Identification of cold-shock protein RBM3 as a possible regulator of skeletal muscle size through expression profiling

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 4, 2008, Pages

  Dupont Versteegden, Esther E ^a,e   Nagarajan, Radhakrishnan ^b   Beggs, Marjorie L ^c   Bearden, Edward D ^c   Simpson, Pippa M ^d   Peterson, Charlotte A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^e NONE   (United States)

Author keywords

Aging; Atrophy; Cirp; Microarray

Indexed keywords

COLD SHOCK PROTEIN; RNA BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; IMMOBILIZATION; MALE; MICROARRAY ANALYSIS; MUSCLE ATROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SOLEUS MUSCLE; UNINDEXED SEQUENCE; UPREGULATION;

AGE FACTORS; ANIMALS; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION PROFILING; HINDLIMB SUSPENSION; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, INBRED BN; RATS, INBRED F344; RNA-BINDING PROTEINS; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 57349185907     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90455.2008     Document Type: Article

References (111)

1. Al-Fageeh MB, Smales CM. Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem J 397: 247-259, 2006.
2. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol Cell Physiol 273: C579-C587, 1997.
3. Altun M, Edstrom E, Spooner E, Flores-Moralez A, Bergman E, Tollet-Egnell P, Norstedt G, Kessler BM, Ulfhake B. Iron load and redox stress in skeletal muscle of aged rats. Muscle Nerve 36: 223-233, 2007.
4. Bassey EJ, Fiatarone MA, O'Neill EA, Kelley M, Evans WJ, Lipsitz LA. Leg extensor power and functional performance in very old men and women. Clin Sci 82: 321-327, 1992.
5. Bearden ED, Simpson PM, Peterson CA, Beggs ML. Assessing the reliability of amplified RNA used in microarrays: a DUMB table approach. Appl Bioinformatics 5: 67-76, 2006.
6. Bey L, Akunuri N, Zhao P, Hoffman EP, Hamilton DG, Hamilton MT. Patterns of global gene expression in rat skeletal muscle during unloading and low-intensity ambulatory activity. Physiol Genomics 13: 157-167, 2003.
7. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
8. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
9. Broome CS, Kayani AC, Palomero J, Dillmann WH, Mestril R, Jackson MJ, McArdle A. Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity. FASEB J 20: 1549-1551, 2006.
10. Brown A, McCartney N, Sale D. Positive adaptations to weight-lifting training in the elderly. J Appl Physiol 69: 1725-1733, 1990.
11. Brown M, Hasser EM. Differential effects of reduced muscle use (hindlimb unweighting) on skeletal muscle with aging. Aging 8: 99-105, 1996.
12. Byrne KA, Wang YH, Lehnert SA, Harper GS, McWilliam SM, Bruce HL, Reverter A. Gene expression profiling of muscle tissue in Brahman steers during nutritional restriction. J Anim Sci 83: 1-12, 2005.
13. Campbell WW, Crim MC, Young VR, Evans WJ. Increased energy requirements and changes in body composition with resistance training in older adults. Am J Clin Nutr 60: 167-175, 1994.
14. Campbell WW, Crim MC, Young VR, Joseph LJ, Evans WJ. Effects of resistance training and dietary protein intake on protein metabolism in older adults. Am J Physiol Regul Integr Comp Physiol 268: R208-R213, 1995.
15. Chakravarthy MV, Davis BS, Booth FW. IGF-1 restores satellite cell proliferative potential in immobilized old skeletal muscle. J Appl Physiol 89: 1365-1379, 2000.
16. Chappell SA, Mauro VP. The internal ribosome entry site (IRES) contained within the RNA-binding motif protein 3 (Rbm3) mRNA is composed of functionally distinct elements. J Biol Chem 278: 33793-33800, 2003.
17. Chappell SA, Owens GC, Mauro VP. A 5′ Leader of Rbm3, a cold stress-induced mRNA, mediates internal initiation of translation with increased efficiency under conditions of mild hypothermia. J Biol Chem 276: 36917-36922, 2001.
