Heat stress proteins and myocardial protection: Experimental model or potential clinical tool?

International Journal of Biochemistry and Cell Biology

Volumn 31, Issue 5, 1999, Pages 559-573

  Gray, Caroline C ^a   Amrani, Mohamed ^a   Yacoub, Magdi H ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Heat stress proteins; Ischemia reperfusion injury; Molecular chaperone; Myocardial protection

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90;

ANIMAL MODEL; CELL DAMAGE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE THERAPY; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEAT SHOCK; HEAT STRESS; HUMAN; NONHUMAN; PROTEIN EXPRESSION; REPERFUSION INJURY; REVIEW; TRANSGENIC ANIMAL;

EID: 0032918622     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1357-2725(99)00004-7     Document Type: Review

References (95)

1. Ritossa F. New puffs induced by temperature shock, DNP and salicylate in salivary chromosomes of D. melanogaster. Drosophila Information Service. 37:1963;122-123.
2. Tissieres A., Mitchell H.K., Tracy U.M. Protein synthesis in salivary glands of Drosophila melanogaster: Relation to chromosome puffs. J. Mol. Biol. 85:1974;389-398.
3. Lindquist S., Craig E.A. The heat shock proteins. Annu. Rev. Genet. 22:1988;631-677.
4. G.A. Perdrizet, The heat shock response, in: Heat shock Response and Organ Preservation: Models of Stress Conditioning, Springer, 1997, pp. 27-69.
5. Becker J., Craig E.A. Heat shock proteins as molecular chaperones. Eur. J. Biochem. 219:1994;11-23.
6. Ang D., Liberek K., Skowyra D., Zylicz M., Georgopoulos C. Biological role and regulation of the universally conserved heat shock proteins. J. Biol. Chem. 266:1991;24233-24236.
7. Slakey D.P., Roza A.M., Pieper G.M., Johnson C.P., Adams M.B. Delayed cardiac allograft rejection due to combined cyclosporine and antioxidant therapy. Transplantation. 56:1993;1305-1309.
8. Richard V., Kaeffer N., Thuillez C. Delayed protection of the ischemic heart from pathophysiology to therapeutic applications. Fundam. Clin. Pharmacol. 10:1996;409-415.
9. Patel B., Khaliq A., Jarvis Evans J.et al. Hypoxia induces hsp70 gene expression in human hepatoma (HEP G2) cells. Biochem. Mol. Biol. Int. 36:1995;907-912.
10. A.E. Kabakov, V.L. Gabai, Heat Shock Proteins and Cytoprotection: ATP-deprived Mammalian Cells, Springer-Verlag, Heidelberg, 1997.
11. Kukreja R.C., Kontos M.C., Loesser et al K.E. Oxidant stress increases heat shock protein 70 mRNA in isolated perfused rat heart. Am. J. Physiol. 267:1994;H2213-9.
12. Yang X.M., Baxter G.F., Heads R.J., Yellon D.M., Downey J.M., Cohen M.V. Infarct limitation of the second window of protection in a conscious rabbit model. Cardiovasc. Res. 31:1996;777-783.
13. Heads R.J., Latchman D.S., Yellon D.M. Stable high level expression of a transfected human hsp70 gene protects a heart-derived muscle cell line against thermal stress. J. Mol. Cell. Cardiol. 26:1994;695-699.
14. Amrani M., Allen N.J., O'Shea et al J. Role of catalase and heat shock protein on recovery of cardiac endothelial and mechanical function after ischemia. Cardioscience. 4:1993;193-198.
15. Wynn R.M., Davie J.R., Cox R.P., Chuang D.T. Molecular chaperones: heat shock proteins, foldases and matchmakers. J. Lab. Clin. Med. 124:1994;31-36.
16. Macario A.J. Heat shock proteins and molecular chaperones: implications for pathogenesis, diagnostics and therapeutics. Int. J. Clin. Lab. Res. 25:1995;59-70.
