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Research Articles

Fever, hyperthermia and the heat shock response

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Pages 423-435 | Received 01 Apr 2013, Accepted 21 May 2013, Published online: 17 Jul 2013

References

  • Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D. The adaptive value of fever. Infect Dis Clin North Am 1996;10:1–20
  • Horvath SM, Spurr GB, Hutt BK, Hamilton LH. Metabolic cost of shivering. J Appl Physiol 1956;8:595–602
  • Schumacker PT, Rowland J, Saltz S, Nelson DP, Wood LD. Effects of hyperthermia and hypothermia on oxygen extraction by tissues during hypovolemia. J Appl Physiol 1987;63:1246–52
  • Manthous CA, Hall JB, Olson D, Singh M, Chatila W, Pohlman A, et al. Effect of cooling on oxygen consumption in febrile critically ill patients. Am J Respir Crit Care Med 1995;151:10–14
  • Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu Rev Physiol 1999;61:243–82
  • Lindquist S. The heat-shock response. Annu Rev Biochem 1986;55:1151–91
  • Morimoto RI, Kline MP, Bimston DN, Cotto JJ. The heat-shock response: Regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 1997;32:17–29
  • Akerfelt M, Vihervaara A, Laiho A, Conter A, Christians ES, Sistonen L, et al. Heat shock transcription factor 1 localizes to sex chromatin during meiotic repression. J Biol Chem 2010;285:34469–76
  • McMillan DR, Xiao X, Shao L, Graves K, Benjamin IJ. Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J Biol Chem 1998;273:7523–8
  • Pirkkala L, Nykanen P, Sistonen L. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 2001;15:1118–31
  • Singh IS, Shah NG, Almutairy EA, Hasday JD. Role of HSF1 in infectious disease. In: Pockley AG, Santoro MG, Calderwood SK, eds. Prokaryotic and Eukaryotic Heat Shock Proteins in Infectious Disease. Vol. 4. Dordrecht: Springer, 2009, p. 31
  • Farkas T, Kutskova YA, Zimarino V. Intramolecular repression of mouse heat shock factor 1. Mol Cell Biol 1998;18:906–18
  • Zuo J, Rungger D, Voellmy R. Multiple layers of regulation of human heat shock transcription factor 1. Mol Cell Biol 1995;15:4319–30
  • Zhong M, Orosz A, Wu C. Direct sensing of heat and oxidation by Drosophila heat shock transcription factor. Mol Cell 1998;2:101–8
  • Sarge KD, Zimarino V, Holm K, Wu C, Morimoto RI. Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability. Genes Dev 1991;5:1902–11
  • Clos J, Rabindran S, Wisniewski J, Wu C. Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment. Nature 1993;364:252–5
  • Sarge KD. Regulation of HSF1 activation and HSP expression in mouse tissues under physiological stress conditions. Ann N Y Acad Sci 1998;851:112–16
  • Buckley BA, Owen ME, Hofmann GE. Adjusting the thermostat: The threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J Exp Biol 2001;204:3571–9
  • Jurivich DA, Sistonen L, Sarge KD, Morimoto RI. Arachidonate is a potent modulator of human heat shock gene transcription. Proc Natl Acad Sci USA 1994;91:2280–4
  • Morange M, Dubois MF, Bensaude O, Lebon P. Interferon pretreatment lowers the threshold for maximal heat-shock response in mouse cells. J Cell Physiol 1986;127:417–22
  • Guettouche T, Boellmann F, Lane WS, Voellmy R. Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 2005;6:4
