Increased temperature and protein oxidation lead to HSP72 mRNA and protein accumulation in the in vivo exercised rat heart

Experimental Physiology

Volumn 94, Issue 1, 2009, Pages 71-80

  Staib, Jessica L ^a,d   Tümer, Nihal ^b,c   Powers, Scott K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 72; HEAT SHOCK TRANSCRIPTION FACTOR 1; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; EXERCISE; GENE ACTIVATION; IN VIVO STUDY; MALE; NONHUMAN; OXIDATION; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

EID: 58149138921     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2008.044685     Document Type: Article

References (50)

1. Abravaya K, Phillips B & Morimoto RI (1991). Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev 5, 2117 2127.
2. Agashe VR & Hartl FU (2000). Roles of molecular chaperones in cytoplasmic protein folding. Semin Cell Dev Biol 11, 15 25.
3. Ahn SG & Thiele DJ (2003). Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17, 516 528.
4. Atalay M, Oksala NK, Laaksonen DE, Khanna S, Nakao C, Lappalainen J, Roy S, Hanninen O & Sen CK (2004). Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol 97, 605 611.
5. Bradford MM (1976). 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.
6. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL & Moore RL (2007). Short-term treadmill running in the rat: what kind of stressor is it? J Appl Physiol 103, 1979 1985.
7. Calderwood SK (2005). Regulatory interfaces between the stress protein response and other gene expression programs in the cell. Methods 35, 139 148.
8. Cotto JJ, Kline M & Morimoto RI (1996). Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem 271, 3355 3358.
9. Demirel HA, Powers SK, Zergeroglu MA, Shanely RA, Hamilton K, Coombes J & Naito H (2001). Short-term exercise improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. J Appl Physiol 91, 2205 2212.
10. Farkas T, Kutskova YA & Zimarino V (1998). Intramolecular repression of mouse heat shock factor 1. Mol Cell Biol 18, 906 918.
11. Goodson ML & Sarge KD (1995). Heat-inducible DNA binding of purified heat shock transcription factor 1. J Biol Chem 270, 2447 2450.
12. Guettouche T, Boellmann F, Lane WS & Voellmy R (2005). Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 6, 4.
13. Hamilton KL, Powers SK, Sugiura T, Kim S, Lennon S, Tumer N & Mehta JL (2001). Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins. Am J Physiol Heart Circ Physiol 281, H1346 H1352.
14. Harris MB & Starnes JW (2001). Effects of body temperature during exercise training on myocardial adaptations. Am J Physiol Heart Circ Physiol 280, H2271 H2280.
15. Holmberg CI, Roos PM, Lord JM, Eriksson JE & Sistonen L (1998). Conventional and novel PKC isoenzymes modify the heat-induced stress response but are not activated by heat shock. J Cell Sci 111, 3357 3365.
16. Iwaki K, Chi SH, Dillmann WH & Mestril R (1993). Induction of HSP70 in cultured rat neonatal cardiomyocytes by hypoxia and metabolic stress. Circulation 87, 2023 2032.
17. Jurivich DA, Sistonen L, Kroes RA & Morimoto RI (1992). Effect of sodium salicylate on the human heat shock response. Science 255, 1243 1245.
18. Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C & Jackson MJ (2001). Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 90, 1031 1035.
19. Latchman DS (2001). Heat shock proteins and cardiac protection. Cardiovasc Res 51, 637 646.
20. McDuffee AT, Senisterra G, Huntley S, Lepock JR, Sekhar KR, Meredith MJ, Borrelli MJ, Morrow JD & Freeman ML (1997). Proteins containing non-native disulfide bonds generated by oxidative stress can act as signals for the induction of the heat shock response. J Cell Physiol 171, 143 151.
21. Mazroui R, Di Marco S, Kaufman RJ & Gallouzi IE (2007). Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol Biol Cell 18, 2603 2618.
22. Melling CW, Krause MP & Noble EG (2006). PKA-mediated ERK1/2 inactivation and hsp70 gene expression following exercise. J Mol Cell Cardiol 41, 816 822.
23. Melling CW, Thorp DB, Milne KJ, Krause MP & Noble EG (2007). Exercise-mediated regulation of Hsp70 expression following aerobic exercise training. Am J Physiol Heart Circ Physiol 293, H3692 H3698.
24. Melling CW, Thorp DB, Milne KJ & Noble EG (2008). Myocardial Hsp70 phosphorylation and PKC-mediated cardioprotection following exercise. Cell Stress Chaperones 10.1007/s12192-008-0065-x.
