Advertisement

Cell Stress and Chaperones

, Volume 19, Issue 4, pp 519–527 | Cite as

The effect of heat stress on skeletal muscle contractile properties

  • Marius LockeEmail author
  • Carlo Celotti
Original Paper

Abstract

An elevated heat-shock protein (HSP) content protects cells and tissues, including skeletal muscles, from certain stressors. We determined if heat stress and the elevated HSP content that results is correlated with protection of contractile characteristics of isolated fast and slow skeletal muscles when contracting at elevated temperatures. To elevate muscle HSP content, one hindlimb of Sprague–Dawley rats (21–28 days old, 70–90 g) was subjected to a 15 min 42 °C heat-stress. Twenty-four hours later, both extensor digitorum longus (EDL) and soleus muscles were removed, mounted in either 20 °C or 42 °C Krebs-Ringer solution, and electrically stimulated. Controls consisted of the same muscles from the contra-lateral (non-stressed) hindlimbs as well as muscles from other (unstressed) animals. Isolated muscles were twitched and brought to tetanus every 5 min for 30 min. As expected, HSP content was elevated in muscles from the heat-stressed limbs when compared with controls. Regardless of prior treatment, both EDL and soleus twitch tensions were lower at 42 °C when compared with 20 °C. In addition, when incubated at 42 °C, both muscles showed a drop in twitch tension between 5 and 30 min. For tetanic tension, both muscles also showed an increase in tension between 5 and 30 min when stimulated at 20 °C regardless of treatment but when stimulated at 42 °C no change was observed. No protective effect of an elevated HSP content was observed for either muscle. In conclusion, although heat stress caused an elevation in HSP content, no protective effects were conferred to isolated contracting muscles.