17. Scheibel T., Neuhofen S., Weikl et al T. ATP-binding properties of human hsp90. J. Biol. Chem. 272:1997;18608-18613.
18. Ketis N.V., Lawler J., Bendena W.G. Extracellular matrix components affect the pattern of protein synthesis of endothelial cells responding to hyperthermia. In Vitro Cell Dev. Biol. Anim. 29A:1993;768-772.
19. Nishizawa J., Nakai A., Higashi et al T. Reperfusion causes significant activation of heat shock transcription factor 1 in ischemic rat heart. Circulation. 94:1996;2185-2192.
20. Baulieu E.E., Binart N., Cadepond F.et al. Receptor-associated nuclear proteins and steroid/antisteroid action. Ann. NY Acad. Sci. 595:1990;300-315.
21. Garcia-Cardena G., Fan R., Shah et al V. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature. 392:1998;821-824.
22. Amrani M., Chester A.H., Jayakumar J., Schyns C.J., Yacoub M.H. L-arginine reverses low coronary reflow and enhances postischaemic recovery of cardiac mechanical function. Cardiovasc. Res. 30:1995;200-204.
23. Amrani M., O'Shea J., Allen et al N.J. Role of basal release of nitric oxide on coronary flow and mechanical performance of the isolated rat heart. J. Physiol. Lond. 456:1992;681-687.
24. Nadeau K., Das A., Walsh C.T. Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268:1993;1479-1487.
25. Bose S., Weikl T., Bugl H., Buchner J. Chaperone function of Hsp90-associated proteins. Science. 274:1996;1715-1717.
26. Nishida E., Koyasu S., Sakai H., Yahara I. Calmodulin-regulated binding of the 90-kDa heat shock protein to actin filaments. J. Biol. Chem. 261:1986;16033-16036.
27. Gething M.J., Sambrook J. Protein folding in the cell. Nature. 355:1992;33-45.
28. Minowada G., Welch W.J. Clinical implications of the stress response. J. Clin. Invest. 95:1995;3-12.
29. Beckmann R.P., Lovett M., Welch W.J. Examining the function and regulation of hsp70 in cells subjected to metabolic stress. J. Cell Biol. 116:1992;1137-1150.
30. Fung K.L., Hilgenberg L., Wang N.M., Chirico W.J. Conformations of the nucleotide and polypeptide binding domains of a cytosolic Hsp70 molecular chaperone are coupled. J. Biol. Chem. 271:1996;21559-21565.
31. Amrani M., Corbett J., Allen et al N.J. Induction of heat shock proteins enhances myocardial and endothelial functional recovery after prolonged cardioplegic arrest. Ann. Thorac. Surg. 57:1994;157-160.
32. Schelbert H.R. Cardiac PET: microcirculation and substrate transport in normal and diseased human myocardium. Ann. Nucl. Med. 8:1994;91-100.
33. Chiang H., Terlecky S.R., Plant C.P., Dice J.F. A role for a 70-kDa heat shock protein in lyposomal degradation of intracellular proteins. Science. 246:1989;382-385.
34. Marber M.S., Latchman D.S., Walker J.M., Yellon D.M. Cardiac stress protein elevation 24 h after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation. 88:1993;1264-1272.
35. Ostermann J., Horwich A.L., Neupert W., Hartl F.U. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature. 341:1989;125-130.
36. Kontos M.C., Shipley J.B., Kukreja R.C. Heat stress improves functional recovery and induces synthesis of 27- and 70-kDa heat shock proteins without preserving sarcoplasmic reticulum function in the ischemic rat heart. J. Mol. Cell. Cardiol. 28:1996;1885-1894.
37. Landry J., Lambert H., Zhou et al M. Human hsp27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J. Biol. Chem. 267:1992;794-803.