  • Soncin F, Zhang X, Chu B, Wang X, Asea A, Ann Stevenson M, et al. Transcriptional activity and DNA binding of heat shock factor-1 involve phosphorylation on threonine 142 by CK2. Biochem Biophys Res Commun 2003;303:700–6
  • Wang X, Khaleque MA, Zhao MJ, Zhong R, Gaestel M, Calderwood SK. Phosphorylation of HSF1 by MAPK-activated protein kinase 2 on serine 121, inhibits transcriptional activity and promotes HSP90 binding. J Biol Chem 2006;281:782–91
  • Kim SA, Yoon JH, Lee SH, Ahn SG. Polo-like kinase 1 phosphorylates heat shock transcription factor 1 and mediates its nuclear translocation during heat stress. J Biol Chem 2005;280:12653–7
  • Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A, et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci USA 2006;103:45–50
  • Hong Y, Rogers R, Matunis MJ, Mayhew CN, Goodson ML, Park-Sarge OK, et al. Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J Biol Chem 2001;276:40263–7
  • Hasday JD, Singh IS. Fever and the heat shock response: distinct, partially overlapping processes. Cell Stress Chaperones 2000;5:471–80
  • Tomanek L, Somero GN. Interspecific- and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): Implications for regulation of hsp gene expression. J Exp Biol 2002;205:677–85
  • Gothard LQ, Ruffner ME, Woodward JG, Park-Sarge OK, Sarge KD. Lowered temperature set point for activation of the cellular stress response in T-lymphocytes. J Biol Chem 2003;278:9322–6
  • Ostberg JR, Kaplan KC, Repasky EA. Induction of stress proteins in a panel of mouse tissues by fever-range whole body hyperthermia. Int J Hyperthermia 2002;18:552–62
  • Cotto JJ, Kline M, Morimoto RI. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem 1996;271:3355–8
  • Bharadwaj S, Hnatov A, Ali A, Ovsenek N. Induction of the DNA-binding and transcriptional activities of heat shock factor 1 is uncoupled in Xenopus oocytes. Biochim Biophys Acta 1998;1402:79–85
  • Singh IS, Viscardi RM, Kalvakolanu I, Calderwood S, Hasday JD. Inhibition of tumor necrosis factor-alpha transcription in macrophages exposed to febrile range temperature. A possible role for heat shock factor-1 as a negative transcriptional regulator. J Biol Chem 2000;275:9841–8
  • Laszlo A, Moros EG, Davidson T, Bradbury M, Straube W, Roti Roti J. The heat-shock factor is not activated in mammalian cells exposed to cellular phone frequency microwaves. Radiat Res 2005;164:163–72
  • Tulapurkar ME, Asiegbu BE, Singh IS, Hasday JD. Hyperthermia in the febrile range induces HSP72 expression proportional to exposure temperature but not to HSF-1 DNA-binding activity in human lung epithelial A549 cells. Cell Stress Chaperones 2009;14:499–508
  • Roth J, Rummel C, Barth SW, Gerstberger R, Hubschle T. Molecular aspects of fever and hyperthermia. Immunol Allergy Clin North Am 2009;29:229–45
  • Roth J, Rummel C, Barth SW, Gerstberger R, Hubschle T. Molecular aspects of fever and hyperthermia. Neurol Clin 2006;24:421–39
  • Jiang Q, DeTolla L, van Rooijen N, Singh IS, Fitzgerald B, Lipsky MM, et al. Febrile-range temperature modifies early systemic tumor necrosis factor alpha expression in mice challenged with bacterial endotoxin. Infect Immun 1999;67:1539–46
  • Rice P, Martin E, He JR, Frank M, DeTolla L, Hester L, et al. Febrile-range hyperthermia augments neutrophil accumulation and enhances lung injury in experimental Gram-negative bacterial pneumonia. J Immunol 2005;174:3676–85
