Advertisement

HSP, Exercise and Skeletal Muscle

  • Earl G. NobleEmail author
  • C.W. James Melling
  • Kevin J. Milne
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 5)

Abstract

Skeletal muscle, which represents about 40% of the body mass in man, is an integrated organ, which possesses an extensive blood supply and innervations to support groups of muscles and muscle fibers (motor units) which must respond to a wide range of activities. Over the lifespan, skeletal muscle is forced to adapt to a variety of influences including growth and development, aging, hormonal influences, and changes in activity level. In this regard, skeletal muscle expresses the evolutionarily conserved group of proteins known as heat shock proteins (HSP) which may be critical to this adaptive process. Indeed the induction of HSP by the physiologically relevant stimulus of exercise may be harnessed as a means of protecting skeletal muscle and it’s components against a variety of insults. These proteins may also be important in chaperoning muscle remodeling. The following review addresses these issues while simultaneously revealing the paucity of information available on this subject in such an important organ

Keywords

Vasculature motor nerves intracellular signaling adaptation ischemia/reperfusion, hypertrophy atrophy 

Abbreviations

ADP

adenosine diphosphate

ATP

adenosine triphosphate

DNP

2,4-dinitrophenol

ERK

extracellular signal-regulated kinases

GS

glycogen synthase

HSE

heat shock element

HSF1

heat shock factor 1

HSP

heat shock proteins

Hsp70

inducible seventy kilo-dalton heat shock protein

I/R

ischemia/reperfusion

NFATc1

nuclear factor of activated T-cells

PKA

protein kinaseA

ROS

reactive oxygen species

Notes

Acknowledgements

Preparation of this manuscript was made possible by research grants awarded to Dr. E.G. Noble from National Science and Engineering Research Council of Canada (#8170-05) and the Canadian Institutes of Health Research (#CCT- 83029).

