Advanced search
Publication Cover
International Journal of Hyperthermia Volume 17, 2001 - Issue 5
Submit an article Journal homepage
201
Views
31
CrossRef citations to date
0
Altmetric
Research Article

Whole body hyperthermia and preconditioning of the heart: basic concepts, complexity, and potential mechanisms

L. Xi, D. Tekin, P. Bhargava, R. C. Kukreja
Pages 439-455 | Published online: 09 Jul 2009

  • Henderson MA, Pettigrew RT. Induction of controlled hyperthermia in treatment of cancer. Lancet 1971; 1: 1275-8.
  • Larkin JM, Edwards WS, Smith DE. Total body hyperthermia and preliminary results in human neoplasms. Surg Forum 1976; 27: 121-3.
  • Bull JM, Lees D, Schuette W, Whang-Pang J, Smith R, Bynum G, Atkinson ER, Gottdiener JS, Gralnick HR, Shawker TH, DeVita VT. Whole body hyperthermia: a phase I trial of a potential adjuvant to chemotherapy. Ann Intern Med 1979; 90: 317-23.
  • Parks LC, Minaberry D, Smith DP, Neely W. Treatment of far-advanced bronchogenic carcinoma by extracorporealty induced systemic hyperthermia. J Thorac Cardiovasc Surg 1979; 78: 883-92.
  • Dewhirst MW, Prosnitz L, Thrall D, Prescott D, Clegg S, Charles C, MacFall J, Rosner G, Samulski T, Gillette E, LaRue S. Hyperthermic treatment of malignant diseases: current status and a view toward the future. Semin Oncol 1997; 24: 616-25.
  • Welch WJ. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physio! Rev 1992; 72: 1063-81.
  • Li GC, Mivechi NF, Weitzel G. Heat shock proteins, thermotolerance, and their relevance to clinical hyperthermia Int J Hyperthermia 1995; 11: 459-88.
  • Moseley PL. Heat shock proteins and heat adaptation of the whole organism. J Appl Physiol 1997; 83: 1413-7.
  • Hotchkiss R, Nunnalty I, Lindquist S, Taulien J, Perdrizet G, Karl I. Hyperthermia protects mice against the lethal effects of endotoxin. Am J Physiol 1993; 265: R1447-57.
  • Yang RC, Yang SL, Chen SW, Lai SL, Chen SS, Chiang CS. Previous heat shock treatment attenuates bicuculline-induced convulsions in rats. Exp Brain Res 1996; 108, 18-22.
  • Kimoto S, Yamamoto Y, Yamagami K, Ishikawa Y, Kume M, Yamamoto H, Ozaki N, Yamaoka Y. The augmentative effect of repeated heat shock preconditioning on the production of heat shock protein 72 and on ischemie tolerance in rat liver tissue. Int J Hyperthermia 2000; 16: 247-61.
  • Villar J, Edelson JD, Post M, Mullen JB, Slutsky AS. Induction of heat stress proteins is associated with decreased mortality in an animal model of acute lung injury. Am Rev Respir Dis 1993; 147: 177-81.
  • Stojadinovic A, Kiang J, Smallridge R, Galloway R, Shea-Donohue T. Induction of heat-shock protein 72 protects against ischemia/reperfusion in rat small intestine. Gastroenterobgy 1995; 109: 505-15.
  • Lepore DA, Hurley JV, Stewart AG, Morrison WA, Anderson RL. Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle & Nerve 2000; 23: 1847-55.
  • Currie RW, Karmazyn M, Kloc M, Mailer K. Heat-shock response is associated with enhanced postischemic ventricular recovery. Circ Res 1988; 63: 543-9.
  • Currie RW, Karmazyn M. Improved post-ischemic ventricular recovery in the absence of changes in energy metabolism in working rat hearts after heat shock. J MoI Cell Cordial 1990; 22: 631-6.
  • Karmazyn M, Mailer K, Currie RW. Acquisition and decay of heat-shock-enhanced ventricular recovery. Am J Physiol 1990; 259: H424-31.
  • Donnelly TJ, Sievers RE, Vissern FLJ, Welch WJ, Wolfe CL. Heat shock protein induction in rat hearts: a role for improved myocardial salvage after ischemia and reperfusion? Circulation 1992; 85: 769-78.