  • Gupta A, Cooper ZA, Tulapurkar ME, Potla R, Maity T, Hasday JD, et al. Toll-like receptor agonists and febrile range hyperthermia synergize to induce heat shock protein 70 expression and extracellular release. J Biol Chem 2013;288:2756–66
  • Hasday JD, Fairchild KD, Shanholtz C. The role of fever in the infected host. Microbes Infect 2000;2:1891–904
  • Bernheim HA, Bodel PT, Askenase PW, Atkins E. Effects of fever on host defense mechanisms after infection in the lizard Dipsosaurus dorsalis. Br J Exp Pathol 1978;59:76–84
  • Covert JB, Reynolds WW. Survival value of fever in fish. Nature 1977;267:43–5
  • Jiang Q, Cross AS, Singh IS, Chen TT, Viscardi RM, Hasday JD. Febrile core temperature is essential for optimal host defense in bacterial peritonitis. Infect Immun 2000;68:1265–70
  • Mackowiak PA, Browne RH, Southern PM, Jr., Smith JW. Polymicrobial sepsis: An analysis of 184 cases using log linear models. Am J Med Sci 1980;280:73–80
  • Hoefs JC, Canawati HN, Sapico FL, Hopkins RR, Weiner J, Montgomerie JZ. Spontaneous bacterial peritonitis. Hepatology 1982;2:399–407
  • Ahkee S, Srinath L, Ramirez J. Community-acquired pneumonia in the elderly: Association of mortality with lack of fever and leukocytosis. South Med J 1997;90:296–8
  • Sareh H, Tulapurkar ME, Shah NG, Singh IS, Hasday JD. Response of mice to continuous 5-day passive hyperthermia resembles human heat acclimation. Cell Stress Chaperones 2011;16:297–307
  • Tulapurkar ME, Hasday JD, Singh IS. Prolonged exposure to hyperthermic stress augments neutrophil recruitment to lung during the post-exposure recovery period. Int J Hyperthermia 2011;27:717–25
  • Lipke AB, Matute-Bello G, Herrero R, Kurahashi K, Wong VA, Mongovin SM, et al. Febrile-range hyperthermia augments lipopolysaccharide-induced lung injury by a mechanism of enhanced alveolar epithelial apoptosis. J Immunol 2010;184:3801–13
  • Lipke AB, Matute-Bello G, Herrero R, Wong VA, Mongovin SM, Martin TR. Death receptors mediate the adverse effects of febrile-range hyperthermia on the outcome of lipopolysaccharide-induced lung injury. Am J Physiol Lung Cell Mol Physiol 2011;301:L60–70
  • Hasday JD, Garrison A, Singh IS, Standiford T, Ellis GS, Rao S, et al. Febrile-range hyperthermia augments pulmonary neutrophil recruitment and amplifies pulmonary oxygen toxicity. Am J Pathol 2003;162:2005–17
  • D'Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, et al. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 2009;119:2898–913
  • Brenu EW, Staines DR, Tajouri L, Huth T, Ashton KJ, Marshall-Gradisnik SM. Heat shock proteins and regulatory T cells. Autoimmune Dis 2013;2013:813256
  • Mace TA, Zhong L, Kokolus KM, Repasky EA. Effector CD8+ T cell IFN-gamma production and cytotoxicity are enhanced by mild hyperthermia. Int J Hyperthermia 2012;28:9–18
  • Wachstein J, Tischer S, Figueiredo C, Limbourg A, Falk C, Immenschuh S, et al. HSP70 enhances immunosuppressive function of CD4(+)CD25(+)FoxP3(+) T regulatory cells and cytotoxicity in CD4(+)CD25(-) T cells. PLoS One 2012;7:e51747
  • Chen Q, Fisher DT, Clancy KA, Gauguet JM, Wang WC, Unger E, et al. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 2006;7:1299–308
  • Ellis GS, Carlson DE, Hester L, He JR, Bagby GJ, Singh IS, et al. G-CSF, but not corticosterone, mediates circulating neutrophilia induced by febrile-range hyperthermia. J Appl Physiol 2005;98:1799–804