References

  1. Abravaya, K., Myers, M.P., Murphy, S.P., and Morimoto, R.I. 1992 The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6: 1153–1164. PM:1628823.PubMedCrossRefGoogle Scholar
  2. Agarraberes, F.A., Terlecky, S.R., and Dice, J.F. 1997 An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J. Cell Biol. 137: 825–834. PM:9151685.PubMedCrossRefGoogle Scholar
  3. Allen, D.L. and Leinwand, L.A. 2002 Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter. J. Biol. Chem. 277: 45323–45330. PM:12235157.PubMedCrossRefGoogle Scholar
  4. Allen, D.L., Linderman, J.K., Roy, R.R., Bigbee, A.J., Grindeland, R.E., Mukku, V., and Edgerton, V.R. 1997 Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am. J. Physiol. 273: C579–C587. PM:9277355.PubMedGoogle Scholar
  5. Allen, D.L., Roy, R.R., and Edgerton, V.R. 1999 Myonuclear domains in muscle adaptation and disease. Muscle Nerve. 22: 1350–1360. PM:10487900.PubMedCrossRefGoogle Scholar
  6. Amrani, M., Latif, N., Morrison, K., Gray, C.C., Jayakumar, J., Corbett, J., Goodwin, A.T., Dunn, M.J., and Yacoub, M.H. 1998 Relative induction of heat shock protein in coronary endothelial cells and cardiomyocytes: implications for myocardial protection. J. Thorac. Cardiovasc. Surg. 115: 200–209. PM:0009451064.PubMedCrossRefGoogle Scholar
  7. Angeletti, B., Pascale, E., Verna, R., Passarelli, F., Butler, R.H., and D‘Ambrosio, E. 1996 Differential expression of heat shock protein (HSP70) mRNAs in rat cells. Exp. Cell Res. 227: 160–164. PM:8806463.PubMedCrossRefGoogle Scholar
  8. Appell, H.J. 1990 Muscular atrophy following immobilization. A review. Sports Med. 10: 42–58. PM:2197699.PubMedCrossRefGoogle Scholar
  9. Arrigo, A.P. 2007 The cellular "networking" of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv. Exp. Med. Biol. 594: 14–26. PM:17205671.PubMedCrossRefGoogle Scholar
  10. Baldwin, J., Snow, R.J., Carey, M.F., and Febbraio, M.A. 1999 Muscle IMP accumulation during fatiguing submaximal exercise in endurance trained and untrained men. Am. J. Physiol. 277: R295–R300. PM:10409285.PubMedGoogle Scholar
  11. Baler, R., Welch, W.J., and Voellmy, R. 1992 Heat shock gene regulation by nascent polypeptides and denatured proteins: HSP70 as a potential autoregulatory factor. J. Cell Biol. 117: 1151–1159. PM:1607379.PubMedCrossRefGoogle Scholar
  12. Batulan, Z., Shinder, G.A., Minotti, S., He, B.P., Doroudchi, M.M., Nalbantoglu, J., Strong, M.J., and Durham, H.D. 2003 High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J. Neurosci. 23: 5789–5798. PM:12843283.PubMedGoogle Scholar
  13. Baumeister, S., Ofer, N., Kleist, C., Terne, P., Opelz, G., Gebhard, M.M., Germann, G., and Heitmann, C. 2004 Reduction of skeletal muscle injury in composite tissue allotransplantation by heat stress preconditioning. Plast. Reconstr. Surg. 114: 1832–1841. PM:15577355.PubMedCrossRefGoogle Scholar
  14. Beckmann, R.P., Mizzen, L.E., and Welch, W.J. 1990 Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 248: 850–854. PM:2188360.PubMedCrossRefGoogle Scholar
  15. Benjamin, I.J., Horie, S., Greenberg, M.L., Alpern, R.J., and Williams, R.S. 1992 Induction of stress proteins in cultured myogenic cells. Molecular signals for the activation of heat shock transcription factor during ischemia. J. Clin. Invest. 89: 1685–1689. PM:1569208.PubMedCrossRefGoogle Scholar
  16. Booth, F.W. and Criswell, D.S. 1997 Molecular events underlying skeletal muscle atrophy and the development of effective countermeasures. Int. J. Sports Med. 18 Suppl 4: S265–S269. PM:9391829.PubMedCrossRefGoogle Scholar
  17. Borisov, A.B. and Carlson, B.M. 2000 Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat. Rec. 258: 305–318. PM:10705351.PubMedCrossRefGoogle Scholar
  18. Bornman, L., Steinmann, C.M., Gericke, G.S., and Polla, B.S. 1998 In vivo heat shock protects rat myocardial mitochondria. Biochem. Biophys. Res. Commun. 246: 836–840. PM:9618299.PubMedCrossRefGoogle Scholar
  19. Bottinelli, R. and Reggiani, C. 2000 Human skeletal muscle fibres: molecular and functional diversity. Prog. Biophys. Mol. Biol. 73: 195–262. PM:10958931.PubMedCrossRefGoogle Scholar
  20. Broome, C.S., Kayani, A.C., Palomero, J., Dillmann, W.H., Mestril, R., Jackson, M.J., and McArdle, A. 2006 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. PM:16723383.PubMedCrossRefGoogle Scholar
  21. Bruton, J.D., Place, N., Yamada, T., Silva, J.P., Andrade, F.H., Dahlstedt, A.J., Zhang, S.J., Katz, A., Larsson, N.G., and Westerblad, H. 2008 Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J. Physiol. 586: 175–184. PM:18006575.PubMedCrossRefGoogle Scholar
  22. Callahan, L.A., She, Z.W., and Nosek, T.M. 2001 Superoxide, hydroxyl radical, and hydrogen peroxide effects on single-diaphragm fiber contractile apparatus. J. Appl. Physiol. 90: 45–54. PM:11133892.PubMedGoogle Scholar
  23. Campisi, J. and Fleshner, M. 2003 Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J. Appl. Physiol. 94: 43–52. PM:12391077.PubMedGoogle Scholar
  24. Campisi, J., Leem, T.H., and Fleshner, M. 2003 Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress. Chaperones. 8: 272–286. PM:14984061.PubMedCrossRefGoogle Scholar
  25. Carroll, S.M., Heilman, S.J., Stremel, R.W., Tobin, G.R., and Barker, J.H. 1997 Vascular delay improves latissimus dorsi muscle perfusion and muscle function for use in cardiomyoplasty. Plast. Reconstr. Surg. 99: 1329–1337. PM:9105360.PubMedCrossRefGoogle Scholar
  26. Carson, L.D. and Korzick, D.H. 2003 Dose-dependent effects of acute exercise on PKC levels in rat heart: is PKC the heart’s prophylactic? Acta Physiol. Scand. 178: 97–106. PM:12780383.PubMedCrossRefGoogle Scholar
  27. Chan, S.H., Wang, L.L., Chang, K.F., Ou, C.C., and Chan, J.Y. 2003 Altered temporal profile of heat shock factor 1 phosphorylation and heat shock protein 70 expression induced by heat shock in nucleus tractus solitarii of spontaneously hypertensive rats. Circulation 107: 339–345. PM:12538438.PubMedCrossRefGoogle Scholar
  28. Chang, J., Knowlton, A.A., Xu, F., and Wasser, J.S. 2001 Activation of the heat shock response: relationship to energy metabolites. A (31)P NMR study in rat hearts. Am. J. Physiol. Heart Circ. Physiol. 280: H426–H433. PM:11123260.PubMedGoogle Scholar
  29. Chatterjee, A., Snead, C., Yetik-Anacak, G., Antonova, G., Zeng, J., and Catravas, J.D. 2008 Heat shock protein 90 inhibitors attenuate LPS-induced endothelial hyperpermeability. Am. J. Physiol. Lung Cell Mol. Physiol. 294: L755–L763. PM:18245267.PubMedCrossRefGoogle Scholar
  30. Chen, Y. and Currie, R.W. 2006 Small interfering RNA knocks down heat shock factor-1 (HSF-1) and exacerbates pro-inflammatory activation of NF-kappaB and AP-1 in vascular smooth muscle cells. Cardiovasc. Res. 69: 66–75. PM:16061216.PubMedCrossRefGoogle Scholar
  31. Chen, Y., Voegeli, T.S., Liu, P.P., Noble, E.G., and Currie, R.W. 2007 Heat shock paradox and a new role of heat shock proteins and their receptors as anti-inflammation targets. Inflamm. Allergy Drug Targets. 6: 91–100. PM:17692032.PubMedCrossRefGoogle Scholar
  32. Chu, B., Soncin, F., Price, B.D., Stevenson, M.A., and Calderwood, S.K. 1996 Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271: 30847–30857. PM:8940068.PubMedCrossRefGoogle Scholar
