. P., Raffaello, A., Jagoe, R. T., Roy, R. R., Edgerton, V. R., et al. (2007). Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J. 21, 140-155. doi: 10.1096/fj.06-6604com
199. Salanova, M., Schiffl, G., Püttmann, B., Schoser, B. G., and Blottner, D. (2008). Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long-term bed rest with and without countermeasures. J. Anat. 212, 306-318. doi: 10.1111/j.1469-7580.2008.00854.x
200. Sandonà, D., Desaphy, J. F., Camerino, G. M., Bianchini, E., Ciciliot, S., Danieli-Betto, D., et al. (2012). Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS ONE 7:e33232. doi: 10.1371/journal.pone.0033232
201. Sandri, M. (2010). Autophagy in skeletal muscle. FEBS Lett. 584, 1411-1416. doi: 10.1016/j.febslet.2010.01.056
202. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., et al. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412. doi: 10.1016/S0092-8674(04)00400-3
203. Schiaffino, S., and Mammucari, C. (2011). Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1:4. doi: 10.1186/2044-5040-1-4
204. Scicchitano, B. M., Faraldi, M., and Musarò, A. (2015). The proteolytic systems of muscle wasting. Recent Adv. DNA Gene Seq. 9, 26-35. doi: 10.2174/2352092209999150911121502
205. Senf, S. M., Dodd, S. L., McClung, J. M., and Judge, A. R. (2008). Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J. 22, 3836-3845. doi: 10.1096/fj.08-110163
206. Servais, S., Letexier, D., Favier, R., Duchamp, C., and Desplanches, D. (2007). Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic. Biol. Med. 42, 627-635. doi: 10.1016/j.freeradbiomed.2006.12.001
207. Shangraw, R. E., Stuart, C. A., Prince, M. J., Peters, E. J., and Wolfe, R. R. (1988). Insulin responsiveness of protein metabolism in vivo following bedrest in humans. Am. J. Physiol. 255(4 Pt 1), E548-E558. doi: 10.1152/ajpendo.1988.255.4.E548
208. Shinohara, M., Yoshitake, Y., Kouzaki, M., Fukuoka, H., and Fukunaga, T. (2003). Strength training counteracts motor performance losses during bed rest. J. Appl. Physiol. (1985) 95, 1485-1492. doi: 10.1152/japplphysiol.01173.2002
209. Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., et al. (2005). Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U.S.A. 102, 5618-5623. doi: 10.1073/pnas.0501559102
210. Slimani, L., Micol, D., Amat, J., Delcros, G., Meunier, B., Taillandier, D., et al. (2012). The worsening of tibialis anterior muscle atrophy during recovery post-immobilization correlates with enhanced connective tissue area, proteolysis, and apoptosis. Am. J. Physiol. Endocrinol. Metab. 303, E1335-E1347. doi: 10.1152/ajpendo.00379.2012
211. Smuder, A. J., Hudson, M. B., Nelson, W. B., Kavazis, A. N., and Powers, S. K. (2012). Nuclear factor-kappaB signaling contributes to mechanical ventilation-induced diaphragm weakness. Crit. Care Med. 40, 927-934. doi: 10.1097/CCM.0b013e3182374a84
212. 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. Lond. 586, 283-291. doi: 10.1113/jphysiol.2007.141507
213. Spector, E. R., Smith, S. M., and Sibonga, J. D. (2009). Skeletal effects of long-duration head-down bed rest. Aviat. Space Environ. Med. 80, A23-A28. doi: 10.3357/ASEM.BR02.2009
214. Stein, T. P., and Blanc, S. (2011). Does protein supplementation prevent muscle disuse atrophy and loss of strength? Crit. Rev. Food Sci. Nutr. 51, 828-834. doi: 10.1080/10408398.2010.482679
215. Stein, T. P., Donaldson, M. R., Leskiw, M. J., Schluter, M. D., Baggett, D. W., and Boden, G. (2003). Branched-chain amino acid supplementation during bed rest: effect on recovery. J. Appl. Physiol. (1985) 94, 1345-1352. doi: 10.1152/japplphysiol.00481.2002
216. Stein, T. P., Leskiw, M. J., Schluter, M. D., Donaldson, M. R., and Larina, I. (1999). Protein kinetics during and after long-duration spaceflight on MIR. Am. J. Physiol. 276(6 Pt 1), E1014-E1021. doi: 10.1152/ajpendo.1999.276.6.E1014
217. Stephens, N. A., Gallagher, I. J., Rooyackers, O., Skipworth, R. J., Tan, B. H., Marstrand, T., et al. (2010). Using transcriptomics to identify and validate novel biomarkers of human skeletal muscle cancer cachexia. Genome Med. 2:1. doi: 10.1186/gm122
