Abstract
The objective of this study was to investigate the kinetics of Hsp60, Hsp70, Hsp90 protein, and messenger RNA (mRNA) expression levels and to correlate these heat shock protein (Hsp) levels with tissue damage resulting from exposure to high temperatures for varying amounts of time. One hundred broilers were heat-stressed for 0, 2, 3, 5, and 10 h, respectively, by rapidly increasing the ambient temperature from 22 ± 1°C to 37 ± 1°C. Obvious elevations of plasma creatine kinase indicate damage to myocardial cells after heat stress. Hsp70 and Hsp90, and their corresponding mRNAs in the heart tissue of heat-stressed broilers, elevated significantly after 2 h of heat exposure and decreased quickly with continued heat stress. However, the levels of hsp60 mRNA in the heart of heat-stressed broilers increased sharply (P < 0.01) at 2 h of heat stress but then decreased quickly after 3 h, while the level of Hsp60 protein in the heart increased (P < 0.01) at 2 h of heat stress and maintained a high level throughout heat exposure. The results indicate that the elevation of the three Hsps, especially Hsp60 in heart, may be important markers at the beginning of heat stress and act as protective proteins in adverse environments. The reduction of Hsp signals in the cytoplasm of myocardial cells implies that myocardial cell lesions may have an adverse impact on the function of Hsps during heat stress. Meanwhile, the localization of Hsp70 in blood vessels of broiler hearts suggests another possible mechanism for protection of the heart after heat exposure.
Similar content being viewed by others
References
Benjamin IJ, McMillan DR (1998) Stress heat shock proteins molecular chaperones in cardiovascular biology and disease. Circ Res 83:117–132
Bukau B, Deuerling E, Pfund C, Craig EA (2000) Getting newly synthesized proteins into shape. Cell 101(2):119–122
Cechetto JD, Soltys BJ, Gupta RS (2000) Localization of mitochondrial 60-kD heat shock chaperonin protein (Hsp60) in pituitary growth hormone secretory granules and pancreatic zymogen granules. J Histochem Cytochem 48:45–56
Craig EA (1985) The heat shock response. CRC Crit Rev Biochem 18:239–280
Craig EA, Weissman JS, Horwich AL (1994) Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78:365–372
Eichler TE, Ransom RF, Smoyer WE (2005) Differential induction of podocyte heat shock proteins by prolonged single and combination toxic metal exposure. Toxicol Sci 84(1):120–128
Fostinis Y, Theodoropoulos PA, Gravanis A, Stournaras C (1992) Heat shock protein HSP90 and its association with the cytoskeleton: a morphological study. Biochem Cell Biol 70:779–786
Ganter MT, Ware LB, Howard M, Roux J, Gartland B, Matthay MA, Fleshner M, Pittet J (2006) Extracellular heat shock protein 72 is a marker of the stress protein response in acute lung injury. Am J Physiol Lung Cell Mol Physiol 291:L354–L361
Georgopoulos C, Welch WJ (1993) Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 9:601–634
Geraert PA, Guillaumin S, Leclercq B (1993) Are genetically lean broilers more resistant to hot climate? Br Poult Sci 34(4):643–653
Geraert PA, Padilha JC, Guillaumin S (1996) Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. Br J Nutr 75(2):195–204
Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94(1):73–82
Gray CC, Amrani M, Yacoub MH (1999) Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int J Biochem Cell Biol 31:559–573
Hagiwara S, Iwasaka H, Matsumoto S, Noguchi T, Yoshioka H (2007) Association between heat stress protein 70 induction and decreased pulmonary fibrosis in an animal model of acute lung injury. Lung 185(5):287–293
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Sci 295(5561):1852–1858
Haslbeck M, Miess A, Stromer T, Walter S, Buchner J (2005) Disassembling protein aggregates in the yeast cytosol: the cooperation of Hsp26 with SSA1 and Hsp104. J Biol Chem 25:23861–23868
Hendrick JP, Hartl FU (1995) The role of molecular chaperones in protein folding. FASEB J 9:1559–1569
Hightower LE (1991) Heat shock, stress proteins, chaperones and proteotoxicity. Cell 66:191–197