  33. Connolly, E.M., Kelly, C.J., Chen, G., O‘grady, T., Kay, E., Leahy, A., and Bouchier-Hayes, D.J. 2003 Pharmacological induction of HSP27 attenuates intimal hyperplasia in vivo. Eur. J. Vasc. Endovasc. Surg. 25: 40–47. PM:12525810.PubMedCrossRefGoogle Scholar
  34. Currie, R.W., Karmazyn, M., Kloc, M., and Mailer, K. 1988 Heat-shock response is associated with enhanced postischemic ventricular recovery. Circ. Res. 63: 543–549. PM:3409486.PubMedGoogle Scholar
  35. Dai, R., Frejtag, W., He, B., Zhang, Y., and Mivechi, N.F. 2000 c-Jun NH2-terminal kinase targeting and phosphorylation of heat shock factor-1 suppress its transcriptional activity. J. Biol. Chem. 275: 18210–18218. PM:10747973.PubMedCrossRefGoogle Scholar
  36. Daugaard, M., Jaattela, M., and Rohde, M. 2005 Hsp70-2 is required for tumor cell growth and survival. Cell Cycle. 4: 877–880. PM:15970673.PubMedGoogle Scholar
  37. Davies, K.J., Quintanilha, A.T., Brooks, G.A., and Packer, L. 1982 Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 107: 1198–1205. PM:6291524.PubMedCrossRefGoogle Scholar
  38. Denes, L., Bori, Z., Csonka, E., Entz, L., and Nagy, Z. 2008 Reverse regulation of endothelial cells and myointimal hyperplasia on cell proliferation by a heatshock protein-coinducer after hypoxia. Stroke 39: 1022–1024. PM:18239173.PubMedCrossRefGoogle Scholar
  39. Dunn, S.E., Simard, A.R., Bassel-Duby, R., Williams, R.S., and Michel, R.N. 2001 Nerve activity-dependent modulation of calcineurin signaling in adult fast and slow skeletal muscle fibers. J. Biol. Chem. 276: 45243–45254. PM:11555650.PubMedCrossRefGoogle Scholar
  40. Edwards, R.H., Hill, D.K., Jones, D.A., and Merton, P.A. 1977 Fatigue of long duration in human skeletal muscle after exercise. J. Physiol. 272: 769–778. PM:592214.PubMedGoogle Scholar
  41. Egginton, S., Zhou, A.L., Brown, M.D., and Hudlicka, O. 2001 Unorthodox angiogenesis in skeletal muscle. Cardiovasc. Res. 49: 634–646. PM:11166277.PubMedCrossRefGoogle Scholar
  42. Ellis, S., Killender, M., and Anderson, R.L. 2000 Heat-induced alterations in the localization of HSP72 and HSP73 as measured by indirect immunohistochemistry and immunogold electron microscopy. J. Histochem. Cytochem. 48: 321–332. PM:10681386.PubMedGoogle Scholar
  43. Essig, D.A. and Nosek, T.M. 1997 Muscle fatigue and induction of stress protein genes: a dual function of reactive oxygen species? Can. J. Appl. Physiol. 22: 409–428.PubMedGoogle Scholar
  44. Feasson, L., Stockholm, D., Freyssenet, D., Richard, I., Duguez, S., Beckmann, J.S., and Denis, C. 2002 Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J. Physiol. 543: 297–306. PM:12181300.PubMedCrossRefGoogle Scholar
  45. Febbraio, M.A. and Koukoulas, I. 2000 HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J. Appl. Physiol. 89: 1055–1060. PM:0010956350.PubMedGoogle Scholar
  46. Febbraio, M.A., Steensberg, A., Walsh, R., Koukoulas, I., van, H.G., Saltin, B., and Pedersen, B.K. 2002 Reduced glycogen availability is associated with an elevation in HSP72 in contracting human skeletal muscle. J. Physiol. 538: 911–917. PM:11826174.PubMedCrossRefGoogle Scholar
  47. Feder, M.E. and Hofmann, G.E. 1999 Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243–282. PM:0010099689.PubMedCrossRefGoogle Scholar
  48. Fehrenbach, E., Niess, A.M., Schlotz, E., Passek, F., Dickhuth, H.H., and Northoff, H. 2000 Transcriptional and translational regulation of heat shock proteins in leukocytes of endurance runners. J. Appl. Physiol. 89: 704–710. PM:0010926657.PubMedGoogle Scholar
  49. Ficker, E., Dennis, A.T., Wang, L., and Brown, A.M. 2003 Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ. Res. 92: e87–e100. PM:12775586.PubMedCrossRefGoogle Scholar
  50. Fischer, C.P., Hiscock, N.J., Basu, S., Vessby, B., Kallner, A., Sjoberg, L.B., Febbraio, M.A., and Pedersen, B.K. 2006 Vitamin E isoform-specific inhibition of the exercise-induced heat shock protein 72 expression in humans. J. Appl. Physiol. 100: 1679–1687. PM:16384840.PubMedCrossRefGoogle Scholar
  51. Flanagan, S.W., Ryan, A.J., Gisolfi, C.V., and Moseley, P.L. 1995 Tissue-specific HSP70 response in animals undergoing heat stress. Am. J. Physiol. 268: R28–R32. PM:7840333.PubMedGoogle Scholar
  52. Francis, G.S., Goldsmith, S.R., Ziesche, S.M., and Cohn, J.N. 1982 Response of plasma norepinephrine and epinephrine to dynamic exercise in patients with congestive heart failure. Am. J. Cardiol. 49: 1152–1156. PM:7064841.PubMedCrossRefGoogle Scholar
  53. Fritsch, M. and Wu, C. 1999 Phosphorylation of Drosophila heat shock transcription factor. Cell Stress Chaperones. 4: 102–117. PM:10547060.PubMedCrossRefGoogle Scholar
  54. Gardiner, P.F. 2001. Neuromuscular aspects of physical activity. Human Kinetics, Champaign, IL. pp. 1–256.Google Scholar
  55. Gardiner, P., Beaumont, E., and Cormery, B. 2005 Motoneurones "learn" and "forget" physical activity. Can. J. Appl. Physiol. 30: 352–370. PM:16129890.PubMedGoogle Scholar
  56. Gjovaag, T.F. and Dahl, H.A. 2006 Effect of training and detraining on the expression of heat shock proteins in m. triceps brachii of untrained males and females. Eur. J. Appl. Physiol. 98: 310–322. PM:16924527.PubMedCrossRefGoogle Scholar
  57. Gjovaag, T.F., Vikne, H., and Dahl, H.A. 2006 Effect of concentric or eccentric weight training on the expression of heat shock proteins in m. biceps brachii of very well trained males. Eur. J. Appl. Physiol. 96: 355–362. PM:16284787.PubMedCrossRefGoogle Scholar
  58. Glick, B.S. 1995 Can Hsp70 proteins act as force-generating motors? Cell 80: 11–14. PM:7813006.PubMedCrossRefGoogle Scholar
  59. Golenhofen, N., Perng, M.D., Quinlan, R.A., and Drenckhahn, D. 2004 Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem. Cell Biol. 122: 415–425. PM:15480735.PubMedCrossRefGoogle Scholar
  60. Gollnick, P.D., Piehl, K., and Saltin, B. 1974 Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J. Physiol. 241: 45–57. PM:4278539.PubMedGoogle Scholar
  61. Gonzalez, B., Hernando, R., and Manso, R. 2000 Stress proteins of 70 kDa in chronically exercised skeletal muscle. Pflugers Arch. 440: 42–49. PM:0010863996.PubMedCrossRefGoogle Scholar
  62. Gonzalez, B. and Manso, R. 2004 Induction, modification and accumulation of HSP70s in the rat liver after acute exercise: early and late responses. J. Physiol. 556: 369–385. PM:14754995.PubMedCrossRefGoogle Scholar
  63. Grondard, C., Biondi, O., Pariset, C., Lopes, P., Deforges, S., Lecolle, S., Gaspera, B.D., Gallien, C.L., Chanoine, C., and Charbonnier, F. 2008 Exercise-induced modulation of calcineurin activity parallels the time course of myofibre transitions. J. Cell Physiol. 214: 126–135. PM:17559060.PubMedCrossRefGoogle Scholar
  64. Guan, X., Dei-Anane, G., Liang, R., Gross, M.L., Nickkholgh, A., Kern, M., Ludwig, J., Zeier, M., Buchler, M.W., Schmidt, J., and Schemmer, P. 2008 Donor preconditioning with taurine protects kidney grafts from injury after experimental transplantation. J. Surg. Res. 146: 127–134. PM:18061615.PubMedCrossRefGoogle Scholar
  65. Harder, Y., Amon, M., Schramm, R., Georgi, M., Banic, A., Erni, D., and Menger, M.D. 2005 Heat shock preconditioning reduces ischemic tissue necrosis by heat shock protein (HSP)-32-mediated improvement of the microcirculation rather than induction of ischemic tolerance. Ann. Surg. 242: 869–878. discussion. PM:16327497.PubMedCrossRefGoogle Scholar