218. Stevenson, E. J., Giresi, P. G., Koncarevic, A., and Kandarian, S. C. (2003). Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J. Physiol. 551(Pt 1), 33-48. doi: 10.1113/jphysiol.2003.044701
219. Stipanuk, M. H. (2007). Leucine and protein synthesis: mTOR and beyond. Nutr. Rev. 65, 122-129. doi: 10.1111/j.1753-4887.2007.tb00289.x
220. Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., et al. (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395-403. doi: 10.1016/S1097-2765(04)00211-4
221. Stojiljkovic, D., Arsic, I., and Tadic, V. (2016). Extracts of wild apple fruit (Malus sylvestris (L.) Mill., Rosaceae) as a source of antioxidant substances for use in production of nutraceuticals and cosmeceuticals. Ind. Crops Prod. 80, 165-176. doi: 10.1016/j.indcrop.2015.11.023
222. Stuart, C. A., Shangraw, R. E., Peters, E. J., and Wolfe, R. R. (1990). Effect of dietary protein on bed-rest-related changes in whole-body-protein synthesis. Am. J. Clin. Nutr. 52, 509-514. doi: 10.1093/ajcn/52.3.509
223. Stuart, C. A., Shangraw, R. E., Prince, M. J., Peters, E. J., and Wolfe, R. R. (1988). Bed-rest-induced insulin resistance occurs primarily in muscle. Metab. Clin. Exp. 37, 802-806. doi: 10.1016/0026-0495(88)90018-2
224. Suetta, C., Hvid, L. G., Justesen, L., Christensen, U., Neergaard, K., Simonsen, L., et al. (2009). Effects of aging on human skeletal muscle after immobilization and retraining. J. Appl. Physiol. (1985) 107, 1172-1180. doi: 10.1152/japplphysiol.00290.2009
225. Sugiura, T., Abe, N., Nagano, M., Goto, K., Sakuma, K., Naito, H., et al. (2005). Changes in PKB/Akt and calcineurin signaling during recovery in atrophied soleus muscle induced by unloading. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1273-R1278. doi: 10.1152/ajpregu.00688.2004
226. Talbert, E. E., Smuder, A. J., Min, K., Kwon, O. S., and Powers, S. K. (2013). Calpain and caspase-3 play required roles in immobilization-induced limb muscle atrophy. J. Appl. Physiol. (1985) 114, 1482-1489. doi: 10.1152/japplphysiol.00925.2012
227. Tanner, R. E., Brunker, L. B., Agergaard, J., Barrows, K. M., Briggs, R. A., Kwon, O. S., et al. (2015). Age-related differences in lean mass, protein synthesis and skeletal muscle markers of proteolysis after bed rest and exercise rehabilitation. J. Physiol. (Lond). 593, 4259-4273. doi: 10.1113/JP270699
228. Tesch, P. A., Berg, H. E., Bring, D., Evans, H. J., and LeBlanc, A. D. (2005). Effects of 17-day spaceflight on knee extensor muscle function and size. Eur. J. Appl. Physiol. 93, 463-468. doi: 10.1007/s00421-004-1236-9
229. Thomason, D. B., and Booth, F. W. (1990). Atrophy of the soleus muscle by hindlimb unweighting. J. Appl. Physiol. (1985) 68, 1-12. doi: 10.1152/jappl.1990.68.1.1
230. Trappe, S., Trappe, T., Gallagher, P., Harber, M., Alkner, B., and Tesch, P. (2004). Human single muscle fibre function with 84 day bed-rest and resistance exercise. J. Physiol. 557(Pt 2), 501-513. doi: 10.1113/jphysiol.2004.062166
231. Trappe, T. (2009). Influence of aging and long-term unloading on the structure and function of human skeletal muscle. Appl. Physiol. Nutr. Metab. 34, 459-464. doi: 10.1139/H09-041
232. Tsika, R. W., Herrick, R. E., and Baldwin, K. M. (1987). Effect of anabolic steroids on skeletal muscle mass during hindlimb suspension. J. Appl. Physiol. (1985) 63, 2122-2127. doi: 10.1152/jappl.1987.63.5.2122
233. Veldhuizen, J. W., Verstappen, F. T., Vroemen, J. P., Kuipers, H., and Greep, J. M. (1993). Functional and morphological adaptations following four weeks of knee immobilization. Int. J. Sports Med. 14, 283-287. doi: 10.1055/s-2007-1021178
234. Verdijk, L. B., Dirks, M. L., Snijders, T., Prompers, J. J., Beelen, M., Jonkers, R. A., et al. (2012). Reduced satellite cell numbers with spinal cord injury and aging in humans. Med. Sci. Sports Exerc. 44, 2322-2330. doi: 10.1249/MSS.0b013e3182667c2e
235. Wall, B. T., Dirks, M. L., Snijders, T., Senden, J. M., Dolmans, J., and van Loon, L. J. (2014). Substantial skeletal muscle loss occurs during only 5 days of disuse. Acta Physiol. (Oxf). 210, 600-611. doi: 10.1111/apha.12190