House SD, Guidon PT Jr, Perdrizet GA, Rewinski M, Kyriakos R, Bockman RS, Mistry T, Gallagher PA, Hightower LE (2001) Effects of heat shock, stannous chloride, and gallium nitrate on the rat inflammatory response. Cell Stress Chaperones 6:164–171
Hutter JJ, Mestril R, Tam EKW, Sievers RE, Dillmann WH, Wolfe CL (1996) Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 94:1408–1411
Jayakumar J, Suzuki K, Sammut IA, Smolenski RT, Khan M, Latif N, Abunasra H, Murtuza B, Amrani M, Yacoub MH (2001) Heat shock protein 70 gene transfection protects mitochondrial and ventricular function against ischemia-reperfusion injury. Circulation 104:I303–307
Kabakov AE, Gabai VL (1997) Heat shock proteins and cytoprotection: ATP-deprived mammalian cells. R.G. Landes Co., Austin
Kawana K, Miyamoto Y, Tanonaka K, Han-no Y, Yoshida H, Takahashi M, Takeo S (2000) Cytoprotective mechanism of heat shock protein 70 against hypoxia/reoxygenation injury. J Mol Cell Cardiol 32:2229–2237
Kellermayer MS, Csermely P (1995) ATP induces dissociation of the 90 kDa heat shock protein (hsp90) from F-actin: interference with the binding of heavy meromyosin. Biochem Biophys Res Commun 211:166–174
Kervinen H, Huittinen T, Vaarala O, Leinonen M, Saikku P, Manninen V, Mänttäri M (2003) Antibodies to human heat shock protein 60, hypertension and dyslipidemia. A study of joint effects on coronary risk. Atherosclerosis 169:339–344
Knowlton AA (1994) Heat-shock proteins, stress and the heart. Ann NY Acad Sci 723:128–137
Koelkebeck KW, Odom TW (1995) Laying hen response to acute heat stress and carbon dioxide supplementation: II changes in plasma enzymes, metabolites and electrolytes. Comp Biochem Physiol Part A: Physiol 122:119–122
Kreisel W, Hildebrandt H, Schiltz E, Kohler G, Spamer C, Dietz C, Mossner W, Heilmann C (1994) Immuno-gold electron microscopical detection of heat shock protein 60 (hsp60) in mitochondria of rat hepatocytes and myocardiocytes. Acta Histochem 96:51–62
Latif N, Taylor PM, Khan MA, Yacoub MH, Dunn MJ (1999) The expression of heat shock protein 60 in patients with dilated cardiomyopathy. Basic Res Cardiol l94:112–119
Lau S, Patnaik N, Sayen R, Mestril R (1997) Simultaneous overexpression of two stress proteins in rat cardiomyocytes and myogenic cells confers protection against ischemia-induced injury. Circulation 96:2287–2294
Liang P, MacRae TH (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110:1431–1440
Lindquist S (1986) The heat-shock responses. Annu Rev Biochem 55:1151–1191
Liu JC, He M, Wan L, Cheng XS (2007) Heat shock protein 70 gene transfection protects rat myocardium cell against anoxia-reoxygeneration injury. Chin Med J (Engl) 120(7):578–583
Locke M, Noble EG (1995) Stress protein: the exercise response. Can J Appl Physiol 20:155–167
Lu Q, Wen J, Zhang H (2007) Effect of chronic heat exposure on fat deposition and meat quality in two genetic types of chicken. Poult Sci 86(6):1059–1064
Luh SP, Kuo PH, Kuo TF, Tsai TP, Tsao TC, Chen JY, Tsai CH, Yang PC (2007) Effects of thermal preconditioning on the ischemia-reperfusion-induced acute lung injury in minipigs. Shock 28(5):615–622
Marques C, Guo W, Pereira P, Taylor A, Patterson C, Evans PC, Shang F (2006) The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones. FASEB J 20:741–743
Mashaly MM, Hendricks GL, Kalama MA, Gehad AE, Abbas AO, Patterson PH (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci 83(6):889–894
Mayer MP, Bukau B (2004) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
McCormick PH, Chen G, Tlerney S, Kelly CJ, Bouchier-Hayes DJ (2003a) Clinically relevant thermal preconditioning attenuates ischemia-reperfusion injury. J Surg Res 109:24–30
McCormick PH, Chen G, Tierney S, Kelly CJ, Bouchier-Hayes DJ (2003b) Clinically applicable thermal preconditioning attenuates leukocyte–endothelial interactions. J Am Coll Surg 197:71–78
McCully JD, Myrmel T, Lotz M, Krukenkamp IB, Levitsky S (1995) The rapid expression of myocardial hsp70 mRNA and the heat shock 70 kDa protein can be achieved after only a brief period of retrograde hyperthermic perfusion. J Mol Cell Cardiol 27:873–882