  66. Hedges, J.C., Dechert, M.A., Yamboliev, I.A., Martin, J.L., Hickey, E., Weber, L.A., and Gerthoffer, W.T. 1999 A role for p38(MAPK)/HSP27 pathway in smooth muscle cell migration. J. Biol. Chem. 274: 24211–24219. PM:10446196.PubMedCrossRefGoogle Scholar
  67. Hennig, R. and Lomo, T. 1985 Firing patterns of motor units in normal rats. Nature 314: 164–166. PM:3974720.PubMedCrossRefGoogle Scholar
  68. Hernando, R. and Manso, R. 1997 Muscle fibre stress in response to exercise: synthesis, accumulation and isoform transitions of 70-kDa heat-shock proteins. Eur. J. Biochem. 243: 460–467. PM:9030773.PubMedCrossRefGoogle Scholar
  69. Heydari, A.R., You, S., Takahashi, R., Gutsmann-Conrad, A., Sarge, K.D., and Richardson, A. 2000 Age-related alterations in the activation of heat shock transcription factor 1 in rat hepatocytes. Exp. Cell Res. 256: 83–93. PM:10739655.PubMedCrossRefGoogle Scholar
  70. Hirano, S., Rees, R.S., Yancy, S.L., Welsh, M.J., Remick, D.G., Yamada, T., Hata, J., and Gilmont, R.R. 2004 Endothelial barrier dysfunction caused by LPS correlates with phosphorylation of HSP27 in vivo. Cell Biol. Toxicol. 20: 1–14. PM:15119843.PubMedCrossRefGoogle Scholar
  71. Holmberg, C.I., Hietakangas, V., Mikhailov, A., Rantanen, J.O., Kallio, M., Meinander, A., Hellman, J., Morrice, N., MacKintosh, C., Morimoto, R.I., Eriksson, J.E., and Sistonen, L. 2001 Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20: 3800–3810. PM:11447121.PubMedCrossRefGoogle Scholar
  72. Holmgren, R., Corces, V., Morimoto, R., Blackman, R., and Meselson, M. 1981 Sequence homologies in the 5' regions of four Drosophila heat-shock genes. Proc. Natl. Acad. Sci. U. S. A. 78: 3775–3778. PM:6791161.PubMedCrossRefGoogle Scholar
  73. Hoogeveen, J.F., Troost, D., van der Kracht, A.H., Wondergem, J., Haveman, J., and Gonzalez, G.D. 1993 Ultrastructural changes in the rat sciatic nerve after local hyperthermia. Int. J. Hyperthermia. 9: 723–730. PM:8245583.PubMedCrossRefGoogle Scholar
  74. Hoogeveen, J.F., Troost, D., Wondergem, J., van der Kracht, A.H., and Haveman, J. 1992 Hyperthermic injury versus crush injury in the rat sciatic nerve: a comparative functional, histopathological and morphometrical study. J. Neurol. Sci. 108: 55–64. PM:1624953.PubMedCrossRefGoogle Scholar
  75. Hsu, C.C., Hsu, M.C., Huang, M.S., Chen, C.S., Shiang, T.Y., Wang, C.H., Chen, T., and Su, B. 2005 The HSP expression of passive repetitive plyometric trained skeletal muscle. Res. Commun. Mol. Pathol. Pharmacol. 117–118: 91–103. PM:18426081.PubMedGoogle Scholar
  76. Huerta-Bahena, J., Villalobos-Molina, R., and Garcia-Sainz, J.A. 1983 Roles of alpha 1- and beta-adrenergic receptors in adrenergic responsiveness of liver cells formed after partial hepatectomy. Biochim. Biophys. Acta. 763: 112–119. PM:6311281.PubMedCrossRefGoogle Scholar
  77. Huey, K.A., Thresher, J.S., Brophy, C.M., and Roy, R.R. 2004 Inactivity-induced modulation of Hsp20 and Hsp25 content in rat hindlimb muscles. Muscle Nerve. 30: 95–101. PM:15221884.PubMedCrossRefGoogle Scholar
  78. Hung, J.J., Cheng, T.J., Lai, Y.K., and Chang, M.D. 1998 Differential activation of p38 mitogen-activated protein kinase and extracellular signal-regulated protein kinases confers cadmium-induced HSP70 expression in 9L rat brain tumor cells. J. Biol. Chem. 273: 31924–31931. PM:9822662.PubMedCrossRefGoogle Scholar
  79. Ikeda, T., Ikenoue, T., Xia, X.Y., and Xia, Y.X. 2000 Important role of 72-kd heat shock protein expression in the endothelial cell in acquisition of hypoxic-ischemic tolerance in the immature rat. Am. J. Obstet. Gynecol. 182: 380–386. PM:10694341.PubMedCrossRefGoogle Scholar
  80. Ikeyama, S., Kusumoto, K., Miyake, H., Rokutan, K., and Tashiro, S. 2001 A non-toxic heat shock protein 70 inducer, geranylgeranylacetone, suppresses apoptosis of cultured rat hepatocytes caused by hydrogen peroxide and ethanol. J. Hepatol. 35: 53–61. PM:11495042.PubMedCrossRefGoogle Scholar
  81. Inaguma, Y., Hasegawa, K., Goto, S., Ito, H., and Kato, K. 1995 Induction of the synthesis of hsp27 and alpha B crystallin in tissues of heat-stressed rats and its suppression by ethanol or an alpha 1-adrenergic antagonist. J. Biochem. 117: 1238–1243. PM:7490266.PubMedGoogle Scholar
  82. Ivy, J.L. and Kuo, C.H. 1998 Regulation of GLUT4 protein and glycogen synthase during muscle glycogen synthesis after exercise. Acta Physiol. Scand. 162: 295–304. PM:9578375.PubMedCrossRefGoogle Scholar
  83. Jaattela, M. 1999 Escaping cell death: survival proteins in cancer. Exp. Cell Res. 248: 30–43. PM:10094811.PubMedCrossRefGoogle Scholar
  84. Jensen, J., Brors, O., and Dahl, H.A. 1995 Different beta-adrenergic receptor density in different rat skeletal muscle fibre types. Pharmacol. Toxicol. 76: 380–385. PM:7479580.PubMedCrossRefGoogle Scholar
  85. Johnson, A.D., Berberian, P.A., Tytell, M., and Bond, M.G. 1995 Differential distribution of 70-kD heat shock protein in atherosclerosis. Its potential role in arterial SMC survival. Arterioscler. Thromb. Vasc. Biol. 15: 27–36. PM:7749813.PubMedGoogle Scholar
  86. Johnson, J.D., Campisi, J., Sharkey, C.M., Kennedy, S.L., Nickerson, M., and Fleshner, M. 2005 Adrenergic receptors mediate stress-induced elevations in extracellular Hsp72. J. Appl. Physiol. 99: 1789–1795. PM:16037404.PubMedCrossRefGoogle Scholar
  87. Joyeux, M., Baxter, G.F., Thomas, D.L., Ribuot, C., and Yellon, D.M. 1997 Protein kinase C is involved in resistance to myocardial infarction induced by heat stress. J Mol Cell Cardiol. 29: 3311–3319. PM:9441837.PubMedCrossRefGoogle Scholar
  88. Joyner, M.J. and Wilkins, B.W. 2007 Exercise hyperaemia: is anything obligatory but the hyperaemia? J. Physiol. 583: 855–860. PM:17640934.PubMedCrossRefGoogle Scholar
  89. Jurivich, D.A., Sistonen, L., Kroes, R.A., and Morimoto, R.I. 1992 Effect of sodium salicylate on the human heat shock response. Science 255: 1243–1245. PM:1546322.PubMedCrossRefGoogle Scholar
  90. Kawano, F., Matsuoka, Y., Oke, Y., Higo, Y., Terada, M., Wang, X.D., Nakai, N., Fukuda, H., Imajoh-Ohmi, S., and Ohira, Y. 2007 Role(s) of nucleoli and phosphorylation of ribosomal protein S6 and/or HSP27 in the regulation of muscle mass. Am. J. Physiol. Cell Physiol. 293: C35–C44. PM:17182729.PubMedCrossRefGoogle Scholar
  91. Kayani, A.C., Close, G.L., Jackson, M.J., and McArdle, A. 2008 Prolonged treadmill training increases HSP70 in skeletal muscle but does not affect age-related functional deficits. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294: R568–R576. PM:17989141.PubMedGoogle Scholar
  92. Keezer, S.M., Ivie, S.E., Krutzsch, H.C., Tandle, A., Libutti, S.K., and Roberts, D.D. 2003 Angiogenesis inhibitors target the endothelial cell cytoskeleton through altered regulation of heat shock protein 27 and cofilin. Cancer Res. 63: 6405–6412. PM:14559830.PubMedGoogle Scholar
  93. Kelly, D.A., Tiidus, P.M., Houston, M.E., and Noble, E.G. 1996 Effect of vitamin E deprivation and exercise training on induction of HSP70. J. Appl. Physiol. 81: 2379–2385.PubMedGoogle Scholar
  94. Khassaf, M., McArdle, A., Esanu, C., Vasilaki, A., McArdle, F., Griffiths, R.D., Brodie, D.A., and Jackson, M.J. 2003 Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J. Physiol. PM:12692182.Google Scholar
  95. Kim, J., Nueda, A., Meng, Y.H., Dynan, W.S., and Mivechi, N.F. 1997 Analysis of the phosphorylation of human heat shock transcription factor-1 by MAP kinase family members. J. Cell Biochem. 67: 43–54. PM:9328838.PubMedCrossRefGoogle Scholar