25. Melling CW, Thorp DB & Noble EG (2004). Regulation of myocardial heat shock protein 70 gene expression following exercise. J Mol Cell Cardiol 37, 847 855.
26. Milne KJ & Noble EG (2002). Exercise-induced elevation of HSP70 is intensity dependent. J Appl Physiol 93, 561 568.
27. Moran M, Delgado J, González B, Manso R & Megías A (2004). Responses of rat myocardial antioxidant defences and heat shock protein HSP72 induced by 12 and 24-week treadmill training. Acta Physiol Scand 180, 157 166.
28. Morimoto RI (1998). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12, 3788 3796.
29. Morimoto RI (2002). Dynamic remodeling of transcription complexes by molecular chaperones. Cell 110, 281 284.
30. Morimoto RI, Kline MP, Bimston DN & Cotto JJ (1997). The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32, 17 29.
31. Morimoto RI, Kroeger PE & Cotto JJ (1996). The transcriptional regulation of heat shock genes: a plethora of heat shock factors and regulatory conditions. EXS 77, 139 163.
32. Morton JP, MacLaren DP, Cable NT, Bongers T, Griffiths RD, Campbell IT, Evans L, Kayani A, McArdle A & 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.
33. Moseley PL, Wallen ES, McCafferty JD, Flanagan S & Kern JA (1993). Heat stress regulates the human 70-kDa heat-shock gene through the 3′-untranslated region. Am J Physiol Lung Cell Mol Physiol 264, L533 L537.
34. Nishizawa J, Nakai A, Higashi T, Tanabe M, Nomoto S, Matsuda K, Ban T & Nagata K (1996). Reperfusion causes significant activation of heat shock transcription factor 1 in ischemic rat heart. Circulation 94, 2185 2192.
35. Ogura Y, Naito H, Akin S, Ichinoseki-Sekine N, Kurosaka M, Kakigi R, Sugiura T, Powers SK, Katamoto S & Demirel HA (2008). Elevation of body temperature is an essential factor for exercise-increased extracellular heat shock protein 72 level in rat plasma. Am J Physiol Regul Integr Comp Physiol 294, R1600 R1607.
36. Paroo Z, Meredith MJ, Locke M, Haist JV, Karmazyn M & Noble EG (2002). Redox signaling of cardiac HSF1 DNA binding. Am J Physiol Cell Physiol 283, C404 C411.
37. Pirkkala L, Nykanen P & Sistonen L (2001). Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15, 1118 1131.
38. Qian YZ, Shipley JB, Levasseur JE & Kukreja RC (1998). Dissociation of heat shock proteins expression with ischemic tolerance by whole body hyperthermia in rat heart. J Mol Cell Cardiol 30, 1163 1172.
39. Quindry JC, Hamilton KL, French JP, Lee Y, Murlasits Z, Tumer N & Powers SK (2007). Exercise-induced HSP-72 elevation and cardioprotection against infarct and apoptosis. J Appl Physiol 103, 1056 1062.
40. Ruell PA, Hoffman KM, Chow CM & Thompson MW (2004). Effect of temperature and duration of hyperthermia on HSP72 induction in rat tissues. Mol Cell Biochem 267, 187 194.
41. Sarge KD, Murphy SP & Morimoto RI (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.
42. Shinohara T, Takahashi N, Ooie T, Ichinose M, Hara M, Yonemochi H, Saikawa T & Yoshimatsu H (2004). Estrogen inhibits hyperthermia-induced expression of heat-shock protein 72 and cardioprotection against ischemia/reperfusion injury in female rat heart. J Mol Cell Cardiol 37, 1053 1061.
43. Staib JL, Quindry JC, French JP, Criswell DS & Powers SK (2007). Increased temperature, not cardiac load, activates heat shock transcription factor 1 and heat shock protein 72 expression in the heart. Am J Physiol Regul Integr Comp Physiol 292, R432 R439.
44. Taylor RP, Harris MB & Starnes JW (1999). Acute exercise can improve cardioprotection without increasing heat shock protein content. Am J Physiol Heart Circ Physiol 276, H1098 H1102.
45. Voellmy R (2004). Transcriptional regulation of the metazoan stress protein response. Prog Nucleic Acid Res Mol Biol 78, 143 185.
46. Watkins AM, Cheek DJ, Harvey AE, Goodwin JD, Blair KE & Mitchell JB (2007). Heat shock protein (HSP-72) levels in skeletal muscle following work in heat. Aviat Space Environ Med 78, 901 905.
47. Xia W & 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.
48. Yamanaka K, Takahashi N, Ooie T, Kaneda K, Yoshimatsu H & 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.
49. Zhong M, Orosz A & Wu C (1998). Direct sensing of heat and oxidation by Drosophila heat shock transcription factor. Mol Cell 2, 101 108.
50. Zou J, Salminen WF, Roberts SM & Voellmy R (1998). Correlation between glutathione oxidation and trimerization of heat shock factor 1, an early step in stress induction of the Hsp response. Cell Stress Chaperones 3, 130 141.