  • Yellon DM, Iliodromitis E, Latchman DS, Van Winkle D, Downey JM, Williams FM, Williams TJ. Whole body heat stress fails to limit infarct size in the reperfused rabbit heart. Cardiovasc Res 1992; 26: 342-6.
  • Yellon DM, Pasini E, Cargnoni A, Marber MS, Latchman DS, Ferrari R. The protective role of heat stress in the ischemic and reperfused rabbit myocardium. J MoI Cell Cordial 1992; 24: 895-907.
  • Currie RW, Tanguay RM, Kingma Jr JG. Heat-shock response and limitation of tissue necrosis during occlusion/reperfusion in rabbit hearts. Circulation 1993; 87: 963-71.
  • Marber MS, Latchman DS, Walker JM, Yellon DM. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 1993; 88: 1264-72.
  • Marber MS, Walker JM, Latchman DS, Yellon DM. Attenuation by heat stress of a submaximal calcium paradox in the rabbit heart J MoI Cell Cordial 1993; 25: 1119-26.
  • Walker DM, Pasini E, Kucukoghi S, Marber MS, Iliodromites E, Ferrari R, Yellon DM. Heat stress limits infarct size in the isolated perfused rabbit heart Cardiovasc Res 1993; 27: 962-7.
  • Wall SR, Fliss H, Korecky B. Role of catalase in myocardial protection against ischemia in heat shocked rats. MoI Cell Biochem 1993; 129: 187-94.
  • Steare SE, Yellon DM. The protective effect of heat stress against reperfusion arrhythmias in the rat. J MoI Cell Cordial 1993; 25: 1471-81.
  • Hutter MM, Sievers RE, Barbosa V, Wolfe CL. Heat-shock protein induction in rat hearts: a direct correlation between the amount of heat-shock protein induced and the degree of myocardial protection. Circulation 1994; 89: 355-60.
  • Amrani M, Corbett J, Alien NJ, O'Shea J, Boateng SY, May AJ, Dunn MJ, Yacoub MH. Induction of heat-shock proteins enhances myocardial and endothelial functional recovery after prolonged cardioplegic arrest. Ann Thorac Surg 1994; 57: 157-60.
  • Cornelussen R, Spiering W, Webers JHG, de Bruin LGA, Reneman RS, Van der Vusse GJ, Snoeckx LHEH. Heat shock improves ischemic tolerance of hypertrophie! rat hearts. Am J Physiol 1994; 267: H1941-7.
  • Auyeung Y, Sievers RE, Weng D, Barbosa V, Wolfe CL. Catalase inhibition with 3-amino-l,2,4-triazole does not abolish infarct size reduction in heat-shocked rats. Circulation 1995; 92: 3318-22.
  • Cornelussen R, Van Der Vusse GJ, Reneman RS, Snoeckx LHEH. Inability of the heat-shocked heart to adjust its pre-ischemic and post-ischemc performance to variable loading conditions. J MoI Cell Cordial 1996; 28: 291-8.
  • Kontos MC, Shipley JB, Kukreja RC. 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 MoI Cell Cordial 1996; 28: 1885-94.
  • Kingma Jr JG, Simard D, Rouleau JR, Tanguay RM, Currie RW. Effect of 3-aminotriazole on hyperthermia-mediated cardioprotection in rabbits. Am J Physiol 1996; 270:1165-71.
  • Yamashita N, Hoshida S, Nishida M, Igarashi J, Aoki K, Hori M, Kuzuya T, Tada M. Time course of tolerance to ischemia-reperfusicn injury and induction of heat shock protein 72 by heat stress in the rat heart J MoI Cell Cordial 1997; 29: 1815-21.
  • Cornelussen R, Garnier AV, York MM, Geurten P, Reneman RS, Van der Vusse GJ, Snoeckx LHEH. Heat stress protects aged hypertrophied and nonhypertrophied rat hearts against ischemic damage. Am J Physiol 1997; 273: H333-41.
  • 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 1997; 99: 1645-50.
  • Hoag JB, Qian Y-Z, Nayeem MA, D'Angelo M, Kukreja RC. ATP-sensitive potassium channel mediates delayed ischemic protection by heat stress in rabbit heart Am J Physiol 1997; 273: H2458-64.