18. Chen YW, Gregory CM, Scarborough MT, Shi R, Walter GA, Vandenborne K. Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol Genomics, 2007.
19. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
20. Closs EI, Boissel JP, Habermeier A, Rotmann A. Structure and function of cationic amino acid transporters (CATs). J Membr Biol 213: 67-77, 2006.
21. Cros N, Tkatchenko AV, Pisani DF, Leclerc L, Leger JJ, Marini JF, Dechesne CA. Analysis of altered gene expression in rat soleus muscle atrophied by disuse. J Cell Biochem 83: 508-519, 2001.
22. Danno S, Nishiyama H, Higashitsuji H, Yokoi H, Xue JH, Itoh K, Matsuda T, Fujita J. Increased transcript level of RBM3, a member of the glycine-rich RNA-binding protein family, in human cells in response to cold stress. Biochem Biophys Res Commun 236: 804-807, 1997.
23. Derry JM, Kerns JA, Francke U. RBM3, a novel human gene in Xp11.23 with a putative RNA-binding domain. Hum Mol Genet 4: 2307-2311, 1995.
24. Dresios J, Aschrafi A, Owens GC, Vanderklish PW, Edelman GM, Mauro VP. Cold stress-induced protein Rbm3 binds 60S ribosomal subunits, alters microRNA levels, and enhances global protein synthesis. Proc Natl Acad Sci USA 102: 1865-1870, 2005.
25. Dupont-Versteegden EE. Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 40: 473-481, 2005.
26. Dupont-Versteegden EE. Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 12: 7463-7466, 2006.
27. Dupont-Versteegden EE, Fluckey JD, Knox M, Gaddy D, Peterson CA. Effect of flywheel-based resistance exercise on processes contributing to muscle atrophy during unloading in adult rats. J Appl Physiol 101: 202-212, 2006.
28. Dupont-Versteegden EE, Knox M, Gurley CM, Houlé JD, Peterson CA. Maintenance of muscle mass is not dependent on the calcineurin-NFAT pathway. Am J Physiol Cell Physiol 282: C1387-C1395, 2002.
29. Dupont-Versteegden EE, Strotman BA, Gurley CM, Gaddy D, Knox M, Fluckey JD, Peterson CA. Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am J Physiol Regul Integr Comp Physiol 291: R1730-R1740, 2006.
30. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263: 3029-3034, 1990.
31. Fluck M, Schmutz S, Wittwer M, Hoppeler H, Desplanches D. Transcriptional reprogramming during reloading of atrophied rat soleus muscle. Am J Physiol Regul Integr Comp Physiol 289: R4-R14, 2005.
32. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64: 1038-1044, 1988.
33. Gallegly JC, Turesky NA, Strotman BA, Gurley CM, Peterson CA, Dupont-Versteegden EE. Satellite cell regulation of muscle mass is altered at old age. J Appl Physiol 97: 1082-1090, 2004.
34. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G. Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286: 433-442, 2001.
35. Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA, Kandarian SC. Identification of a molecular signature of sarcopenia. Physiol Genomics 21: 253-263, 2005.
36. Goldspink G, Fernandes K, Williams PE, Wells DJ. Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice. Neuromuscul Disord 4: 183-191, 1994.
37. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001.
38. Graumann PL, Marahiel MA. A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23: 286-290, 1998.
39. Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflügers Arch 447: 619-628, 2004.
40. Harlow HJ, Lohuis T, Beck TD, Iaizzo PA. Muscle strength in overwintering bears. Nature 409: 997, 2001.
41. Hellen CU, Sarnow P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev 15: 1593-1612, 2001.
42. Hirose T, Sugita M, Sugiura M. cDNA structure, expression and nucleic acid-binding properties of three RNA-binding proteins in tobacco: occurrence of tissue-specific alternative splicing. Nucleic Acids Res 21: 3981-3987, 1993.
43. Hofer T, Marzetti E, Xu J, Seo AY, Gulec S, Knutson MD, Leeuwenburgh C, Dupont-Versteegden EE. Increased iron content and RNA oxidative damage in skeletal muscle with aging and disuse atrophy. Exp Gerontol 43: 563-570, 2008.