236. Wall, B. T., Snijders, T., Senden, J. M., Ottenbros, C. L., Gijsen, A. P., Verdijk, L. B., et al. (2013). Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men. J. Clin. Endocrinol. Metab. 98, 4872-4881. doi: 10.1210/jc.2013-2098
237. Wang, X. D., Kawano, F., Matsuoka, Y., Fukunaga, K., Terada, M., Sudoh, M., et al. (2006). Mechanical load-dependent regulation of satellite cell and fiber size in rat soleus muscle. Am. J. Physiol. Cell Physiol. 290, C981-C989. doi: 10.1152/ajpcell.00298.2005
238. Welsh, G. I., Miller, C. M., Loughlin, A. J., Price, N. T., and Proud, C. G. (1998). Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in response to insulin. FEBS Lett. 421, 125-130. doi: 10.1016/S0014-5793(97)01548-2
239. West, D. W., Burd, N. A., Tang, J. E., Moore, D. R., Staples, A. W., Holwerda, A. M., et al. (2010). Elevations in ostensibly anabolic hormones with resistance exercise enhance neither training-induced muscle hypertrophy nor strength of the elbow flexors. J. Appl. Physiol. (1985) 108, 60-67. doi: 10.1152/japplphysiol.01147.2009
240. Widrick, J. J., Bangart, J. J., Karhanek, M., and Fitts, R. H. (1996). Soleus fiber force and maximal shortening velocity after non-weight bearing with intermittent activity. J. Appl. Physiol. (1985) 80, 981-987. doi: 10.1152/jappl.1996.80.3.981
241. Witkowski, S., Lovering, R. M., and Spangenburg, E. E. (2010). High-frequency electrically stimulated skeletal muscle contractions increase p70(s6k) phosphorylation independent of known IGF-I sensitive signaling pathways. FEBS Lett. 584, 2891-2895. doi: 10.1016/j.febslet.2010.05.003
242. Wu, X., Gao, Y. F., Zhao, X. H., and Cui, J. H. (2012). [Effects of tetramethylpyrazine on nitric oxide synthase activity and calcium ion concentration of skeletal muscle in hindlimb unloading rats]. Zhonghua Yi Xue Za Zhi 92, 2075-2077. doi: 10.3760/cma.j.issn.0376-2491.2012.29.016
243. Xu, P. T., Li, Q., Sheng, J. J., Chang, H., Song, Z., and Yu, Z. B. (2012). Passive stretch reduces calpain activity through nitric oxide pathway in unloaded soleus muscles. Mol. Cell. Biochem. 367, 113-124. doi: 10.1007/s11010-012-1325-8
244. You, J. S., Park, M. N., Song, W., and Lee, Y. S. (2010). Dietary fish oil alleviates soleus atrophy during immobilization in association with Akt signaling to p70s6k and E3 ubiquitin ligases in rats. Appl. Physiol. Nutr. Metab. 35, 310-318. doi: 10.1139/H10-022
245. Zha, H., Aimé-Sempé, C., Sato, T., and Reed, J. C. (1996). Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J. Biol. Chem. 271, 7440-7444. doi: 10.1074/jbc.271.13.7440
246. Zhang, H., He, Z., Gao, Y., Hinghofer-Szalkay, H. G., and Fan, X. (2007). Muscle composition after 14-day hindlimb unloading in rats: effects of two herbal compounds. Aviat. Space Environ. Med. 78, 926-931. doi: 10.3357/ASEM.2072.2007
247. Zhang, J., Li, Y., Li, G., Ma, X., Wang, H., Goswami, N., et al. (2017). Identification of the optimal dose and calpain system regulation of tetramethylpyrazine on the prevention of skeletal muscle atrophy in hindlimb unloading rats. Biomed. Pharmacother. 96, 513-523. doi: 10.1016/j.biopha.2017.10.012
248. Zhang, Q. W., Li, G. Y., Ren, Y. P., and Gao, Y. F. (2015). [Effect of two Pi deficiency syndrome models on the configuration and function of the skeletal muscle in mice]. Zhongguo Zhong Xi Yi Jie He Za Zhi 35, 71-75. doi: 10.7661/CJIM.2015.01.0071
249. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., et al. (2007). FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483. doi: 10.1016/j.cmet.2007.11.004
250. Zhong, H., Roy, R. R., Siengthai, B., and Edgerton, V. R. (2005). Effects of inactivity on fiber size and myonuclear number in rat soleus muscle. J. Appl. Physiol. (1985) 99, 1494-1499. doi: 10.1152/japplphysiol.00394.2005
251. Zhou, Y., Xue, S., and Yang, J. J. (2013). Calciomics: integrative studies of Ca2+-binding proteins and their interactomes in biological systems. Metallomics 5, 29-42. doi: 10.1039/C2MT20009K
252. Zuo, L., and Pannell, B. K. (2015). Redox characterization of functioning skeletal muscle. Front. Physiol. 6:338. doi: 10.3389/fphys.2015.00338