  • Tulapurkar ME, Almutairy EA, Shah NG, He JR, Puche AC, Shapiro P, et al. Febrile-range hyperthermia modifies endothelial and neutrophilic functions to promote extravasation. Am J Respir Cell Mol Biol 2012;46:807–14
  • Hasday JD, Bannerman D, Sakarya S, Cross AS, Singh IS, Howard D, et al. Exposure to febrile temperature modifies endothelial cell response to tumor necrosis factor-alpha. J Appl Physiol 2001;90:90–8
  • Nagarsekar A, Greenberg RS, Shah NG, Singh IS, Hasday JD. Febrile-range hyperthermia accelerates caspase-dependent apoptosis in human neutrophils. J Immunol 2008;181:2636–43
  • Nagarsekar A, Tulapurkar ME, Singh IS, Atamas SP, Shah NG, Hasday JD. Hyperthermia promotes and prevents respiratory epithelial apoptosis through distinct mechanisms. Am J Respir Cell Mol Biol 2012;47:824–33
  • Lee CT, Repasky EA. Opposing roles for heat and heat shock proteins in macrophage functions during inflammation: A function of cell activation state? Front Immunol 2012;3:140
  • Ostberg JR, Taylor SL, Baumann H, Repasky EA. Regulatory effects of fever-range whole-body hyperthermia on the LPS-induced acute inflammatory response. J Leukoc Biol 2000;68:815–20
  • Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 2001;97:2727–33
  • Wang WC, Goldman LM, Schleider DM, Appenheimer MM, Subjeck JR, Repasky EA, Evans SS. Fever-range hyperthermia enhances L-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol 1998;160:961–9
  • Fisher DT, Chen Q, Skitzki JJ, Muhitch JB, Zhou L, Appenheimer MM, et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest 2011;121:3846–59
  • Singh V, Aballay A. Heat shock and genetic activation of HSF-1 enhance immunity to bacteria. Cell Cycle 2006;5:2443–6
  • Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, Richardson JA, et al. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. Embo J 1999;18:5943–52
  • Westwood JT, Clos J, Wu C. Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 1991;353:822–7
  • Trinklein ND, Chen WC, Kingston RE, Myers RM. Transcriptional regulation and binding of heat shock factor 1 and heat shock factor 2 to 32 human heat shock genes during thermal stress and differentiation. Cell Stress Chaperones 2004;9:21–8
  • Nagarsekar A, Hasday JD, Singh IS. CXC chemokines: A new family of heat-shock proteins? Immunol Invest 2005;34:381–98
  • Maity TK, Henry MM, Tulapurkar ME, Shah NG, Hasday JD, Singh IS. Distinct, gene-specific effect of heat shock on heat shock factor-1 recruitment and gene expression of CXC chemokine genes. Cytokine 2011;54:61–7
  • Singh IS, Gupta A, Nagarsekar A, Cooper Z, Manka C, Hester L, et al. Heat shock co-activates interleukin-8 transcription. Am J Respir Cell Mol Biol 2008;39:235–42
  • Dinh HK, Zhao B, Schuschereba ST, Merrill G, Bowman PD. Gene expression profiling of the response to thermal injury in human cells. Physiol Genomics 2001;7:3–13
  • Murray JI, Whitfield ML, Trinklein ND, Myers RM, Brown PO, Botstein D. Diverse and specific gene expression responses to stresses in cultured human cells. Mol Biol Cell 2004;15:2361–74
  • Sonna LA, Gaffin SL, Pratt RE, Cullivan ML, Angel KC, Lilly CM. Effect of acute heat shock on gene expression by human peripheral blood mononuclear cells. J Appl Physiol 2002;92:2208–20
  • Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012;150:549–62