44. Howard G, Steffen JM, Geoghegan TE. Transcriptional regulation of decreased protein synthesis during skeletal muscle unloading. J Appl Physiol 66: 1093-1098, 1989.
45. Ikeda R, Yoshida K, Ushiyama M, Yamaguchi T, Iwashita K, Futagawa T, Shibayama Y, Oiso S, Takeda Y, Kariyazono H, Furukawa T, Nakamura K, Akiyama S, Inoue I, Yamada K. The small heat shock protein αB-crystallin inhibits differentiation-induced caspase 3 activation and myogenic differentiation. Biol Pharm Bull 29: 1815-1819, 2006.
46. Inaguma Y, Goto S, Shinohara H, Hasegawa K, Ohshima K, Kato K. Physiological and pathological changes in levels of the two small stress proteins, HSP27 and α-B crystallin, in rat hindlimb muscles. J Biochem (Tokyo) 114: 378-384, 1993.
47. Ishihara A, Oishi Y, Roy RR, Edgerton VR. Influence of two weeks of non-weight bearing on rat soleus motoneurons and muscle fibers. Aviat Space Environ Med 68: 421-425, 1997.
48. Jagoe RT, Lecker SH, Gomes M, Goldberg AL. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 16: 1697-1712, 2002.
49. Jozsi AC, Dupont-Versteegden EE, Taylor-Jones JM, Evans WJ, Trappe TA, Campbell WW, Peterson CA. Aged human muscle demonstrates an altered gene expression profile consistent with an impaired response to exercise. Mech Ageing Dev 120: 45-56, 2000.
50. Kamradt MC, Chen F, Sam S, Cryns VL. The small heat shock protein αB-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J Biol Chem 277: 38731-38736, 2002.
51. Kayo T, Allison DB, Weindruch R, Prolla TA. Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci USA 98: 5093-5098, 2001.
52. Kita H, Carmichael J, Swartz J, Muro S, Wyttenbach A, Matsubara K, Rubinsztein DC, Kato K. Modulation of polyglutamine-induced cell death by genes identified by expression profiling. Hum Mol Genet 11: 2279-2287, 2002.
53. Kohno K, Izumi H, Uchiumi T, Ashizuka M, Kuwano M. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25: 691-698, 2003.
54. Koncarevic A, Jackman RW, Kandarian SC. The ubiquitin-protein ligase Nedd4 targets Notch1 in skeletal muscle and distinguishes the subset of atrophies caused by reduced muscle tension. FASEB J 21: 427-437, 2007.
55. Lawler JM, Song W, Kwak HB. Differential response of heat shock proteins to hindlimb unloading and reloading in the soleus. Muscle Nerve 33: 200-207, 2006.
56. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51, 2004.
57. Lee CK, Klopp RG, Weindruch R, Prolla TA. Gene expression profile of aging and its retardation by caloric restriction. Science 285: 1390-1393, 1999.
58. Leeuwenburgh C, Gurley CM, Strotman BA, Dupont-Versteegden EE. Age-related differences in apoptosis with disuse atrophy in soleus muscle. Am J Physiol Regul Integr Comp Physiol 288: R1288-R1296, 2005.
59. Lexell J, Downham D, Larsson Y, Bruhn E, Morsing B. Heavy resistance training in older Scandinavian men and women: short-and long-term effects on arm and leg muscles. J Med Sci Sports 5: 329-341, 1995.
60. Lipman R, Chrisp E, Hazzard D, Bronson R. Pathologic characterization of Brown Norway, Brown Norway X Fischer 344, and Fischer 344 X Brown Norway rats with relation to age. J Gerontol Biol Sci 51A: B54-B59, 1996.
61. Liu Y, Steinacker JM. Changes in skeletal muscle heat shock proteins: pathological significance. Front Biosci 6: D12-D25, 2001.
62. Lohuis TD, Harlow HJ, Beck TD. Hibernating black bears (Ursus americanus) experience skeletal muscle protein balance during winter anorexia. Comp Biochem Physiol B Biochem Mol Biol 147: 20-28, 2007.
63. Lohuis TD, Harlow HJ, Beck TD, Iaizzo PA. Hibernating bears conserve muscle strength and maintain fatigue resistance. Physiol Biochem Zool 80: 257-269, 2007.
64. McCarthy JJ, Fox AM, Tsika GL, Gao L, Tsika RW. -β-MHC transgene expression in suspended and mechanically overloaded/suspended soleus muscle of transgenic mice. Am J Physiol Regul Integr Comp Physiol 272: R1552-R1561, 1997.
65. Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci 57: B359-B365, 2002.