  96. Kjaer, M. 2004 Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84: 649–698. PM:15044685.PubMedCrossRefGoogle Scholar
  97. Klose, M.K., Atwood, H.L., and Robertson, R.M. 2008 Hyperthermic preconditioning of presynaptic calcium regulation in Drosophila. J. Neurophysiol. 99: 2420–2430. PM:18272873.PubMedCrossRefGoogle Scholar
  98. Koh, T.J. and Escobedo, J. 2004 Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions. Am. J. Physiol. Cell Physiol. 286: C713–C722. PM:14627610.PubMedCrossRefGoogle Scholar
  99. Kurucz, I., Morva, A., Vaag, A., Eriksson, K.F., Huang, X., Groop, L., and Koranyi, L. 2002 Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51: 1102–1109. PM:11916932.PubMedCrossRefGoogle Scholar
  100. Lai, H.C., Liu, T.J., Ting, C.T., Yang, J.Y., Huang, L., Wallace, D., Kaiser, P., and Wang, P.H. 2007 Regulation of IGF-I receptor signaling in diabetic cardiac muscle: dysregulation of cytosolic and mitochondria HSP60. Am. J. Physiol. Endocrinol. Metab. 292: E292–E297. PM:16985260.PubMedCrossRefGoogle Scholar
  101. Lakshmikuttyamma, A., Selvakumar, P., Anderson, D.H., Datla, R.S., and Sharma, R.K. 2004 Molecular cloning of bovine cardiac muscle heat-shock protein 70 kDa and its phosphorylation by cAMP-dependent protein kinase in vitro. Biochemistry 43: 13340–13347. PM:15491140.PubMedCrossRefGoogle Scholar
  102. Lattouf, J.B., Srinivasan, R., Pinto, P.A., Linehan, W.M., and Neckers, L. 2006 Mechanisms of disease: the role of heat-shock protein 90 in genitourinary malignancy. Nat. Clin. Pract. Urol. 3: 590–601. PM:17088927.PubMedCrossRefGoogle Scholar
  103. Lee, C.E., McArdle, A., and Griffiths, R.D. 2007. The role of hormones, cytokines and heat shock proteins during age-related muscle loss. Clin. Nutr. 26: 524–534. PM:17590243.Google Scholar
  104. Lee, K., Park, J.Y., Yoo, W., Gwag, T., Lee, J.W., Byun, M.W., and Choi, I. 2008 Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: proteomic and molecular assessment. J. Cell Biochem. 104: 642–656. PM:18181155.PubMedCrossRefGoogle Scholar
  105. Leger, J.P., Smith, F.M., and Currie, R.W. 2000 Confocal microscopic localization of constitutive and heat shock- induced proteins HSP70 and HSP27 in the rat heart. Circulation 102: 1703–1709. PM:11015351.PubMedGoogle Scholar
  106. Lepore, D.A., Hurley, J.V., Stewart, A.G., Morrison, W.A., and Anderson, R.L. 2000 Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle Nerve. 23: 1847–1855. PM:0011102908.PubMedCrossRefGoogle Scholar
  107. Lepore, D.A. and Morrison, W.A. 2000 Ischemic preconditioning: lack of delayed protection against skeletal muscle ischemia-reperfusion. Microsurgery 20: 350–355. PM:11119291.PubMedCrossRefGoogle Scholar
  108. Lille, S., Su, C.Y., Schoeller, T., Suchy, H., Lyons, S., Russell, R.C., Neumeister, M., and Lai, C.C. 1999 Induction of heat-shock protein 72 in rat skeletal muscle does not increase tolerance to ischemia-reperfusion injury. Muscle Nerve. 22: 390–393. PM:0010086900.PubMedCrossRefGoogle Scholar
  109. Liu, Y., Gampert, L., Nething, K., and Steinacker, J.M. 2006 Response and function of skeletal muscle heat shock protein 70. Front Biosci. 11: 2802–2827. PM:16720354.PubMedCrossRefGoogle Scholar
  110. Liu, Y., Lormes, W., Baur, C., Opitz-Gress, A., Altenburg, D., Lehmann, M., and Steinacker, J.M. 2000 Human skeletal muscle HSP70 response to physical training depends on exercise intensity. Int. J. Sports Med. 21: 351–355. PM:0010950444.PubMedCrossRefGoogle Scholar
  111. Locke, M. 2007 Heat shock protein accumulation and heat shock transcription factor activation in rat skeletal muscle during compensatory hypertrophy. Acta Physiol. (Oxf). PM:17973955.Google Scholar
  112. Locke, M., Atkinson, B.G., Tanguay, R.M., and Noble, E.G. 1994 Shifts in type I fiber proportion in rat hindlimb muscle are accompanied by changes in HSP72 content. Am. J. Physiol. 266: C1240–C1246.PubMedGoogle Scholar
  113. Locke, M., Noble, E.G., and Atkinson, B.G. 1990 Exercising mammals synthesize stress proteins. Am. J. Physiol. 258: C723–C729.PubMedGoogle Scholar
  114. Locke, M., Noble, E.G., and Atkinson, B.G. 1991 Inducible isoform of HSP70 is constitutively expressed in a muscle fiber type specific pattern. Am. J. Physiol. 261: C774–C779. PM:0001951668.PubMedGoogle Scholar
  115. Locke, M., Noble, E.G., Tanguay, R.M., Feild, M.R., Ianuzzo, S.E., and Ianuzzo, C.D. 1995 Activation of heat-shock transcription factor in rat heart after heat shock and exercise. Am. J. Physiol. 268: C1387–C1394. PM:7611357.PubMedGoogle Scholar
  116. Locke, M. and Tanguay, R.M. 1996 Increased HSF activation in muscles with a high constitutive Hsp70 expression. Cell Stress Chaperones. 1: 189–196. PM:9222604.PubMedCrossRefGoogle Scholar
  117. Loktionova, S.A. and Kabakov, A.E. 1998 Protein phosphatase inhibitors and heat preconditioning prevent Hsp27 dephosphorylation, F-actin disruption and deterioration of morphology in ATP-depleted endothelial cells. FEBS Lett. 433: 294–300. PM:9744814.PubMedCrossRefGoogle Scholar
  118. Long, Y.C. and Zierath, J.R. 2008 Influence of AMP-activated protein kinase and calcineurin on metabolic networks in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. PM:18544643.Google Scholar
  119. Maglara, A.A., Vasilaki, A., Jackson, M.J., and McArdle, A. 2003. Damage to developing mouse skeletal muscle myotubes in culture: protective effect of heat shock proteins. J. Physiol. 548: 837–846. PM:12598587.PubMedCrossRefGoogle Scholar
  120. Markuns, J.F., Wojtaszewski, J.F., and Goodyear, L.J. 1999 Insulin and exercise decrease glycogen synthase kinase-3 activity by different mechanisms in rat skeletal muscle. J. Biol. Chem. 274: 24896–24900. PM:0010455163.PubMedCrossRefGoogle Scholar
  121. Marshall, J.M. 1982 The influence of the sympathetic nervous system on individual vessels of the microcirculation of skeletal muscle of the rat. J. Physiol. 332: 169–186. PM:7153926.PubMedGoogle Scholar
  122. Martin, W.H., III, Coggan, A.R., Spina, R.J., and Saffitz, J.E. 1989 Effects of fiber type and training on beta-adrenoceptor density in human skeletal muscle. Am. J. Physiol. 257: E736–E742. PM:2556938.PubMedGoogle Scholar
  123. Martinez, J.A., Tavarez, J.J., Oliveira, C.M., and Banerjee, D.K. 2006 Potentiation of angiogenic switch in capillary endothelial cells by cAMP: A cross-talk between up-regulated LLO biosynthesis and the HSP-70 expression. Glycoconj. J. 23: 209–220. PM:16691504.PubMedCrossRefGoogle Scholar
  124. Matsumoto, K., Honda, K., and Kobayashi, N. 2001 Protective effect of heat preconditioning of rat liver graft resulting in improved transplant survival. Transplantation 71: 862–868. PM:11349717.PubMedCrossRefGoogle Scholar
  125. Mattson, M.P., Duan, W., Wan, R., and Guo, Z. 2004 Prophylactic activation of neuroprotective stress response pathways by dietary and behavioral manipulations. NeuroRx 1: 111–116. PM:15717011.PubMedCrossRefGoogle Scholar
  126. McArdle, A., Broome, C.S., Kayani, A.C., Tully, M.D., Close, G.L., Vasilaki, A., and Jackson, M.J. 2006 HSF expression in skeletal muscle during myogenesis: implications for failed regeneration in old mice. Exp. Gerontol. 41: 497–500. PM:16580804.PubMedCrossRefGoogle Scholar
  127. McCormick, P.H., Chen, G., Tierney, S., Kelly, C.J., and Bouchier-Hayes, D.J. 2003 Clinically applicable thermal preconditioning attenuates leukocyte-endothelial interactions. J. Am. Coll. Surg. 197: 71–78. PM:12831927.PubMedCrossRefGoogle Scholar
