Abstract
In 1962 Ferruccio Ritossa described a distinct, hyperthermia-dependent puffing pattern in the giant chromosomes from the salivary glands of Drosophila (1). Subsequent investigations linked this puffing pattern with the expression of a specific group of proteins that were fittingly named “heat shock proteins,” and the expression of these proteins in response to hyperthermia was termed the “heat shock response.” During the ensuing four decades the field of heat shock response biology has grown immensely and it has become evident that all organisms have the capacity to induce the heat shock response, which is now recognized as having fundamental importance in both cellular biology and medicine. One of the more important functional consequences of the heat shock response is its ability to confer cytoprotection against a variety of cellular and tissue injuries relevant to clinical medicine, including ischemia-reperfusion injury, inflammatory injury, and oxidant-mediated injury.
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References
Ritossa, F.M. (1962) A new puffing pattern induced by a temperature shock and DNP in Drosophila. Experientia 18, 571-573
Welch, W.J. (1992) Mammalian stress response: cell physiology structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72, 1063-1081
Morimoto, R.I., and Santoro, M.G. (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16, 833-838
Ciocca, D.R., Oestereich, S., Chamness, G.C., McGuire, W.L., and Fuqua, S.A.W. (1993) Biological and clinical implications of heat shock protein 27000 (Hsp27): a review. J Natl Cancer Inst 85, 1558-1570
DeMaio, A. (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11, 1-12
Leppa, S., and Sistonen, L. (1997) Heat shock response pathophysiological implications. Ann Med 29, 73-78
Wong, H.R., and Wispé, J.R. (1997) The stress response and the lung. Am J Physiol 273, L1-L9
Wong, H.R. (1998) Potential protective role of the heat shock response against sepsis. New Horiz 6, 194-200
Lanks, K.W. (1986) Modulators of the eukaryotic heat shock response. Exp Cell Res 165, 1-10
Wong, H.R., Finder, J.D., Wasserloos, K., and Pitt, B.R. (1995) Expression of inducible nitric oxide synthase in cultured rat pulmonary artery smooth muscle cells is inhibited by the heat shock response. Am J Physiol 269, L843-L848
Eaves-Pyles, T., Wong, H.R., and Alexander, J.W. (2000) Sodium arsenite induces heat shock protein-70 in the gut and decreases bacterial translocation in a burned mouse model with gut-derived sepsis. Shock 13, 314-319
Thomas, S.C., Ryan, M.A., Shanley, T.P., and Wong, H.R. (1998) Induction of the stress response with prostaglandin-A, increases I-κBα gene expression. FASEB J 12, 1371-1378
Rossi, A., Elia, G., and Santoro, M.G. (1997) Inhibition of nuclear factor κB by prostaglandin A1: an effect associated with heat shock transcription factor activation. Proc Natl Acad Sci USA 94, 746-750
Santoro, M.G., Garaci, E., and Amici, C. (1989) Prostaglandins with antiproliferative activity induce the synthesis of a heat shock protein in human cells. Proc Natl Acad Sci USA 86, 8407-8411
Urayama, S., Musch, M.W., Retsky, J., Madonna, M.B., Straus, D., and Chang, E.B. (1998) Dexamethasone protection of rat intestinal epithelial cells against oxidant injury is mediated by induction of heat shock protein 72. J Clin Invest 102, 1860-1865
Sun, L., Chang, J., Kirchhoff, S.R., and Knowlton, A.A. (2000) Activation of HSF and selective increase in heat shock proteins by acute dexamethasone treatment. Am J Physiol 278, H1091-H1097
Vigh, L., Literati, P.N., Horvath, I., Torok, Z., Balogh, G., Glatz, A., Kovacs, E., Boros, I., Ferdinancy, P., Farkas, B., Jaszlits, L., Jednakovits, A., Korvanyi, L., and Maresca, B. (1997) Bimoclomol: a nontoxic, hydroxylamine derivative with stress protein-inducing activity and cytoprotective effects. Nat Med 3, 1150-1154
Morris, S.D., Cumming, D.V.E., Latchman, D.S., and Yellon, D.M. (1996) Specific induction of the 70-kD heat stress proteins by the tyrosine kinase inhibitor herbimycin-A protects rat neonatal cardiomyocytes. J Clin Invest 97, 706-712