  • Joyeux M, Baxter GF, Thomas DL, Ribuot C, Yellon DM. Protein kinase C is involved in resistance to myocardial infarction induced by heat stress. J MoI Cell Cordial 1997; 29: 3311-9.
  • O'Brien PJ, Li GO. Locke M, Klabunde RE, lanuzzo CD. Compensatory up-regulation of cardiac SR Ca2+ -pump by heat-shock counteracts SR Ca2+ -channel activation by ischemia/reperfusion. MoI Cell Biochem 1997; 173: 135-43.
  • Pell TJ, Yellon DM, Goodwill RW, Baxter GF. Myocardial ischemic tolerance following heat stress is abolished by ATP-sensitive potassium channel blockade. Cardiovasc Drugs Ther 1997; 11: 679-86.
  • Saganek LJ, Ignasiak DP, Batley BL, Potoczak RE, Dodd G, Gallagher KP. Heat stress increases cardiac HSP72i but fails to reduce myocardial infarct size in rabbits 24 hours later. Basic Res Cordial 1997; 92: 331-8.
  • Cornelussen R, Gamier AV, Van Der Vusse GJ, Reneman RS, Snoeckx LHEH. Biphasic effect of heat stress pretreatment on ischemic tolerance of isolated rat hearts. J Mol Cell Cordial 1998; 30: 365-72.
  • 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 rat isolated heart. Br J Pharmacol 1998; 123: 1085-8.
  • Joyeux M, Godin-Ribuot D, Patel A, Demenge P, Yellon DM, Ribuot C. Infarct size-reducing effect of heat stress and alphal adrenoceptois in rats. Br J Pharmacol 1998; 125: 645-50.
  • Joyeux M, Lagneux C, Bricca G, Yellon DM, Demenge P, Ribuot C. Heat stress-induced resistance to myocardial infarction in the isolated heart from transgenic [(mREN-2)27] hypertensive rats. Cardiovasc Res 1998; 40: 124-30.
  • Qian Y-Z, Shipley JB, Levasseur JE, Kukreja RC. Dissociation of heat shock proteins expression with ischemic tolerance by whole body hyperthermia in rat heart J MoI Cell Cardiol 1998; 30: 1163-72.
  • Yamashita N, Hoshida S, Taniguchi N, Kuzuya T, Hori M. Whole-body hyperthermia provides biphasic cardioprotection against ischemia/reperfusion injury in the rat. Circulation 1998; 98: 1414-21.
  • Xi L, Chelliah J, Nayeem MA, Levasseur JE, Hess ML, Kukreja RC. Whole body heat stress fails to protect mouse heart against ischemia/reperfusion injury: Role of 72 kDa heat shock protein and antioxidant enzymes. J MoI Cell Cardiol 1998; 30: 2213-27.
  • Song Q-J, Li Y-J, Deng H-W. Early and delayed cardioprotection by heat stress is mediated by calcitonin gene-related peptide. Naunyn-Schmiedeberg's Arch Pharmacol 1999; 359: 477-83.
  • Joyeux M, Faure P, Godin-Ribuot D, Halimi S, Patel A, Yellon DM, Demenge P, Ribuot C. Heat stress fails to protect myocardium of streptozotocin-induced diabetic rats against infarction. Cardiovasc Res 1999; 43: 939-46.
  • Patel HH, Hsu A, Gross GJ. Cardioprotection is strain dependent in rat in response to whole body hyperthermia Am J Physiol 2001; 280: H1208-14.
  • Tekin D, Xi L, Zhao T, Tejero-Taldo MI, Atluri S, Kukreja RC. Mitogen-activated protein kinases mediate heat shock-induced delayed protection in mouse heart Am J Physiol 2001; 281: H523-32.
  • Gray CC, Amrani M, Smolensk! RT, Taylor GL, Yacoub MH. Age dependence of heat stress mediated cardioprotection. Ann Thorac Surg 2000; 70: 621-6.
  • Hall DM, Buettner G-R, Matthes RD, Gisolfi CV. Hyperthermia stimulates nitric oxide formation: electron paramagnetic resonance detection of ·NO-heme in blood. J Appl Physiol 1994; 77: 548-53.