38. Rouse J., Cohen P., Trigon et al S. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 78:1994;1027-1037.
39. Lavoie J.N., Lambert H., Hickey E., Weber L.A., Landry J. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol. Cell Biol. 15:1995;505-516.
40. Lavoie J.N., Gingras Breton G., Tanguay R.M., Landry J. Induction of Chinese hamster hsp27 gene expression in mouse cells confers resistance to heat shock: hsp27 stabilization of the microfilament organization. J. Biol. Chem. 268:1993;3420-3429.
41. Rabindran S.K., Haroun R.I., Clos J., Wisniewski J., Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 259:1993;230-234.
42. Morimoto R.I. Cells in stress: transcriptional activation of heat shock genes. Science. 259:1993;1409-1410.
43. M. Fernandes, T. O'Brien, J.T. Lis, Structure and regulation of heat shock gene promoters, in: R.I. Morimoto, A. Tissieres, C. Georgopoulos (Eds.), The Biology of Heat Shock Proteins and Molecular Chaperones, Cold Spring Harbor Laboratory Press, New York, 1994, pp. 417-455.
44. Theodorakis N.G., Morimoto R.I. Posttranscriptional regulation of hsp70 expression in human cells: effects of heat shock, inhibition of protein synthesis, and adenovirus infection on translation and mRNA stability. Mol. Cell Biol. 7:1987;4357-4368.
45. H. Abe, T.S.J. Nowak, The stress response and its role in cellular defense mechanisms after ischemia, in: B.K. Siesjo, T. Wieloch (Eds.), Cellular and Molecular Mechanisms of Ischemic Brain Damage, Lippincott-Raven Publishers, Philadelphia, 1996, pp. 451-467.
46. Das D.K., Engelman R.M., Kimura Y. Molecular adaptation of cellular defenses following preconditioning of the heart by repeated ischaemia. Cardiovasc. Res. 27:1993;578-584.
47. Dillmann W.H., Mehta H.B., Barrieux A., Guth B.D., Neeley W.E., Ross J. Jr. Ischemia of the dog heart induces the appearance of a cardiac mRNA coding for a protein with migration characteristics similar to heat shock/stress protein 71. Circ. Res. 59:1986;110-114.
48. Currie R.W., Karmazyn M., Kloc M., Mailer K. Heat shock response is associated with enhanced postischemic ventricular recovery. Circ. Res. 63:1988;543-549.
49. Yellon D.M., Pasini E., Cargnoni A., Marber M.S., Latchman D.S., Ferrari R. The protective role of heat stress in the ischaemic and reperfused rabbit myocardium. J. Mol. Cell. Cardiol. 24:1992;895-907.
50. Yellon D.M., Iliodromitis E., Latchman et al D.S. Whole body heat stress fails to limit infarct size in the reperfused rabbit heart. Cardiovasc. Res. 26:1992;342-346.
51. Donnelly T.J., Sievers R.E., Vissern F.L., Welch W.J., Wolfe C.L. Heat shock protein induction in rat hearts: a role for improved myocardial salvage after ischemia and reperfusion? Circulation. 85:1992;769-778.
52. Yellon D.M., Marber M.S. Hsp70 in myocardial ischaemia. Experientia. 50:1994;1075-1084.
53. Williams R.S., Thomas J.A., Fina M., German Z., Benjamin I.J. Human heat shock protein 70 (hsp70) protects murine cells from injury during metabolic stress. J. Clin. Invest. 92:1993;503-508.
54. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 74:1986;1124-1136.
55. Yellon D.M., Baxter G.F. A 'second window of protection' or delayed preconditioning phenomenon: future horizons for myocardial protection? J. Thorac. Cardiovasc. Surg. 115:1995;200-209.
56. V. Popovic, P. Popovic, Hypothermia in Biology and Medicine, Grune and Stratton, New York, 1974.
57. Ferrari R., Raddino R., Di Lisa et al F. Effects of temperature on myocardial calcium homeostasis and mitochondrial function during ischemia and respefusion. J. Thorac. Cardiovasc. Surg. 99:1990;919-928.