  • Christians E, Davis AA, Thomas SD, Benjamin IJ. Maternal effect of Hsf1 on reproductive success. Nature 2000;407:693–4
  • Izu H, Inouye S, Fujimoto M, Shiraishi K, Naito K, Nakai A. Heat shock transcription factor 1 is involved in quality-control mechanisms in male germ cells. Biol Reprod 2004;70:18–24
  • Pirkkala L, Alastalo TP, Zuo X, Benjamin IJ, Sistonen L. Disruption of heat shock factor 1 reveals an essential role in the ubiquitin proteolytic pathway. Mol Cell Biol 2000;20:2670–5
  • Santos SD, Saraiva MJ. Enlarged ventricles, astrogliosis and neurodegeneration in heat shock factor 1 null mouse brain. Neuroscience 2004;126:657–63
  • Takaki E, Fujimoto M, Nakahari T, Yonemura S, Miyata Y, Hayashida N, et al. Heat shock transcription factor 1 is required for maintenance of ciliary beating in mice. J Biol Chem 2007;282:37285–92
  • Takaki E, Fujimoto M, Sugahara K, Nakahari T, Yonemura S, Tanaka Y, et al. Maintenance of olfactory neurogenesis requires HSF1, a major heat shock transcription factor in mice. J Biol Chem 2006;281:4931–7
  • Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007;130:1005–18
  • Xie Y, Chen C, Stevenson MA, Auron PE, Calderwood SK. Heat shock factor 1 represses transcription of the IL-1beta gene through physical interaction with the nuclear factor of interleukin 6. J Biol Chem 2002;277:11802–10
  • Xie Y, Zhong R, Chen C, Calderwood SK. Heat shock factor 1 contains two functional domains that mediate transcriptional repression of the c-fos and c-fms genes. J Biol Chem 2003;278:4687–98
  • Chen C, Xie Y, Stevenson MA, Auron PE, Calderwood SK. Heat shock factor 1 represses Ras-induced transcriptional activation of the c-fos gene. J Biol Chem 1997;272:26803–6
  • Cahill CM, Waterman WR, Xie Y, Auron PE, Calderwood SK. Transcriptional repression of the prointerleukin 1beta gene by heat shock factor 1. J Biol Chem 1996;271:24874–9
  • Singh IS, He JR, Hester L, Fenton MJ, Hasday JD. Bacterial endotoxin modifies heat shock factor-1 activity in RAW 264.7 cells: Implications for TNF-alpha regulation during exposure to febrile range temperatures. J Endotoxin Res 2004;10:175–84
  • Singh IS, He JR, Calderwood S, Hasday JD. A high affinity HSF-1 binding site in the 5'-untranslated region of the murine tumor necrosis factor-alpha gene is a transcriptional repressor. J Biol Chem 2002;277:4981–8
  • Cooper ZA, Singh IS, Hasday JD. Febrile range temperature represses TNF-alpha gene expression in LPS-stimulated macrophages by selectively blocking recruitment of Sp1 to the TNF-alpha promoter. Cell Stress Chaperones 2010;15:665–73
  • Cooper ZA, Ghosh A, Gupta A, Maity T, Benjamin IJ, Vogel SN, et al. Febrile-range temperature modifies cytokine gene expression in LPS-stimulated macrophages by differentially modifying NF-{kappa}B recruitment to cytokine gene promoters. Am J Physiol Cell Physiol 2010;298:C171–81
  • Wang J, He H, Yu L, Xia HH, Lin MC, Gu Q, et al. HSF1 down-regulates XAF1 through transcriptional regulation. J Biol Chem 2006;281:2451–9
  • Goldring CE, Reveneau S, Chantome A, Pance A, Fleury C, Hume DA, et al. Heat shock enhances transcriptional activation of the murine-inducible nitric oxide synthase gene. FASEB J 2000;14:2393–5
  • Inouye S, Fujimoto M, Nakamura T, Takaki E, Hayashida N, Hai T, et al. Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J Biol Chem 2007;282:33210–17