  • Malyshev IY, Manukhina EB, Mikoyan VD, Kubrina LN, Vanin AF. Nitric oxide is involved in heat-induced HSP70 accumulation. FEBS Lett 1995; 370: 159-62.
  • Wong HR, Finder JD, Wasserloos K, Pitt BR. Expression of iNOS in cultured rat pulmonary artery smooth muscle cells is inhibited by the heat shock response. Am J Physio! 1995; 269: L843-8.
  • Feinstein DL, Galea E, Aquino DA, Li GC, Xu H, Reis DJ. Heat shock protein 70 suppresses astroglial-inducible nitric oxide synthase expression by decreasing NF-?B activation. J Biol Chem 1996; 271: 17724-32.
  • Wong HR, Ryan M, Wispe JR. The heat shock response inhibits inducible nitric oxide synthase gene expression by blocking I?-B degradation and NF-?B nuclear translocation. Biochem Biophys Res Comm 1997; 231: 257-63.
  • Zhao L, Weber PA, Smith JR, Comerford ML, Elliott GT. Role of inducible nitric oxide synthase in pharmacological 'preconditioning* with monophosphorjl lipid A. J MoI Cell Cardiol 1997; 29: 1567-76.
  • Xi L, Jarrett NC, Hess ML, Kukreja RC. Essential role of inducible nitric oxide synthase in monophosphoryl lipid A-induced late cardioprotection: evidence from pharmacological inhibition and gene knockout mice. Circulation 1999; 99: 2157-63.
  • Xi L, Salloum F, Tekin D, Jarrett NC, Kukreja RC. Glycolipids RC-552 induces delayed preconditioning-like effect via iNOS-dependent pathway in mice. Am J Physiol 1999; 277: H2418-24.
  • Zhao T, Xi L, Chelliah J, Levasseur JE, Kukreja RC. Inducible nitric oxide synthase mediates delayed myocardial protection induced by activation of adenosine AI receptors: evidence from gene knockout mice. Circulation 2000; 102: 902-7.
  • Takano H, Manchikalapudi S, Tang XL, Qiu Y, Rizvi A, Jadoon AK, Zhang Q, Bolli R. Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits. Circulation 1998; 98: 441-9.
  • Imagawa J, Yellon DM, Baxter GF. Pharmacological evidence that inducible nitric oxide synthase is a mediator of delayed preconditioning Br J Pharmacol 1999; 126: 701-8.
  • Yellon DM, Latchman DS. Stress proteins and myocardial protection. J MoI Cell Cardiol 1992; 24: 113-24.
  • Yellon DM, Latchman DS, Marber MS. Stress proteins--an endogenous route to myocardial protection: fact or fiction? Cardiovasc Res 1993; 27: 158-61.
  • Black SC, Lucchesi BR. Heat shock proteins and the ischemic heart: an endogenous protective mechanism. Circulation 1993; 87: 1048-51.
  • Benjamin IJ, McMillan DR. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 1998; 83: 117-32.
  • Ohtsuka K, Hata M. Molecular chaperone function of mammalian Hsp70 and Hsp40--a review. Int J Hyperthermia 2000; 16: 231-45.
  • Leger JP, Smith FM, Currie RW. Confocal microscopic localization of constitutive and heat shock-induced proteins HSP70 and HSP27 in the rat heart Circulation 2000; 102: 1703-9.
  • Amrani M, Latif N, Morrison K, Gray CC, Jayakumar J, Corbett J, Goodwin AT, Dunn MJ, Yacoub MH. Relative induction of heat shock protein in coronary endothelial cells and cardiomyocytes: implications for myocardial protection. J Cardiovasc Surg 1998; 115: 200-9.
  • Marber MS, Walker JM, Latchman DS, Yellon DM. Myocardial protection after whole body heat stress in the rabbit is dependent on metabolic substrate and is related to the amount of the inducible 70-kD heat stress protein. J Clin Invest 1994; 93: 1087-94.
  • Kukreja RC, Qian Y-Z, Okubo S, Flaherty EE. Role of protein kinase C and 72kDa heat shock protein in ischemic tolerance following heat stress in the rat heart MoI Cell Biochem 1999; 195: 123-31.
  • Clerk A, Fuller SJ, Michael A, Sugden PH. Stimulation of 'stress-regulated' mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J Biol Chem 1998; 273: 7228-34.