Keywords

Heat stress Hsp25 Hsp72 Skeletal muscle Contraction Rat In vitro 

References

  1. Allen DG (2009) Fatigue in working muscles. J Appl Physiol 106(2):358–359PubMedCrossRefGoogle Scholar
  2. Armstrong RB, Phelps RO (1984) Muscle fiber type composition of the rat hindlimb. Am J Anat 171(3):259–272PubMedCrossRefGoogle Scholar
  3. Brooks GA, Hittleman KJ, Faulkner JA, Beyer RE (1971) Tissue temperature and whole-animal oxygen consumption after exercise. Am J Physiol 221:427–431PubMedGoogle Scholar
  4. Bryantsev AL, Loktionova SA, Ilyinskaya OP, Tararak EM, Kampinga HH, Kabakov AE (2002) Distribution, phosphorylation, and activities of HSP25 in heat-stressed H9c2 myoblasts: a functional link to cytoprotection. Cell Stress Chaperones 7:146–155PubMedCentralPubMedCrossRefGoogle Scholar
  5. Coupland ME, Ranatunga KW (2003) Force generation induced by rapid temperature jumps in intact mammalian (rat) skeletal muscle fibres. J Physiol 548(2):439–449PubMedCentralPubMedCrossRefGoogle Scholar
  6. Currie RW, Tanguay RM, Kingma JG Jr (1993) Heat-shock response and limitation of tissue necrosis during occlusion/reperfusion in rabbit hearts. Circulation 87:963–971PubMedCrossRefGoogle Scholar
  7. Fu MH, Tupling AR (2009) Protective effects of Hsp70 on the structure and function of SERCA2a expressed in HEK-293 cells during heat stress. Am J Physiol Heart Circ Physiol 296(4):H1175–H1183PubMedCrossRefGoogle Scholar
  8. Garramone RR Jr, Winters RM, Das DK, Deckers PJ (1994) Reduction of skeletal muscle injury through stress conditioning using the heat-shock response. Plast Reconstr Surg 93(6):1242–1247PubMedCrossRefGoogle Scholar
  9. Gollnick PD, Hodgson DR (1986) The identification of fiber types in skeletal muscle: a continual dilemma. Exerc Sport Sci Rev 14:81–104PubMedCrossRefGoogle Scholar
  10. Harrison SM, Bers DM (1989) Influence of temperature on the calcium sensitivity of the myofilaments of skinned ventricular muscle from the rabbit. J Gen Physiol 93(3):411–428PubMedCrossRefGoogle Scholar
  11. Karmazyn M, Mailer K, Currie WR (1990) Acquisition and decay of heat-shock-enhanced postischemic ventricular recovery. Am J Physiol 259:H424–H431PubMedGoogle Scholar
  12. Kawana K, Miyamoto Y, Tanonaka K, Han-no Y, Yoshida H, Takahashi M, Takeo S (2000) Cytoprotective mechanism of heat shock protein 70 against hypoxia/reoxygenation injury. J Mol Cell Cardiol 32(12):2229–2237PubMedCrossRefGoogle Scholar
  13. Kayani AC, Close GL, Broome CS, Jackson MJ, McArdle A (2008) Enhanced recovery from contraction-induced damage in skeletal muscles of old mice following treatment with the heat shock protein inducer 17-(allylamino)-17-demethoxygeldanamycin. Rejuvenation Res 11(6):1021–1030PubMedCrossRefGoogle Scholar
  14. Kössler F, Küchler G (1987) Contractile properties of fast and slow twitch muscles of the rat at temperatures between 6 and 42 degrees C. Biomed Biochim Acta 46(11):815–822PubMedGoogle Scholar
  15. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  16. Larkins NT, Murphy RM, Lamb GD (2012) Absolute amounts and diffusibility of HSP72, HSP25, and αB-crystallin in fast- and slow-twitch skeletal muscle fibers of rat. Am J Physiol Cell Physiol 302:C228–C239PubMedCrossRefGoogle Scholar
  17. Latchman DS (2001) Heat shock proteins and cardiac protection. Cardiovasc Res 51(4):637–646PubMedCrossRefGoogle Scholar
  18. Lepore DA, Hurley JV, Stewart AG, Morrison WA, Anderson RL (2000) Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle Nerve 23:1847–1855PubMedCrossRefGoogle Scholar
  19. Li GC, Meyer JL, Mak JY, Hahn GM (1983) Heat-induced protection of mice against thermal death. Cancer Res 43:5758–5760PubMedGoogle Scholar
  20. Li GC, Li LG, Liu YK, Mak JY, Chen LL, Lee WM (1991) Thermal response of rat fibroblasts stabily transfected with the human 70-kDa heat shock protein-encoding gene. Proc Natl Acad Sci 88:1681–1685PubMedCentralPubMedCrossRefGoogle Scholar
  21. Liu CC, Lin CH, Lin CY, Lee CC, Lin MT, Wen HC (2013) Transgenic overexpression of heat shock protein 72 in mouse muscle protects against exhaustive exercise-induced skeletal muscle damage. J Formos Med Assoc 112:24–30PubMedCrossRefGoogle Scholar
  22. Locke M (2008) Hsp accumulation and Hsf activation in rat skeletal muscle during compensatory hypertrophy. Acta Physiol 192(3):403–411CrossRefGoogle Scholar
  23. Locke M, Tanguay RM (1996) Increased HSF activation in muscles with a high constitutive HSP 70 expression. Cell Stress and Chaperones 1:189–196PubMedCentralPubMedCrossRefGoogle Scholar
  24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurements with the folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  25. McArdle A, Dillmann WH, Mestril R, Faulkner JA, Jackson MJ (2004) Overexpression of HSP70 in mouse skeletal muscle protects against muscle damage and age-related muscle dysfunction. FASEB J 18:355–357PubMedGoogle Scholar
  26. Myers J, Ashley E (1997) Dangerous curves. A perspective on exercise, lactate, and the anaerobic threshold. Chest 111(3):787–795PubMedCrossRefGoogle Scholar
  27. Noble EG, Milne KJ, Melling CWJ (2008) Heat shock proteins and exercise: a primer. Applied physiology, nutrition, and metabolism 33(5):1050–1065PubMedCrossRefGoogle Scholar
  28. Nosek TM, Brotto MA, Essig DA, Mestril R, Conover RC, Dillmann WH, Kolbeck RC (2000) Functional properties of skeletal muscle from transgenic animals with upregulated heat shock protein 70. Physiol Genomics 4(1):25–33PubMedGoogle Scholar
  29. O’Brien PJ, Li GO, Locke M, Klabunde RE, Ianuzzo CD (1997) Compensatory up-regulation of cardiac SR Ca2 + −pump by heat-shock counteracts SR Ca2 + −channel activation by ischemia/reperfusion. Mol Cell Biochem 173(1–2):135–143PubMedCrossRefGoogle Scholar
  30. Ranatunga KW, Wylie SR (1983) Temperature-dependent transitions in isometric contractions of rat muscle. J Physiol 339:87–95PubMedCentralPubMedGoogle Scholar
  31. Segal SS, Faulkner JA (1985) Temperature-dependent physiological stability of rat skeletal muscle in vitro. Am J Physiol 248(3):C265–C270PubMedGoogle Scholar
  32. Stein RB, Gordon T, Shriver J (1982) Temperature dependence of mammalian muscle contractions and ATPase activities. Biophys J 40(2):97–107PubMedCentralPubMedCrossRefGoogle Scholar
  33. Thomas JA, Noble EG (1999) Heat shock does note attenuate low-frequency fatigue. Can J Physiol Pharmacol 77(1):64–70PubMedCrossRefGoogle Scholar
  34. Touchberry CD, Gupte AA, Bomhoff GL, Graham ZA, Geiger PC, Gallagher PM (2012) Acute heat stress prior to downhill running may enhance skeletal muscle remodeling. Cell Stress and Chaperones 17(6):693–705PubMedCentralPubMedCrossRefGoogle Scholar
  35. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci 76(9):4350–4354PubMedCentralPubMedCrossRefGoogle Scholar
  36. Tupling AR, Gramolini AO, Duhamel TA, Kondo H, Asahi M, Tsuchiya SC, Borrelli MJ, Lepock JR, Otsu K, Hori M, MacLennan DH, Green HJ (2004) HSP70 binds to the fast-twitch skeletal muscle sarco(endo)plasmic reticulum Ca2+ − ATPase (SERCA1a) and prevents thermal inactivation. J Biol Chem 279(50):52382–52389PubMedCrossRefGoogle Scholar
  37. Tupling AR, Bombardier E, Vigna C, Quadrilatero J, Fu M (2008) Interaction between Hsp70 and the SR Ca2+ pump: a potential mechanism for cytoprotection in heart and skeletal muscle. Applied physiology, nutrition, and metabolism 33(5):1023–1032PubMedCrossRefGoogle Scholar
  38. Welch WJ (1987) The mammalian heat shock (or stress) response: a cellular defense mechanism. Adv Exp Med Biol 225:287–304PubMedCrossRefGoogle Scholar
  39. Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72:1063–1081PubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2013

Authors and Affiliations

  1. 1.Faculty of Kinesiology and Physical EducationUniversity of TorontoTorontoCanada

Personalised recommendations