Conde, A.G., Lau, S.S., Dillmann, W.H., and Mestril, R. (1997) Induction of heat shock proteins by tyrosine kinase inhibitors in rat cardiomyocytes and myogenic cells confers protection against simulated ischemia. J Mol Cell Cardiol 29, 1927-2938
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
Lee, B.S., Chen, J., Angelidis, C., Jurivich, D.A., and Morimoto, R.I. (1995) Pharmacological modulation of heat shock factor 1 by antiinflammatory drugs results in protection against stress-induced cellular damage. Proc Natl Acad Sci USA 1995, 7207-7211
Rossi, A., Elia, G., and Santoro, M.G. (1998) Activation of the heat shock factor 1 by serine protease inhibitors. J Biol Chem 273, 16446-16452
DeMeester, S. L., Buchman, T. G., Qiu, Y., Dunnigan, K., Hotchkiss, R. S., Karl, I.E., and Cobb, J.P. (1998) Pyrrolidine dithiocarbamate activates the heat shock response and thereby induces apoptosis in primed endothelial cells. Shock 10, 1-6
Wischmeyer, P.E., Musch, M.W., Madonna, M.B., Thisted, R., and Chang, E.B. (1997) Glutamine protects intestinal epithelial cells: role of inducible HSP70. Am J Physiol 272, G879-G884
Wagner, M., Hermanns, I., Bittinger, F., and Kirkpatrick, C.J. (1999) Induction of stress proteins in human endothelial cells by heavy metal ions and heat shock. Am J Physiol 277, L1026-L1033
Mivechi, N.F., Murai, T., and Hahn, G.M. (1994) Inhibitors of tyrosine and Ser/Thr phosphatases modulate the heat shock response. J Cell Biochem 54, 186-197
Chang, N.T., Huang, L.E., and Liu, A.Y. (1993) Okadaic acid markedly potentiates the heat-induced hsp 70 promoter activity. J Biol Chem 268, 1436-1439
Kato, K., Ito, H., Kamei, K., and Iwamoto, I. (1998) Stimulation of the stress-induced expression of stress proteins by curcumin in cultured cells and in rat tissues in vivo. Cell Stress Chaperones 3, 152-160
Hirakawa, T., Rokutan, K., Nikawa, T., and Kishi, K. (1996) Geranylgeranylacetone induces heat shock proteins in cultured guinea pig gastric mucosal cells and rat gastric mucosa. Gastroenterology 111, 345-357
Schoeniger, L.O., Curtis, W., Esnaola, N.F., Beck, S.C., Gardner, T., and Buchman, T. (1994) Myocardial heat shock gene expression in pigs is dependent on superoxide anion generated at reperfusion. Shock 1, 31-35
Fincato, G., Polentarutti, N., Sica, A., Mantovani, A., and Colotta, F. (1991) Expression of a heat-inducible gene of hsp70 family in human myelomonocytic cells: regulation by bacterial products and cytokines. Blood 77, 579-586
Aucoin, M.M., Barhoumi, R., Kochevar, D.T., Granger, H.J., and Burghardt, R.C. (1995) Oxidative injury of coronary venular endothelial cells depletes intracellular glutathione and induces HSP 70 mRNA. Am J Physiol 268, H1651-H1658
Kukreja, R.C., Kontos, M.C., Loesser, K.E., Batra, S.K., Qian, Y.Z., Gbur, C.J., Naseem, S.A., Jesse, R.L., and Hess, M.L. (1994) Oxidant stress increases heat shock protein 70 mRNA in isolated perfused rat heart. Am J Physiol 267, H2213-H2219
Folch, E., Closa, D., Neco, P., Sole, S., Planas, A., Gelpi, E., and Rosello-Catafau, J. (2000) Pancreatitis induces HSP72 in the lung: role of neutrophils and xanthine oxidase. Biochem Biophys Res Commun 273, 1078-1083
Bonay, M., Soler, P., Riquet, M., Battesti, J.P., Hance, A.J., and Tazi, A. (1994) Expression of heat shock proteins in human lung and lung cancers. Am J Respir Cell Mol Biol 10, 453-461
Durand, P., Bachelet, M., Brunet, F., Richard, M.J., Dhainaut, J.F., Dall’Ava, J., and Polla, B.S. (2000) Inducibility of the 70 kD heat shock protein in peripheral blood monocytes is decreased in human acute respiratory distress syndrome and recovers over time. Am J Respir Crit Care Med 161, 286-292
Kindas-Mugge, I., Pohl, W.R., Zavadova, E., Kohn, H.D., Fitzal, S., Kummer, F., and Micksche, M. (1996) Alveolar macrophages of patients with adult respiratory distress syndrome express high levels of heat shock protein 72 mRNA. Shock 5, 184-189
Polla, B.S., Kantengwa, S., Gleich, G.J., Kondo, M., Reimert, C.M., and Junod, A.F. (1993) Spontaneous heat shock protein synthesis by alveolar macrophages in interstitial lung disease associated with phagocytosis of eosinophils. Eur Respir J 6, 483-488