  • Rossi A, Trotta E, Brandi R, Arisi I, Coccia M, Santoro MG. AIRAP, a new human heat shock gene regulated by heat shock factor 1. J Biol Chem 2010;285:13607–15
  • Rossi A, Coccia M, Trotta E, Angelini M, Santoro MG. Regulation of cyclooxygenase-2 expression by heat: A novel aspect of heat shock factor 1 function in human cells. PLoS One 2012;7:e31304
  • Skaggs HS, Xing H, Wilkerson DC, Murphy LA, Hong Y, Mayhew CN, et al. HSF1-TPR interaction facilitates export of stress-induced HSP70 mRNA. J Biol Chem 2007;282:33902–7
  • Huang J, Nueda A, Yoo S, Dynan WS. Heat shock transcription factor 1 binds selectively in vitro to Ku protein and the catalytic subunit of the DNA-dependent protein kinase. J Biol Chem 1997;272:26009–16
  • Xie Y, Chen C, Stevenson MA, Hume DA, Auron PE, Calderwood SK. NF-IL6 and HSF1 have mutually antagonistic effects on transcription in monocytic cells. Biochem Biophys Res Commun 2002;291:1071–80
  • Singh U, Bongcam-Rudloff E, Westermark B. A DNA sequence directed mutual transcription regulation of HSF1 and NFIX involves novel heat sensitive protein interactions. PLoS One 2009;4:e5050
  • Yuan CX, Gurley WB. Potential targets for HSF1 within the preinitiation complex. Cell Stress Chaperones 2000;5:229–42
  • Lee YJ, Lee HJ, Lee JS, Jeoung D, Kang CM, Bae S, et al. A novel function for HSF1-induced mitotic exit failure and genomic instability through direct interaction between HSF1 and Cdc20. Oncogene 2008;27:2999–3009
  • Charette SJ, Lavoie JN, Lambert H, Landry J. Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol 2000;20:7602–12
  • Singhal SS, Yadav S, Drake K, Singhal J, Awasthi S. Hsf-1 and POB1 induce drug sensitivity and apoptosis by inhibiting Ralbp1. J Biol Chem 2008;283:19714–29
  • Li QL, Ju ZH, Huang JM, Li JB, Li RL, Hou MH, et al. Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA Cell Biol 2011;30:247–54
  • Bridges TM, Singh IS, Liggett SB, Hasday JD. Polymorphisms of heat shock factor-1: Genetic divesity in an evolutionarily conserved, multifunctional regulator gene. Am J Respir Crit Care Med 2011;183:A6018
  • Barenboim M, Zoltick BJ, Guo Y, Weinberger DR. MicroSNiPer: A web tool for prediction of SNP effects on putative microRNA targets. Hum Mutat 2010;31:1223–32
  • Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL. The Vienna RNA websuite. Nucleic Acids Res 2008;36:W70–4
  • Hashiguchi N, Ogura H, Tanaka H, Koh T, Nakamori Y, Noborio M, et al. Enhanced expression of heat shock proteins in activated polymorphonuclear leukocytes in patients with sepsis. J Trauma 2001;51:1104–9
  • Delogu G, Lo Bosco L, Marandola M, Famularo G, Lenti L, Ippoliti F, et al. Heat shock protein (HSP70) expression in septic patients. J Crit Care 1997;12:188–92
  • Wheeler DS, Fisher LE, Jr., Catravas JD, Jacobs BR, Carcillo JA, Wong HR. Extracellular hsp70 levels in children with septic shock. Pediatr Crit Care Med 2005;6:308–11
  • Njemini R, Lambert M, Demanet C, Mets T. Elevated serum heat-shock protein 70 levels in patients with acute infection: Use of an optimized enzyme-linked immunosorbent assay. Scand J Immunol 2003;58:664–9
  • Njemini R, Bautmans I, Onyema OO, Van Puyvelde K, Demanet C, Mets T. Circulating heat shock protein 70 in health, aging and disease. BMC Immunol 2011;12:24
  • Stulik J, Hernychova L, Macela A, Krocova Z, Kroca M. Production of stress-inducible form of heat-shock protein 70 in mouse peritoneal adherent cells after in vivo infection by Francisella tularensis. Folia Microbiol (Praha) 1999;44:306–10