66. Naito H, Powers SK, Demirel HA, Suguira T, Dodd SL, Aoki J. Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats. J Appl Physiol 88: 359-363, 2000.
67. Nikawa T, Ishidoh K, Hirasaka K, Ishihara I, Ikemoto M, Kano M, Kominami E, Nonaka I, Ogawa T, Adams GR, Baldwin KM, Yasui N, Kishi K, Takeda S. Skeletal muscle gene expression in space-flown rats. FASEB J 18: 522-524, 2004.
68. Nishiyama H, Higashitsuji H, Yokoi H, Itoh K, Danno S, Matsuda T, Fujita J. Cloning and characterization of human CIRP (cold-inducible RNA-binding protein) cDNA and chromosomal assignment of the gene. Gene 204: 115-120, 1997.
69. Oishi Y, Ishihara A, Talmadge RJ, Ohira Y, Taniguchi K, Matsumoto H, Roy RR, Edgerton VR. Expression of heat shock protein 72 in atrophied rat skeletal muscles. Acta Physiol Scand 172: 123-130, 2001.
70. Pattison JS, Folk LC, Madsen RW, Booth FW. Identification of differentially expressed genes between young and old rat soleus muscle during recovery from immobilization-induced atrophy. J Appl Physiol 95: 2171-2179, 2003.
71. Pattison JS, Folk LC, Madsen RW, Childs TE, Booth FW. Transcriptional profiling identifies extensive downregulation of extracellular matrix gene expression in sarcopenic rat soleus muscle. Physiol Genomics 15: 34-43, 2003.
72. Pattison JS, Folk LC, Madsen RW, Childs TE, Spangenburg EE, Booth FW. Expression profiling identifies dysregulation of myosin heavy chains IIb and IIx during limb immobilization in the soleus muscles of old rats. J Physiol 553: 357-368, 2003.
73. Phadtare S, Alsina J, Inouye M. Cold-shock response and cold-shock proteins. Curr Opin Microbiol 2: 175-180, 1999.
74. Raffaello A, Laveder P, Romualdi C, Bean C, Toniolo L, Germinario E, Megighian A, Danieli-Betto D, Reggiani C, Lanfranchi G. Denervation in murine fast-twitch muscle: short-term physiological changes and temporal expression profiling. Physiol Genomics 25: 60-74, 2006.
75. Rizwan AN, Burckhardt G. Organic anion transporters of the SLC22 family: biopharmaceutical, physiological, and pathological roles. Pharm Res 24: 450-470, 2007.
76. Roth SM, Ferrell RE, Peters DG, Metter EJ, Hurley BF, Rogers MA. Influence of age, sex, and strength training on human muscle gene expression determined by microarray. Physiol Genomics 10: 181-190, 2002.
77. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155, 2007.
78. Sakurai T, Fujita Y, Ohto E, Oguro A, Atomi Y. The decrease of the cytoskeleton tubulin follows the decrease of the associating molecular chaperone αB-crystallin in unloaded soleus muscle atrophy without stretch. FASEB J 19: 1199-1201, 2005.
79. Salem M, Kenney PB, Rexroad CE, 3rd, Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28: 33-45, 2006.
80. Sato N. A family of cold-regulated RNA-binding protein genes in the cyanobacterium Anabaena variabilis M3. Nucleic Acids Res 23: 2161-2167, 1995.
81. Selsby JT, Dodd SL. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol Regul Integr Comp Physiol 289: R134-R139, 2005.
82. Shavlakadze T, Grounds M. Of bears, frogs, meat, mice and men: complexity of factors affecting skeletal muscle mass and fat. Bioessays 28: 994-1009, 2006.
83. Simard C, Lacaille M, Vallieres J. Effects of hypokinesia/ hypodynamia on contractile and histochemical properties of young and old rat soleus muscle. Exp Neurol 97: 106-114, 1987.
84. Singh MA, Ding W, Manferdi TJ, Solares GR, O'Neill EF, Clements KM, Ryan ND, Kehayias JJ, Fielding RA, Evans WJ. Insulin-like growth factor I in skeletal muscle after weight-lifting exercise in frail elders. Am J Physiol Endocrinol Metab 277: E135-E143, 1999.
85. Siu PM, Pistilli EE, Butler DC, Alway SE. Aging influences the cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol 288: C338-C349, 2005.
86. Smart F, Aschrafi A, Atkins A, Owens GC, Pilotte J, Cunningham BA, Vanderklish PW. Two isoforms of the cold-inducible mRNA-binding protein RBM3 localize to dendrites and promote translation. J Neurochem 101: 1367-1379, 2007.