Schroeder, S., Lindemann, C., Hoeft, A., Putensen, C., Decker, D., Ruecker, A.A., and Stuber, F. (1999) Impaired inducibility of heat shock protein 70 in peripheral blood lymphocytes of patients with severe sepsis. Crit Care Med 27, 1080-1084
Schroeder, S., Bischoff, J., Lehmann, L.E., Hering, R., Spiegel, T.V., Putensen, C., Hoeft, A., and Stuber, E. (1999) Endotoxin inhibits heat shock protein 70 (HSP70) expression in peripheral blood mononuclear cells of patients with severe sepsis. Intensive Care Med 25, 52-57
Vignola, A.M., Chanez, P., Polla, B.S., Vic, P., Godard, P., and Bousquet, J. (1995) Increased expression of heat shock protein 70 on airway cells in asthma and chronic bronchitis. Am J Respir Cell Mol Biol 13, 683-691
Wright, B. H., Corton, J. M., El-Nahas, A.M., Wood, R.F., and Pockley, A.G. (2000) Elevated levels of circulating heat shock protein 70 (Hsp70) in peripheral and renal vascular disease. Heart Vessels 15, 18-22
Shehata, S.M., Sharma, H.S., Mooi, W.J., and Tibboel, D. (1999) Expression patterns of heat shock proteins in lungs of neonates with congenital diaphragmatic hernia. Arch Surg 134, 1248-1253
Li, G.C., Li, L., Liu, Y.-K., Mak, J.Y., Chen, L., and Lee, W.M.F. (1991) Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc Natl Acad Sci 88, 1681-1685
Chi, S.H., and Mestril, R. (1996) Stable expression of a human hsp70 gene in a rat myogenic cell line confers protection against endotoxin. Am J Physiol 270, C1017-1021
Marber, M.S., Mestril, R., Chi, S.H., Sayen, M.R., Yellon, D.M., and Dillman, W.H. (1995) 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, 1446-1456
Plumier, J.-C.L., Ross, B.M., Currie, R.W., Angelidis, C.E., Kazlaris, H., Kollias, G., and Pagoulatos, G.N. (1995) Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 95, 1854-1860
Wong, H.R., Mannix, R.J., Rusnak, J.M., Boota, A., Zar, H., Watkins, S. C., Lazo, J.S., and Pitt, B.R. (1996) The heat shock response attenuates lipopolysaccharide-mediated apoptosis in cultured sheep pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 15, 745-751
Wong, H.R., Menendez, I.Y., Ryan, M.A., Denenberg, A., and Wispé, J. R. (1998) Increased expression of heat shock protein-70 protects human respiratory epithelium against hyperoxia. Am J Physiol 275, L836-L841
McMillan, D.R., Xiao, X., Shao, L., Graves, K., and Benjamin, I.J. (1998) Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J Biol Chem 273, 7523-7528
Xiao, X.Z., Zuo, X.X., Davis, A.A., McMillan, D.R., Curry, B.B., Richardson, J.A., and Benjamin, I.J. (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J 18, 5943-5952
Wang, J.R., Xiao, X.Z., Huang, S.N., Luo, F.J., You, J.L., Luo, H., and Luo, Z.Y. (1996) Heat shock pretreatment prevents hydrogen peroxide injury of pulmonary endothelial cells and macrophages in culture. Shock 6, 134-141
Wong, H.R., Ryan, M., Menendez, I.Y., Denenberg, A., and Wispé, J.R. (1997) Heat shock protein induction protects human respiratory epithelium against nitric oxide-mediated cytotoxicity. Shock 8, 213-218
Wong, H.R., Ryan, M., Gebb, S., and Wispé, J.R. (1997) Selective and transient in vitro effects of heat shock on alveolar type II cell gene expression. Am J Physiol 272, L132-L138
Wong, H.R., Menendez, I.Y., Ryan, M.A., Denenberg, A., and Wispé, J.R. (1998) Increased expression of heat shock protein-70 protects human respiratory epithelium against hyperoxia. Am J Physiol 275, L836-L841
Villar, J., Edelson, J.D., Post, M., Mullen, J.B., and Slutsky, A.S. (1993) Induction of heat stress proteins is associated with decreased mortality in an animal model of acute lung injury. Am Rev Respir Dis 147, 177-181
Villar, J., Riberio, S.P., Mullen, J.B.M., Kuliszewski, M., Post, M., and Slutsky, A.S. (1994) Induction of the heat shock response reduces mortality rate and organ damage in a sepsis-induced acute lung injury model. Crit Care Med 22, 914-922
Koh, Y., Lim, C.M., Kim, M.J., Shim, T.S., Lee, S.D., Kim, W.S., Kim, D.S., and Kim, W.D. (1999) Heat shock response decreases endotoxin-induced acute lung injury in rats. Respirology 4, 325-330