  • Martinez J, Perez-Serrano J, Bernadina WE, Rodriguez-Caabeiro F. Shock response induced in rat brain and spleen during primary infection with Trichinella spiralis larvae. Parasitology 1999;118:605–13
  • Singleton KD, Serkova N, Beckey VE, Wischmeyer PE. Glutamine attenuates lung injury and improves survival after sepsis: Role of enhanced heat shock protein expression. Crit Care Med 2005;33:1206–13
  • Weiss YG, Bouwman A, Gehan B, Schears G, Raj N, Deutschman CS. Cecal ligation and double puncture impairs heat shock protein 70 (HSP-70) expression in the lungs of rats. Shock 2000;13:19–23
  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 2004;118:229–41
  • Kotsiopriftis M, Tanner JE, Alfieri C. Heat shock protein 90 expression in Epstein-Barr virus-infected B cells promotes gammadelta T-cell proliferation in vitro. J Virol 2005;79:7255–61
  • Brasier AR, Spratt H, Wu Z, Boldogh I, Zhang Y, Garofalo RP, et al. Nuclear heat shock response and novel nuclear domain 10 reorganization in respiratory syncytial virus-infected a549 cells identified by high-resolution two-dimensional gel electrophoresis. J Virol 2004;78:11461–76
  • Melcher A, Murphy S, Vile R. Heat shock protein expression in target cells infected with low levels of replication-competent virus contributes to the immunogenicity of adenoviral vectors. Hum Gene Ther 1999;10:1431–42
  • O'Reilly DA, Roberts JR, Cartmell MT, Demaine AG, Kingsnorth AN. Heat shock factor-1 and nuclear factor-kappaB are systemically activated in human acute pancreatitis. JOP 2006;7:174–84
  • Ethridge RT, Ehlers RA, Hellmich MR, Rajaraman S, Evers BM. Acute pancreatitis results in induction of heat shock proteins 70 and 27 and heat shock factor-1. Pancreas 2000;21:248–56
  • McGrath LB, Locke M, Cane M, Chen C, Ianuzzo CD. Heat shock protein (HSP 72) expression in patients undergoing cardiac operations. J Thorac Cardiovasc Surg 1995;109:370–6
  • Taggart DP, Bakkenist CJ, Biddolph SC, Graham AK, McGee JO. Induction of myocardial heat shock protein 70 during cardiac surgery. J Pathol 1997;182:362–6
  • Calderwood SK, Mambula SS, Gray PJ, Jr., Theriault JR. Extracellular heat shock proteins in cell signaling. FEBS Lett 2007;581:3689–94
  • De Nardo D, Masendycz P, Ho S, Cross M, Fleetwood AJ, Reynolds EC, et al. A central role for the Hsp90.Cdc37 molecular chaperone module in interleukin-1 receptor-associated-kinase-dependent signaling by toll-like receptors. J Biol Chem 2005;280:9813–22
  • Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 2002;277:15107–12
  • Tsan MF, Gao B. Heat shock proteins and immune system. J Leukoc Biol 2009;85:905–10
  • Gao B, Tsan MF. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor alpha release by murine macrophages. J Biol Chem 2003;278:174–9
  • Zheng H, Nagaraja GM, Kaur P, Asea EE, Asea A. Chaperokine function of recombinant Hsp72 produced in insect cells using a baculovirus expression system is retained. J Biol Chem 2010;285:349–56
  • Wang R, Kovalchin JT, Muhlenkamp P, Chandawarkar RY. Exogenous heat shock protein 70 binds macrophage lipid raft microdomain and stimulates phagocytosis, processing, and MHC-II presentation of antigens. Blood 2006;107:1636–42