  128. Melkani, G.C., Cammarato, A., and Bernstein, S.I. 2006 alphaB-crystallin maintains skeletal muscle myosin enzymatic activity and prevents its aggregation under heat-shock stress. J. Mol. Biol. 358: 635–645. PM:16546210.PubMedCrossRefGoogle Scholar
  129. Melling, C.W., Krause, M.P., and Noble, E.G. 2006 PKA-mediated ERK1/2 inactivation and hsp70 gene expression following exercise. J. Mol. Cell Cardiol. 41: 816–822. PM:16806261.PubMedCrossRefGoogle Scholar
  130. Melling, C.W., Thorp, D.B., Milne, K.J., Krause, M.P., and Noble, E.G. 2007 Exercise-mediated regulation of Hsp70 expression following aerobic exercise training. Am. J. Physiol. Heart Circ. Physiol. 293: H3692–H3698. PM:17921326.PubMedCrossRefGoogle Scholar
  131. Melling, C.J.W., Thorp, D.B., Milne, K.J., and Noble, E.G. 2009 Myocardial Hsp70 phosphorylation and PKC-mediated cardioprotection following exercise. Cell Stress Chaperones 14: 141–150.PubMedCrossRefGoogle Scholar
  132. Melling, C.W., Thorp, D.B., and Noble, E.G. 2004 Regulation of myocardial heat shock protein 70 gene expression following exercise. J. Mol. Cell Cardiol. 37: 847–855. PM:15380675.PubMedCrossRefGoogle Scholar
  133. Meng, X., Brown, J.M., Ao, L., Banerjee, A., and Harken, A.H. 1996 Norepinephrine induces cardiac heat shock protein 70 and delayed cardioprotection in the rat through alpha 1 adrenoceptors. Cardiovasc. Res. 32: 374–383. PM:8796125.PubMedCrossRefGoogle Scholar
  134. Milkiewicz, M., Doyle, J.L., Fudalewski, T., Ispanovic, E., Aghasi, M., and Haas, T.L. 2007 HIF-1alpha and HIF-2alpha play a central role in stretch-induced but not shear-stress-induced angiogenesis in rat skeletal muscle. J. Physiol. 583: 753–766. PM:17627993.PubMedCrossRefGoogle Scholar
  135. Milne, K.J. and Noble, E.G. 2002 Exercise-induced elevation of HSP70 is intensity dependent. J. Appl. Physiol. 93: 561–568. PM:12133865.PubMedGoogle Scholar
  136. Milne, K.J. and Noble, E.G. 2007 Response of the myocardium to exercise: sex-specific regulation of Hsp70. Med. Sci. Sports Exerc. 40: 655–663.Google Scholar
  137. Morton, J.P., MacLaren, D.P., Cable, N.T., Bongers, T., Griffiths, R.D., Campbell, I.T., Evans, L., Kayani, A., McArdle, A., and Drust, B. 2006 Time course and differential responses of the major heat shock protein families in human skeletal muscle following acute nondamaging treadmill exercise. J. Appl. Physiol. 101: 176–182. PM:16565353.PubMedCrossRefGoogle Scholar
  138. Morton, J.P., MacLaren, D.P., Cable, N.T., Campbell, I.T., Evans, L., Bongers, T., Griffiths, R.D., Kayani, A.C., McArdle, A., and Drust, B. 2007 Elevated core and muscle temperature to levels comparable to exercise do not increase heat shock protein content of skeletal muscle of physically active men. Acta Physiol. (Oxf). 190: 319–327. PM:17488245.CrossRefGoogle Scholar
  139. Morton, J.P., MacLaren, D.P., Cable, N.T., Campbell, I.T., Evans, L., Kayani, A.C., McArdle, A., and Drust, B. 2008 Trained men display increased basal heat shock protein content of skeletal muscle. Med. Sci. Sports Exerc. 40: 1255–1262. PM:18580405.PubMedCrossRefGoogle Scholar
  140. Moseley, P.L. 2000 Exercise, stress, and the immune conversation. Exerc. Sport Sci. Rev. 28: 128–132. PM:10916705.PubMedGoogle Scholar
  141. Murashov, A.K., Talebian, S., and Wolgemuth, D.J. 1998 Role of heat shock protein Hsp25 in the response of the orofacial nuclei motor system to physiological stress. Brain Res. Mol. Brain Res. 63: 14–24. PM:9838025.PubMedCrossRefGoogle Scholar
  142. Murlasits, Z., Cutlip, R.G., Geronilla, K.B., Rao, K.M., Wonderlin, W.F., and Alway, S.E. 2006 Resistance training increases heat shock protein levels in skeletal muscle of young and old rats. Exp. Gerontol. 41: 398–406. PM:16524679.PubMedCrossRefGoogle Scholar
  143. Mutungi, G. 2008 The expression of NFATc1 in adult rat skeletal muscle fibres. Exp. Physiol. 93: 399–406. PM:17965140.PubMedCrossRefGoogle Scholar
  144. Nader, G.A. and Esser, K.A. 2001 Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J. Appl. Physiol. 90: 1936–1942. PM:11299288.PubMedGoogle Scholar
  145. Naito, H., Powers, S.K., Demirel, H.A., Sugiura, T., Dodd, S.L., and Aoki, J. 2000 Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats. J. Appl. Physiol. 88: 359–363. PM:0010642402.PubMedGoogle Scholar
  146. Najemnikova, E., Rodgers, C.D., and Locke, M. 2007 Altered heat stress response following streptozotocin-induced diabetes. Cell Stress. Chaperones. 12: 342–352. PM:18229453.PubMedCrossRefGoogle Scholar
  147. Neschis, D.G., Safford, S.D., Raghunath, P.N., Langer, D.J., David, M.L., Hanna, A.K., Tomaszewski, J.E., Kariko, K., Barnathan, E.S., and Golden, M.A. 1998 Thermal preconditioning before rat arterial balloon injury: limitation of injury and sustained reduction of intimal thickening. Arterioscler. Thromb. Vasc. Biol. 18: 120–126. PM:9445265.PubMedGoogle Scholar
  148. Nguyen, V.T. and Bensaude, O. 1994 Increased thermal aggregation of proteins in ATP-depleted mammalian cells. Eur. J. Biochem. 220: 239–246. PM:7907018.PubMedCrossRefGoogle Scholar
  149. Noble, E.G. 2002 Heat shock proteins and their induction with exercise. In: Exercise and Stress Response: Role of Stress Proteins. (eds. M. Locke and E.G. Noble). CRC Press. Boca Raton, Florida. pp. 43–78.Google Scholar
  150. Noble, E.G., Milne, K.J., and Melling, C.J.W. 2008. Heat shock proteins and exercise: A primer. Appl. Physiol. Nutr. Metab. 33: 1050–1065.Google Scholar
  151. Nosek, T.M., Brotto, M.A., Essig, D.A., Mestril, R., Conover, R.C., Dillmann, W.H., and Kolbeck, R.C. 2000 Functional properties of skeletal muscle from transgenic animals with upregulated heat shock protein 70. Physiol. Genomics. 4: 25–33. PM:0011074010.PubMedGoogle Scholar
  152. Ogata, T., Oishi, Y., Roy, R.R., and Ohmori, H. 2003 Endogenous expression and developmental changes of HSP72 in rat skeletal muscles. J. Appl. Physiol. 95: 1279–1286. PM:12909603.PubMedGoogle Scholar
  153. Ogata, T., Oishi, Y., Roy, R.R., and Ohmori, H. 2005 Effects of T3 treatment on HSP72 and calcineurin content of functionally overloaded rat plantaris muscle. Biochem. Biophys. Res. Commun. 331: 1317–1323. PM:15883019.PubMedCrossRefGoogle Scholar
  154. Oguro, A., Sakurai, T., Fujita, Y., Lee, S., Kubota, H., Nagata, K., and Atomi, Y. 2006 The molecular chaperone HSP47 rapidly senses gravitational changes in myoblasts. Genes Cells. 11: 1253–1265. PM:17054723.PubMedCrossRefGoogle Scholar
  155. Ohnishi, K., Wang, X., Takahashi, A., Matsumoto, H., and Ohnishi, T. 1999 The protein kinase inhibitor, H-7, suppresses heat induced activation of heat shock transcription factor 1. Mol. Cell Biochem. 197: 129–135. PM:10485332.PubMedCrossRefGoogle Scholar
  156. Oishi, Y., Imoto, K., Ogata, T., Taniguchi, K., Matsumoto, H., Fukuoka, Y., and Roy, R.R. 2004 Calcineurin and heat-shock proteins modulation in clenbuterol-induced hypertrophied rat skeletal muscles. Pflugers Arch. 448: 114–122. PM:14758479.PubMedCrossRefGoogle Scholar
  157. Oishi, Y., Ogata, T., Yamamoto, K.I., Terada, M., Ohira, T., Ohira, Y., Taniguchi, K., and Roy, R.R. 2008 Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiol. (Oxf). 192: 381–395. PM:17892520.CrossRefGoogle Scholar