Javadpour, M., Kelly, C.J., Chen, G., Stokes, K., Leahy, A., and Bouchier-Hayes, D.J. (1998) Thermotolerance induces heat shock protein 72 expression and protects against ischaemia-reperfusion-induced lung injury. Br J Surg 85, 943-946
Waddell, T.K., Hirai, T., Piovesan, J., Oka, T., Puskas, J.D., Patterson, G.A., and Slutsky, A.S. (1994) The effect of heat shock on immediate post-preservation lung function. Clin Invest Med 17, 405-413
Hiratsuka, M., Yano, M., Mora, B.N., Nagahiro, I., Cooper, J.D., and Patterson, G.A. (1998) Heat shock pretreatment protects pulmonary isografts from subsequent ischemia-reperfusion injury. J Heart Lung Transplant 17, 1238-1246
Hiratsuka, M., Mora, B.N., Yano, M., Mohanakumar, T., and Patterson, G.A. (1999) Gene transfer of heat shock protein 70 protects lung grafts from ischemia-reperfusion injury. Ann Thoracic Surg 67, 1421-1427
Ayad, O., Stark, J.M., Fiedler, M.A., Menendez, I.Y., Ryan, M.A., and Wong, H.R. (1998) The heat shock response inhibits RANTES gene expression in cultured human lung epithelium. J Immunol 161, 2594-2599
Snyder, Y.L., Guthrie, L., Evans, G.F., and Zuckerman, S. (1992) Transcriptional inhibition of endotoxin-induced monokine synthesis following heat shock in murine peritoneal macrophages. J Leuko Biol 51, 181-187
Schmidt, J.A., and Abdulla, E. (1988) Down-regulation of IL-1β biosynthesis by inducers of the heat-shock response. J Immunol 141, 2027-2034
Cahil, C.M., Waterman, W.R., Xie, Y., Auron, P.E., and Calderwood, S.K. (1996) Transcriptional repression of the prointerleukin-1β gene by heat shock factor 1. J Biol Chem 271, 24874-24879
Feinstein, D.L., Galea, E., Aquino, D.A., Li, G.C., Xu, H., and Reis, D.J. (1996) Heat shock protein 70 suppresses astroglial-inducible nitric oxide synthase expression by decreasing NF-κB activation. J Biol Chem 271, 17224-12732
Baldwin, A.S. (1996) The NF-κB and IκB proteins: new discoveries and insights. Annu Rev Immunol 14, 649-681
Ghosh, S., May, M.J., and Koop, E.B. (1998) NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16, 225-260
Wong, H.R., Ryan, M., and Wispé, J.R. (1997) The heat shock response inhibits inducible nitric oxide synthase gene expression by blocking Iκ-B degradation and NF-κB nuclear translocation. Biochem Biophys Res Comm 231, 257-263
Wong, H.R., Ryan, M., and Wispé, J.R. (1997) Stress response decreases NF-κB nuclear translocation and increases I-κBα and expression in A549 cells. J Clin Invest 99, 2423-2428
Pritts, T.A., Want, Q., Sun, X., Moon, M.R., Fischer, D.R., Fischer, J.E., Wong, H.R., and Hasselgren, P.O. (2000) Induction of the stress response in vivo decreases NF-κB activity in jejunal mucosa of endotoxemic mice. Arch Surg 135, 860
Shanley, T.P., Ryan, M.A., Eaves-Pyles, T., and Wong, H.R. (2000) Heat shock inhibits phosphorylation of I-kappaBalpha. Shock 14, 447-450
Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18, 621-663
Curry, H.A., Clemens, R.A., Shah, S., Bradbury, C.M., Botero, A., Goswami, P., and Gius, D. (1999) Heat shock inhibits radiation-induced activation of NF-κB via inhibition of I-κB kinase. J Biol Chem 274, 23061-23067
Yoo, C.G., Lee, S., Lee, C.T., Kim, Y.W., Han, S.K., and Shim, Y.S. (2000) Antiinflammatory effect of heat shock protein induction is related to stabilization of IκBα through preventing IκB kinase activation in respiratory epithelial cells. J Immunol 164, 5416-5423
Wong, H.R., Ryan, M.A., Menendez, I.Y., and Wispé, J.R. (1999) Heat shock activates the I-κBα promoter and increases I-κBα mRNA expression in BEAS-2B cells. Cell Stress Chaperones 4, 1-7
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Wong, H.R. (2001). The Heat Shock Response and Heat Shock Protein 70: Cytoprotection in Acute Lung Injury. In: Wong, H.R., Shanley, T.P. (eds) Molecular Biology of Acute Lung Injury. Molecular and Cellular Biology of Critical Care Medicine, vol 1. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1427-5_18
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DOI: https://doi.org/10.1007/978-1-4615-1427-5_18
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