58. Hearse D.J., Stewart D.A., Braimbridge M.V. Cellular protection during myocardial ischemia: the development and characterization of a procedure for the induction of reversible ischemic arrest. Circulation. 54:1976;193-202.
59. Plumier J.C., Ross B.M., Currie et al R.W. Transgenic mice expressing the human heat shock protein 70 have improved postischemic myocardial recovery. J. Clin. Invest. 95:1995;1854-1860.
60. Wong H.R., Menendez I.Y., Ryan M.A., Denenberg A.G., Wispe J.R. Increased expression of heat shock protein-70 protects A549 cells against hyperoxia. Am. J. Physiol. 275:1998;L836-41.
61. Amrani M., Corbett J., Boateng S.Y., Dunn M.J., Yacoub M.H. Kinetics of induction and protective effect of heat shock proteins after cardioplegic arrest. Ann. Thorac. Surg. 61:1996;1407-1411.
62. R.N. Cornelussen, A.V. Garnier, G.J. van der Vusse, R.S. Reneman, L.H.E.H. Snoeckx, Biphasic effect of heat stress pretreatment on ischemic tolerance of isolated rat hearts. J. Mol. Cell. Cardiol (1998) 365-72.
63. Yamashita N., Hoshida S., Nishida et al M. Time course of tolerance to ischemia-reperfusion injury and induction of heat shock protein 72 by heat stress in the rat heart. J. Mol. Cell. Cardiol. 29:1997;1815-1821.
64. M. Amrani, N. Latif, K. Morrison et al., Relative induction of heat shock protein in coronary endothelial cells and cardiomyocytes: implications for myocardial protection, J. Thorac. Cardiovasc. Surg. (1998) 200-209.
65. T. Shyy, B.B. Asch, H.L. Asch, Concurrent collaspe of keratin filaments, aggregation of organelles and inhibition of protein synthesis during heat shock response in mammary epithelial cells, J. Cell Biol. (1989) 997-1008.
66. R.W. Nickells, T.I. Wang, L.W. Browder heat shock-induced changes in energy metabolism of Xenopus laevis embryos. In: J. Cell Biol. 913 (1986, 26th meeting), 1986.
67. K.J. Henle, A. Stone, Effect of hyperthermia on activity of three glycosyltransferases in Chinese hamster ovary cells, Cancer Res. (1988) 5717-5721.
68. P.M. Harari, M.E. Tome, E.W. Gerner, Heat shock-induced polyamine oxidantion in mammalian cells, J. Cell Biol. (1986) 175a.
69. Currie R.W., Tanguay R.M. Analysis of RNA for transcripts for catalase and SP71 in rat hearts after in vivo hyperthermia. Biochem. Cell Biol. 69:1991;375-382.
70. S.R. Wall, H. Fliss, B. Korecky, Role of catalase in myocardial proetction against ischemia in heat shocked rats, Mol. Cell. Biochem. (1993) 187-194.
71. Liu X., Engelman R.M., Moraru et al I.I. Heat shock: a new approach for myocardial preservation in cardiac surgery. Circulation. 86:1992;II358-363.
72. Suzuki K., Sawa Y., Kaneda Y., Ichikawa H., Shirakura R., Matsuda H. In vivo gene transfection with heat shock protein 70 enhances myocardial tolerance to ischemia-reperfusion injury in rat. J. Clin. Invest. 99:1997;1645-1650.
73. Marber M.S., Mestril R., Chi S.H., Sayen M.R., Yellon D.M., Dillmann W.H. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J. Clin. Invest. 95:1995;1446-1456.
74. Chang J.P., Kiehl D.E., Kennington A. Separation and characterization of the tryptic peptide mapping of recombinant bovine growth hormone by reversed-phase high-performance liquid chromatography electrospray mass spectrometry. Rapid. Commun. Mass. Spectrom. 11:1997;1266-1270.