  • Vega VL, Rodriguez-Silva M, Frey T, Gehrmann M, Diaz JC, Steinem C, et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol 2008;180:4299–307
  • Asea A. Heat shock proteins and toll-like receptors. Handb Exp Pharmacol 2008;183:111–27
  • Aneja R, Odoms K, Dunsmore K, Shanley TP, Wong HR. Extracellular heat shock protein-70 induces endotoxin tolerance in THP-1 cells. J Immunol 2006;177:7184–92
  • Stocki P, Dickinson AM. The immunosuppressive activity of heat shock protein 70. Autoimmune Dis 2012;2012:617213
  • Pockley AG, Muthana M, Calderwood SK. The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 2008;33:71–9
  • Torigoe T, Tamura Y, Sato N. Heat shock proteins and immunity: Application of hyperthermia for immunomodulation. Int J Hyperthermia 2009;25:610–16
  • Borges TJ, Wieten L, van Herwijnen MJ, Broere F, van der Zee R, Bonorino C, et al. The anti-inflammatory mechanisms of Hsp70. Front Immunol 2012;3:95
  • Hunter-Lavin C, Davies EL, Bacelar MM, Marshall MJ, Andrew SM, Williams JH. Hsp70 release from peripheral blood mononuclear cells. Biochem Biophys Res Commun 2004;324:511–17
  • Hightower LE, Guidon PT, Jr. Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol 1989;138:257–66
  • Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol 2000;12:1539–46
  • Mambula SS, Calderwood SK. Heat induced release of Hsp70 from prostate carcinoma cells involves both active secretion and passive release from necrotic cells. Int J Hyperthermia 2006;22:575–85
  • Evdonin AL, Martynova MG, Bystrova OA, Guzhova IV, Margulis BA, Medvedeva ND. The release of Hsp70 from A431 carcinoma cells is mediated by secretory-like granules. Eur J Cell Biol 2006;85:443–55
  • Mambula SS, Stevenson MA, Ogawa K, Calderwood SK. Mechanisms for Hsp70 secretion: crossing membranes without a leader. Methods 2007;43:168–75
  • Mambula SS, Calderwood SK. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 2006;177:7849–57
  • Edelman DA, Jiang Y, Tyburski JG, Wilson RF, Steffes CP. Lipopolysaccharide up-regulates heat shock protein expression in rat lung pericytes. J Surg Res 2007;140:171–6
  • Hirsh MI, Hashiguchi N, Chen Y, Yip L, Junger WG. Surface expression of HSP72 by LPS-stimulated neutrophils facilitates gammadeltaT cell-mediated killing. Eur J Immunol 2006;36:712–21
  • Unoshima M, Nishizono A, Takita-Sonoda Y, Iwasaka H, Noguchi T. Effects of zinc acetate on splenocytes of endotoxemic mice: Enhanced immune response, reduced apoptosis, and increased expression of heat shock protein 70. J Lab Clin Med 2001;137:28–37
  • Ofenstein JP, Heidemann S, Juett-Wilstermann A, Sarnaik A. Expression of stress proteins HSP 72 & HSP 32 in response to endotoxemia. Ann Clin Lab Sci 2000;30:92–8
  • Flohe S, Dominguez Fernandez E, Ackermann M, Hirsch T, Borgermann J, Schade FU. Endotoxin tolerance in rats: Expression of TNF-alpha, IL-6, IL-10, VCAM-1 and HSP 70 in lung and liver during endotoxin shock. Cytokine 1999;11:796–804
  • Murapa P, Gandhapudi S, Skaggs HS, Sarge KD, Woodward JG. Physiological fever temperature induces a protective stress response in T lymphocytes mediated by heat shock factor-1 (HSF1). J Immunol 2007;179:8305–12
  • Sarge KD, Bray AE, Goodson ML. Altered stress response in testis. Nature 1995;374:126
  • Sarge KD. Male germ cell-specific alteration in temperature set point of the cellular stress response. J Biol Chem 1995;270:18745–8

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