  158. Oishi, Y., Taniguchi, K., Matsumoto, H., Ishihara, A., Ohira, Y., and Roy, R.R. 2002 Muscle type-specific response of HSP60, HSP72, and HSC73 during recovery after elevation of muscle temperature. J. Appl. Physiol. 92: 1097–1103. PM:11842045.PubMedGoogle Scholar
  159. O‘Neill, D.E., Aubrey, F.K., Zeldin, D.A., Michel, R.N., and Noble, E.G. 2006 Slower skeletal muscle phenotypes are critical for constitutive expression of Hsp70 in overloaded rat plantaris muscle. J. Appl. Physiol. 100: 981–987. PM:16293703.PubMedCrossRefGoogle Scholar
  160. O‘Neill, D.E. and Noble, E.G. 2004 Constitutive expression of inducible Hsp70 is linked to natural shifts in skeletal muscle phenotype. Acta Physiol. Scand. 181: 35–41. PM:15086450.PubMedCrossRefGoogle Scholar
  161. Palleros, D.R., Welch, W.J., and Fink, A.L. 1991 Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding. Proc. Natl. Acad. Sci. U. S. A. 88: 5719–5723. PM:1829527.PubMedCrossRefGoogle Scholar
  162. Paroo, Z., Haist, J.V., Karmazyn, M., and Noble, E.G. 2002 Exercise improves postischemic cardiac function in males but not females: consequences of a novel sex-specific heat shock protein 70 response. Circ. Res. 90: 911–917. PM:11988493.PubMedCrossRefGoogle Scholar
  163. Paroo, Z. and Noble, E.G. 1999 Isoproterenol potentiates exercise-induction of Hsp70 in cardiac and skeletal muscle. Cell Stress. Chaperones. 4: 199–204. PM:10547069.PubMedGoogle Scholar
  164. Paulsen, G., Vissing, K., Kalhovde, J.M., Ugelstad, I., Bayer, M.L., Kadi, F., Schjerling, P., Hallen, J., and Raastad, T. 2007 Maximal eccentric exercise induces a rapid accumulation of small heat shock proteins on myofibrils and a delayed HSP70 response in humans. Am. J. Physiol. Regul. Integr. Comp Physiol. 293: R844–R853. PM:17522120.PubMedGoogle Scholar
  165. Petersen, A.M. and Pedersen, B.K. 2005 The anti-inflammatory effect of exercise. J. Appl. Physiol. 98: 1154–1162. PM:15772055.PubMedCrossRefGoogle Scholar
  166. Pette, D. and Staron, R.S. 2001 Transitions of muscle fiber phenotypic profiles. Histochem. Cell Biol. 115: 359–372. PM:11449884.PubMedGoogle Scholar
  167. Powers, S.K. and Lennon, S.L. 1999 Analysis of cellular responses to free radicals: focus on exercise and skeletal muscle. Proc. Nutr. Soc. 58: 1025–1033. PM:10817171.PubMedCrossRefGoogle Scholar
  168. Prior, B.M., Yang, H.T., and Terjung, R.L. 2004 What makes vessels grow with exercise training? J. Appl. Physiol. 97: 1119–1128. PM:15333630.PubMedCrossRefGoogle Scholar
  169. Radak, Z., Chung, H.Y., and Goto, S. 2008 Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic. Biol. Med. 44: 153–159. PM:18191751.PubMedCrossRefGoogle Scholar
  170. Redaelli, C.A., Tian, Y.H., Schaffner, T., Ledermann, M., Baer, H.U., and Dufour, J.F. 2002a Extended preservation of rat liver graft by induction of heme oxygenase-1. Hepatology 35: 1082–1092. PM:11981758.PubMedCrossRefGoogle Scholar
  171. Redaelli, C.A., Tien, Y.H., Kubulus, D., Mazzucchelli, L., Schilling, M.K., and Wagner, A.C. 2002b Hyperthermia preconditioning induces renal heat shock protein expression, improves cold ischemia tolerance, kidney graft function and survival in rats. Nephron 90: 489–497. PM:11961410.PubMedCrossRefGoogle Scholar
  172. Redaelli, C.A., Wagner, M., Kulli, C., Tian, Y.H., Kubulus, D., Mazzucchelli, L., Wagner, A.C., and Schilling, M.K. 2001 Hyperthermia-induced HSP expression correlates with improved rat renal isograft viability and survival in kidneys harvested from non-heart-beating donors. Transpl. Int. 14: 351–360. PM:11793032.PubMedCrossRefGoogle Scholar
  173. Reid, M.B., Haack, K.E., Franchek, K.M., Valberg, P.A., Kobzik, L., and West, M.S. 1992 Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J. Appl. Physiol. 73: 1797–1804. PM:1474054.PubMedGoogle Scholar
  174. Riederer, I., Negroni, E., Bigot, A., Bencze, M., Di Santo, J., Aamiri, A., Butler-Browne, G., and Mouly, V. 2008 Heat shock treatment increases engraftment of transplanted human myoblasts into immunodeficient mice. Transplant. Proc. 40: 624–630. PM:18374147.PubMedCrossRefGoogle Scholar
  175. Robinson, M.B., Taylor, A.R., Gifondorwa, D.J., Tytell, M., and Milligan, C.E. 2008 Exogenous Hsc70, but not thermal preconditioning, confers protection to motoneurons subjected to oxidative stress. Dev. Neurobiol. 68: 1–17. PM:17918243.PubMedCrossRefGoogle Scholar
  176. Robinson, M.B., Tidwell, J.L., Gould, T., Taylor, A.R., Newbern, J.M., Graves, J., Tytell, M., and Milligan, C.E. 2005 Extracellular heat shock protein 70: a critical component for motoneuron survival. J. Neurosci. 25: 9735–9745. PM:16237177.PubMedCrossRefGoogle Scholar
  177. Ruete, M.C., Carrizo, L.C., and Valles, P.G. 2008 Na+/K+-ATPase stabilization by Hsp70 in the outer stripe of the outer medulla in rats during recovery from a low-protein diet. Cell Stress Chaperones. 13: 157–167.PubMedCrossRefGoogle Scholar
  178. Sahlin, K., Katz, A., and Broberg, S. 1990 Tricarboxylic acid cycle intermediates in human muscle during prolonged exercise. Am. J. Physiol. 259: C834–C841. PM:2240197.PubMedGoogle Scholar
  179. Salo, D.C., Donovan, C.M., and Davies, K.J. 1991 HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise. Free Radic. Biol. Med. 11: 239–246. PM:1937141.PubMedCrossRefGoogle Scholar
  180. Saltin, B. 1981 Muscle fibre recruitment and metabolism in prolonged exhaustive dynamic exercise. Ciba Found. Symp. 82: 41–58. PM:6913477.PubMedGoogle Scholar
  181. Sammut, I.A., Jayakumar, J., Latif, N., Rothery, S., Severs, N.J., Smolenski, R.T., Bates, T.E., and Yacoub, M.H. 2001 Heat stress contributes to the enhancement of cardiac mitochondrial complex activity. Am. J. Pathol. 158: 1821–1831. PM:11337380.PubMedGoogle Scholar
  182. Sarge, K.D., Murphy, S.P., and Morimoto, R.I. 1993 Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell Biol. 13: 1392–1407. PM:8441385.PubMedGoogle Scholar
  183. Selsby, J.T. and Dodd, S.L. 2005 Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am. J. Physiol. Regul. Integr. Comp Physiol. 289: R134–R139. PM:15761186.PubMedGoogle Scholar
  184. Shan, Y.X., Yang, T.L., Mestril, R., and Wang, P.H. 2003 Hsp10 and Hsp60 suppress ubiquitination of insulin-like growth factor-1 receptor and augment insulin-like growth factor-1 receptor signaling in cardiac muscle: implications on decreased myocardial protection in diabetic cardiomyopathy. J. Biol. Chem. 278: 45492–45498. PM:12970367.PubMedCrossRefGoogle Scholar
  185. Sharp, P., Krishnan, M., Pullar, O., Navarrete, R., Wells, D., and de, B.J. 2006 Heat shock protein 27 rescues motor neurons following nerve injury and preserves muscle function. Exp. Neurol. 198: 511–518. PM:16497297.PubMedCrossRefGoogle Scholar
  186. Shinohara, T., Takahashi, N., Kohno, H., Yamanaka, K., Ooie, T., Wakisaka, O., Murozono, Y., Taniguchi, Y., Torigoe, Y., Hara, M., Shimada, T., Saikawa, T., and Yoshimatsu, H. 2007 Mitochondria are targets for geranylgeranylacetone-induced cardioprotection against ischemia-reperfusion in the rat heart. Am. J. Physiol. Heart Circ. Physiol. 293: H1892–H1899. PM:17586615.PubMedCrossRefGoogle Scholar
  187. Skidmore, R., Gutierrez, J.A., Guerriero, V., Jr., and Kregel, K.C. 1995 HSP70 induction during exercise and heat stress in rats: role of internal temperature. Am. J. Physiol. 268: R92–R97. PM:7840344.PubMedGoogle Scholar
  188. Sluijter, J.P., Smeets, M.B., Velema, E., Pasterkamp, G., and de Kleijn, D.P. 2004 Increase in collagen turnover but not in collagen fiber content is associated with flow-induced arterial remodeling. J. Vasc. Res. 41: 546–555. PM:15542933.PubMedCrossRefGoogle Scholar