  • Hu Y, Metzler B, Xu Q. Discordant activation of stress-activated protein kinase or c-jun-NH2-terminal protein kinases in tissues of heat stressed mice. J Biol Chem 1997; 272: 9113-9.
  • Maroni P, Bendinelli P, Zuccorononno C, Schiaffonati L, Piccoletti R. Cellular signaling after in vivo heat shock in the liver. Cell Biol Int 2000; 24: 145-52.
  • Joyeux M, Boumendjel A, Carroll R, Ribuot C, Godin-Ribuot D, Yellon DM. SB203580, a mitogen-activated protein kinase inhibitor, abolishes resistance to myocardial infarction induced by heat stress. Cardiovasc Drugs Ther 2000; 14: 337-43.
  • Yao Z, Gross GJ. Effects of the KATP channel opener bimakalim on coronary blood flow, monophasic action potential duration, and infarct size in dogs. Circulation 1994; 89:1769-75.
  • Lagneux C, Ribuot C. In vivo evidence for B1-receptor synthesis induction by heat stress in heart. Br J Pharmacol 1997; 121: 1045-6.
  • Lyashko V, Vikulova VK, Chernicov VG, Ivanov VI, Ulmasov KA, Zatsepina OG, Evgen'Ev MB. Comparison of the heat shock response in ethnically and ecologically different human populations. Proc Natl Acad Sci USA 1994; 91: 12492-5.
  • Liedtke AJ, Hughes HC. Effects of hyperthermic stress on myocardial function during experimental coronary ischemia. Circ Res 1976; 39: 647-53.
  • Chien GL, Wolff RA, Davis RF, van Winkle DM. 'Normothermic range' temperature affects myocardial infarct size. Cardiovasc Res 1994; 28: 1014-7.
  • Schwarte LM, Verbinski SG, Vander Heide RS, Reimer KA. Epicardial temperature is a major predictor of myocardial infarct size in dogs. J MoI Cell Cordial 1997; 29: 1577-83.
  • Makino M, Lodato RF, Stephens LC, Strebel FR, Jenkins GN, Ohno S, Sakaguchi Y, Kostergaard J, Tomasovic SP, Bull JM. Protective effect of NG-monomethyl-L-arginine against hypotension induced by combined tumor necrosis factor-alpha and whole body hyperthermia in rats. Int J Hyperthermia 1996; 12: 617-34.
  • Mansoor S, Spano M, Baschieri S, Cividalli A, Mosiello L, Doria G. Effect of in vivo hyperthermia on thymocyte maturation and selectioa Int Immunol 1992; 4: 227-32.
  • Roberts Jr NJ. Differential effects of hyperthermia on human leukocyte production of interferon-alpha and interferon-gamma. Proc Soc Exp Biol Med 1986; 183: 42-7.
  • Moliterno R, Woan M, Bentlejewski C, Qian J, Zeevi A, Pham S, Griffith BP, Duquesnoy RJ. Heat shock protein-induced T-lymphocyte propagation from endomyocardial biopsies in heart transplantation J Heart Lung Transpl 1995; 14: 329-37.
  • Page RL, Meyer RE, Thrall DE, Dewhirst MW. Cardiovascular and metabolic response of tumor-bearing dogs to whole body hyperthermia Int J Hyperthermia 1987; 3: 513-25.
  • Sakaguchi Y, Stephens LC, Makino M, Kaneko T, Strebel FR, Danhauser LL, Jenkins GN, Bull JM. Apoptosis in tumors and normal tissues induced by whole body hyperthermia in rats. Cancer Res 1995; 55: 5459-64.
  • Kanda T, Nakano M, Yokoyama T, Hoshino Y, Okajima F, Tanaka T, Saito Y, Nagai R, Kobayashi I. Heat stress aggravates viral myocarditis in mice. Life Sd 1999; 64: 93-101.
  • Thomas JA, Noble EG. Heat shock does not attenuate low-frequency fatigue. Can J Physiol Pharmacol 1999; 71: 64-70.
  • Dewhirst MW. Thermal dosimetry. In: Seegenschmiedt MH, Fessenden P, Vernon CC, eds. Principles and Practice of Thermoradiotherapy and Thermochemotherapy. Berlin: Springer-Verlag, 1995, Vol. 1, 123-36.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.