75. Anathan J., Goldberg A.L., Voellmy R. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science. 232:1986;252-254.
76. Abravaya K., Myers M.P., Murphy S.P., Morimoto R.I. The human heat shock protein Hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6:1992;1153-1164.
77. Craig E.A., Gross C. Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16:1991;135-140.
78. Pelham H.R. Speculations on the functions of major heat shock and glucose regulated proteins. Cell. 46:1986;959-961.
79. Baler R., Welch W.J., Voellmy R. Heat shock regulationby nascent polypeptides and denaturated proteins: hsp70 as a potential autoregulatory factor. J. Cell Biol. 117:1992;1151-1159.
80. Mifflin L.C., Cohen R. Hsc70 moderates the heat shock (stress) response in Xenopus laevis oocytes and binds to denatured protein inducers. J. Biol. Chem. 269:1994;15718-15723.
81. Agarraberes F.A., Terlecky S.R., Dice J.F. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degardation. J. Cell Biol. 137:1997;825-834.
82. Kim D., Ouyang H., Li G.C. Heat shock protein hsp70 accelerates the recovery of heat shocked mammalian cells through the modulation of heat shock transcription factor HSF1. Proc. Natl. Acad. Sci. USA. 92:1995;2126-2130.
83. Jayakumar J., Smolenski R.T., Gray et al C.C. Influence of heat stress on myocardial metabolism and functional recovery after cardioplegic arrest: a 31P NMR study. Eur. J. Cardiothorac. Surg. 12:1998;467-474.
84. Radford N.B., Fina M., Benjamin et al I.J. Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc. Natl. Acad. Sci. USA. 93:1996;2339-2342.
85. Saad A.H., Hahn G.M. Activation of potassium channels: relationship to the heat shock response. Proc. Natl. Acad. Sci. USA. 89:1992;9396-9399.
86. Joyeux M., Godin-Ribuot D., Ribuot C. Resistance to myocardial infarction induced by heat stress and the effect of ATP-sensitive potassium channel blockade in the isolated heart. Br. J. Pharmacol. 123:1998;1085-1088.
87. Pell T.J., Yellon D.M., Goodwin R.W., Baxter G.F. Myocardial ischemic tolerance following heat stress is abolished by ATP-sensitive potassium channel blockade. Cardiovasc. Drugs Ther. 11:1997;676-686.
88. McConkey D.J., Orrenius S. Signal transduction pathways to apoptosis. Trends Cell Biol. 4:1994;370-375.
89. Fliss H., Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ. Res. 79:1996;949-956.
90. Knowlton A.A., Kapadia S., Torre-Amione et al G. Differential expression of heat shock proteins in normal and failing human hearts. J. Mol. Cell. Cardiol. 30:1998;811-818.
91. Mehlen P., Schulze-Osthoff K., Arrigo A.P. Small stress proteins as novel regulators of apoptosis: heat shock protein 27 blocks FAS/APO-1 and staurosporine-induced cell death. J. Biol. Chem. 271:1996;16510-16514.
92. Li W.X., Chen C.H., Ling C.C., Li G.C. Apoptosis in heat-induced cell killing: the protective role of hsp-70 and the sensitization effect of the c-myc gene. Radiat. Res. 145:1996;324-330.
93. Buzzard K.A., Giaccia A.J., Killender M., Anderson R.L. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J. Biol. Chem. 273:1998;17147-17153.
94. Fuller B.J., Busza A.L., Proctor E. Possible resuscitation of liver function by hypothermic reperfusion in vitro after prolonged (24-h) cold preservation-a 31P NMR study. Transplantation. 50:1990;511-513.
95. Currie R.W., Tanguay R.M., Kingma J.G. Jr. Heat shock response and limitation of tissue necrosis during occlusion/reperfusion in rabbit hearts. Circulation. 87:1993;963-971.