  189. Someren, J.S., Faber, L.E., Klein, J.D., and Tumlin, J.A. 1999 Heat shock proteins 70 and 90 increase calcineurin activity in vitro through calmodulin-dependent and independent mechanisms. Biochem. Biophys. Res. Commun. 260: 619–625. PM:0010403816.PubMedCrossRefGoogle Scholar
  190. Soncin, F., Zhang, X., Chu, B., Wang, X., Asea, A., Ann, S.M., Sacks, D.B., and Calderwood, S.K. 2003 Transcriptional activity and DNA binding of heat shock factor-1 involve phosphorylation on threonine 142 by CK2. Biochem. Biophys. Res. Commun. 303: 700–706. PM:12659875.PubMedCrossRefGoogle Scholar
  191. Suzuki, K., Smolenski, R.T., Jayakumar, J., Murtuza, B., Brand, N.J., and Yacoub, M.H. 2000 Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart. Circulation 102: III216–III221. PM:11082390.PubMedGoogle Scholar
  192. Tarricone, E., Scapin, C., Vitadello, M., Esposito, F., Margonato, V., Milano, G., Samaja, M., and Gorza, L. 2008 Cellular distribution of Hsp70 expression in rat skeletal muscles. Effects of moderate exercise training and chronic hypoxia. Cell Stress. Chaperones. PM:18528785.Google Scholar
  193. Tessier, D.J., Komalavilas, P., Liu, B., Kent, C.K., Thresher, J.S., Dreiza, C.M., Panitch, A., Joshi, L., Furnish, E., Stone, W., Fowl, R., and Brophy, C.M. 2004 Transduction of peptide analogs of the small heat shock-related protein HSP20 inhibits intimal hyperplasia. J. Vasc. Surg. 40: 106–114. PM:15218470.PubMedCrossRefGoogle Scholar
  194. Thomas, J.A. and Noble, E.G. 1999 Heat shock does not attenuate low-frequency fatigue. Can. J. Physiol. Pharmacol. 77: 64–70. PM:0010535668.PubMedCrossRefGoogle Scholar
  195. Thomason, D.B., Biggs, R.B., and Booth, F.W. 1989 Protein metabolism and beta-myosin heavy-chain mRNA in unweighted soleus muscle. Am. J. Physiol. 257: R300–R305. PM:2764153.PubMedGoogle Scholar
  196. Thompson, H.S., Clarkson, P.M., and Scordilis, S.P. 2002 The repeated bout effect and heat shock proteins: intramuscular HSP27 and HSP70 expression following two bouts of eccentric exercise in humans. Acta Physiol. Scand. 174: 47–56. PM:11851596.PubMedCrossRefGoogle Scholar
  197. Thompson, H.S., Scordilis, S.P., Clarkson, P.M., and Lohrer, W.A. 2001 A single bout of eccentric exercise increases HSP27 and HSC/HSP70 in human skeletal muscle. Acta Physiol. Scand. 171: 187–193. PM:11350279.PubMedCrossRefGoogle Scholar
  198. Tonkiss, J. and Calderwood, S.K. 2005 Regulation of heat shock gene transcription in neuronal cells. Int. J. Hyperthermia. 21: 433–444. PM:16048840.PubMedCrossRefGoogle Scholar
  199. Tumlin, J.A., Lea, J.P., Swanson, C.E., Smith, C.L., Edge, S.S., and Someren, J.S. 1997 Aldosterone and dexamethasone stimulate calcineurin activity through a transcription-independent mechanism involving steroid receptor- associated heat shock proteins. J. Clin. Invest. 99: 1217–1223. PM:0009077529.PubMedCrossRefGoogle Scholar
  200. Tupling, A.R., Bombardier, E., Stewart, R.D., Vigna, C., and Aqui, A.E. 2007 Muscle fiber type-specific response of Hsp70 expression in human quadriceps following acute isometric exercise. J. Appl. Physiol. 103: 2105–2111. PM:17916670.PubMedCrossRefGoogle Scholar
  201. Tupling, A.R., Gramolini, A.O., Duhamel, T.A., Kondo, H., Asahi, M., Tsuchiya, S.C., Borrelli, M.J., Lepock, J.R., Otsu, K., Hori, M., MacLennan, D.H., and Green, H.J. 2004 HSP70 binds to the fast-twitch skeletal muscle sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA1a) and prevents thermal inactivation. J. Biol. Chem. 279: 52382–52389. PM:15371420.PubMedCrossRefGoogle Scholar
  202. Uchida, S., Fujiki, M., Nagai, Y., Abe, T., and Kobayashi, H. 2006 Geranylgeranylacetone, a noninvasive heat shock protein inducer, induces protein kinase C and leads to neuroprotection against cerebral infarction in rats. Neurosci. Lett. 396: 220–224. PM:16406313.PubMedCrossRefGoogle Scholar
  203. Udelsman, R., Blake, M.J., Stagg, C.A., Li, D.G., Putney, D.J., and Holbrook, N.J. 1993 Vascular heat shock protein expression in response to stress. Endocrine and autonomic regulation of this age-dependent response. J. Clin. Invest. 91: 465–473. PM:8094399.PubMedCrossRefGoogle Scholar
  204. Udelsman, R., Gallucci, W.T., Bacher, J., Loriaux, D.L., and Chrousos, G.P. 1986 Hemodynamic effects of corticotropin releasing hormone in the anesthetized cynomolgus monkey. Peptides 7: 465–471. PM:3490657.PubMedCrossRefGoogle Scholar
  205. Volloch, V. and Rits, S. 1999 A natural extracellular factor that induces Hsp72, inhibits apoptosis, and restores stress resistance in aged human cells. Exp. Cell Res. 253: 483–492. PM:0010585271.PubMedCrossRefGoogle Scholar
  206. Walker, P.M. 1991 Ischemia/reperfusion injury in skeletal muscle. Ann. Vasc. Surg. 5: 399–402. PM:1878303.PubMedCrossRefGoogle Scholar
  207. Wang, X.L., Fu, A., Raghavakaimal, S., and Lee, H.C. 2007 Proteomic analysis of vascular endothelial cells in response to laminar shear stress. Proteomics 7: 588–596. PM:17309104.PubMedCrossRefGoogle Scholar
  208. Wang, X., Grammatikakis, N., Siganou, A., and Calderwood, S.K. 2003 Regulation of molecular chaperone gene transcription involves the serine phosphorylation, 14-3-3 epsilon binding, and cytoplasmic sequestration of heat shock factor 1. Mol. Cell Biol. 23: 6013–6026. PM:12917326.PubMedCrossRefGoogle Scholar
  209. Welch, W.J. 1991 The role of heat-shock proteins as molecular chaperones. Curr. Opin. Cell Biol. 3: 1033–1038. PM:1687649.PubMedCrossRefGoogle Scholar
  210. Whitham, M. and Fortes, M.B. 2008 Heat shock protein 72: release and biological significance during exercise. Front Biosci. 13: 1328–1339. PM:17981633.PubMedCrossRefGoogle Scholar
  211. Wong, H.R., Finder, J.D., Wasserloos, K., and Pitt, B.R. 1995 Expression of iNOS in cultured rat pulmonary artery smooth muscle cells is inhibited by the heat shock response. Am. J. Physiol. 269: L843–L848. PM:8572246.PubMedGoogle Scholar
  212. Xia, W. and Voellmy, R. 1997 Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers. J. Biol. Chem. 272: 4094–4102. PM:9020119.PubMedCrossRefGoogle Scholar
  213. Xu, Q. and Wick, G. 1996 The role of heat shock proteins in protection and pathophysiology of the arterial wall. Mol. Med. Today. 2: 372–379. PM:8885256.PubMedCrossRefGoogle Scholar
  214. Yamanaka, K., Takahashi, N., Ooie, T., Kaneda, K., Yoshimatsu, H., and Saikawa, T. 2003 Role of protein kinase C in geranylgeranylacetone-induced expression of heat-shock protein 72 and cardioprotection in the rat heart. J. Mol. Cell Cardiol. 35: 785–794. PM:12818569.PubMedCrossRefGoogle Scholar
  215. Zheng, Y., Im, C.N., and Seo, J.S. 2006 Inhibitory effect of Hsp70 on angiotensin II-induced vascular smooth muscle cell hypertrophy. Exp. Mol. Med. 38: 509–518. PM:17079867.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Earl G. Noble
    • 1
    • 2
    Email author
  • C.W. James Melling
    • 3
  • Kevin J. Milne
    • 4
  1. 1.School of KinesiologyThe University of Western OntarioLondonCanada
  2. 2.Lawson Health Research InstituteThe University of Western OntarioLondonCanada
  3. 3.School of Health Studies, Faculty of Health SciencesThe University of Western OntarioLondonCanada
  4. 4.Department of Kinesiology, Faculty of Human KineticsUniversity of WindsorWindsorCanada

Personalised recommendations