87. Sonna LA, Fujita J, Gaffin SL, Lilly CM. Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92: 1725-1742, 2002.
88. St-Amand J, Okamura K, Matsumoto K, Shimizu S, Sogawa Y. Characterization of control and immobilized skeletal muscle: an overview from genetic engineering. FASEB J 15: 684-692, 2001.
89. Stevens L, Sultan KR, Peuker H, Gohlsch B, Mounier Y, Pette D. Time-dependent changes in myosin heavy chain mRNA and protein isoforms in unloaded soleus muscle of rat. Am J Physiol Cell Physiol 277: C1044-C1049, 1999.
90. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551: 33-48, 2003.
91. Stump CS, Tipton CM, Henriksen EJ. Muscle adaptations to hindlimb suspension in mature and old Fisher 344 rats. J Appl Physiol 82: 1875-1881, 1997.
92. Sutherland LC, Rintala-Maki ND, White RD, Morin CD. RNA binding motif (RBM) proteins: a novel family of apoptosis modulators? J Cell Biochem 94: 5-24, 2005.
93. Thomason DB, Biggs RB, Booth FW. Protein metabolism and --myosin heavy-chain mRNA in unweighted soleus muscle. Am J Physiol Regul Integr Comp Physiol 257: R300-R305, 1989.
94. Thomason DB, Booth FW. Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68: 1-12, 1990.
95. Thompson LV, Johnson SA, Shoeman JA. Single soleus muscle fiber function after hindlimb unweighting in adult and aged rats. J Appl Physiol 84: 1937-1942, 1998.
96. Thompson LV, Shoeman JA. Contractile function of single muscle fibers after hindlimb unweighting in aged rats. J Appl Physiol 84: 229-235, 1998.
97. Urso ML, Chen YW, Scrimgeour AG, Lee PC, Lee KF, Clarkson PM. Alterations in mRNA expression and protein products following spinal cord injury in humans. J Physiol 579: 877-892, 2007.
98. Urso ML, Clarkson PM, Price TB. Immobilization effects in young and older adults. Eur J Appl Physiol 96: 564-571, 2006.
99. Urso ML, Scrimgeour AG, Chen YW, Thompson PD, Clarkson PM. Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J Appl Physiol 101: 1136-1148, 2006.
100. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research 0034.1- 0034.11, 2002.
101. Vasilaki A, Jackson MJ, McArdle A. Attenuated HSP70 response in skeletal muscle of aged rats following contractile activity. Muscle Nerve 25: 902-905, 2002.
102. Vasilaki A, McArdle F, Iwanejko LM, McArdle A. Adaptive responses of mouse skeletal muscle to contractile activity: the effect of age. Mech Ageing Dev 127: 830-839, 2006.
103. Webster KA. Serine phosphorylation and suppression of apoptosis by the small heat shock protein αB-crystallin. Circ Res 92: 130-132, 2003.
104. Welle S, Brooks A, Thornton CA. Senescence-related changes in gene expression in muscle: similarities and differences between mice and men. Physiol Genomics 5: 67-73, 2001.
105. Welle S, Brooks AI, Delehanty JM, Needler N, Thornton CA. Gene expression profile of aging in human muscle. Physiol Genomics 14: 149-159, 2003.
106. Welle S, Totterman S, Thornton C. Effect of age on muscle hypertrophy induced by resistance training. J Gerontol 51A: M270-M275, 1996.
107. Williams DR, Epperson LE, Li W, Hughes MA, Taylor R, Rogers J, Martin SL, Cossins AR, Gracey AY. Seasonally hibernating phenotype assessed through transcript screening. Physiol Genomics 24: 13-22, 2005.
108. Wittwer M, Fluck M, Hoppeler H, Muller S, Desplanches D, Billeter R. Prolonged unloading of rat soleus muscle causes distinct adaptations of the gene profile. FASEB J 16: 884-886, 2002.
109. Wright EM, Turk E. The sodium/glucose cotransport family SLC5. Pflügers Arch 447: 510-518, 2004.
110. Yan J, Barnes BM, Kohl F, Marr TG. Modulation of gene expression in hibernating arctic ground squirrels. Physiol Genomics 32: 170-181, 2008.
111. Zarzhevsky N, Carmeli E, Fuchs D, Coleman R, Stein H, Reznick AZ. Recovery of muscles of old rats after hindlimb immobilisation by external fixation is impaired compared with those of young rats. Exp Gerontol 36: 125-140, 2001.