Miller L, Qureshi MA (1992) Molecular changes associated with heat shock treatment in avian mononuclear and lymphoid lineage cells. Poult Sci 71:473–481
Morimoto RI, Santoro GM (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16:833–838
Morimoto RI, Tisieres A, Georgopoulos C (1990) The stress response function of the proteins and perspective. In: Morimoto RI, Tisieres A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Springs Harbor, NY, pp 1–36
Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci U S A 94:12949–12956
Northcutt JK, Foegeding EA, Edens FW (1994) Waterholding properties of thermally preconditioned chicken breast and leg meat. Poult Sci 73:308–316
Plumier JCL, Ross BM, Currie RW, Angelidis CE, Kazlaris H, Kollias G (1995) Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 95:1854–1860
Richard J, Derek M, David SL (1995) Differential cytoprotection against heat stress or hypoxia following expression of specific stress protein genes in myogenic cells. J Mol Cell Cardiol 27(8):1669–1678
Ryan MT, Pfanner N (2001) Hsp70 proteins in protein translocation. Adv Protein Chem 59:223–242
Sandercock DA, Hunter RR, Nute GR, Mitchell MA, Hocking PM (2001) Acute heat stress-induced alterations in blood acid–base status and skeletal muscle membrane integrity in broiler chickens at two ages: implications for meat quality. Poult Sci 80:418–425
Shaila S, Angshuman S, Abhijeet K, Samindranath M, Pal JK (2005) Flufenoxuron, an acylurea insect growth regulator, alters development of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) by modulating levels of chitin, soluble protein content, and HSP70 and p34cdc2 in the larval tissues. Pestic Biochem Physiol 85:84–90
Soltys BJ, Gupta RS (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp Cell Res 222:16–27
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
Sun PM, Liu YT, Zhao YG, Bao ED, Wang ZL (2005) Relationship between heat damages and HSPs mRNA in persistent heat stressed broilers. Agric Sci China 6:227–233
Szalay L, Shimizu T, Schwacha MG, Choudhry MA, Rue LW III, Bland KI, Chaudry IH (2005) Mechanism of the salutary effects of estradiol on organ function following trauma-hemorrhage: upregulation of hemeoxygenase. Am J Physiol 289:H92–H98
Takenaka IM, Hightower LE (1993) Regulation of chicken Hsp70 and Hsp90 family gene expression by transforming growth factor-b1. J Cell Physiol 155:54–62
van der Hel W, Versteqen MW, Pijls L, van Kampen M (1992) Effect of two-day temperature exposure of neonatal broiler chicks on growth performance and body composition during two weeks at normal conditions. Poult Sci 71(12):2014–2021
Wang SY, Edens FW (1993) Stress induced heat shock protein synthesis in peripheral leukocytes of turkeys, Meleagris gallopavo. Comp Biochem Physiol 106B(3):621–628
Wang JH, Redmond HP, Watson RW, Condron C, Bouchier-Hayes D (1995) Induction of heat shock protein 72 prevents neutrophil-mediated human endothelial cell necrosis. Arch Surg 130(12):1260–1265
Wang TT, Chiang AS, Chu JJ, Cheng TJ, Chen TM, Lai YK (1998) Concomitant alterations in distribution of 70 kDa heat shock proteins, cytoskeleton and organelles in heat shocked 9L cells. Int J Biochem Cell Biol 30:745–759
White FP (1980) The synthesis and possible transport of specific proteins by cells associated with brain capillaries. J Neurochem 35(1):88–94
Wiech H, Buchner J, Zimmermann R, Jakob U (1992) Hsp90 chaperones protein folding in vitro. Nature 358:169–170
Zhang XY, Clark AF, Yorio T (2006) Heat shock protein 90 is an essential molecular chaperone for nuclear transport of glucocorticoid receptor b. Invest Ophthalmol Vis Sci 47:700–708
Zhang HY, Lv NH, Xie Y, Guo GH, Zhan JH, Chen J (2007) Protection of heat shock preconditioning on acute gastric mucosal lesion in scalded rats and its mechanism. Zhonghua Shao Shang Za Zhi 23(1):58–61
Zietkiewicz S, Krzewska J, Liberek K (2004) Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J Biol Chem 279:44376–44383
Acknowledgments
This study was supported by grants (30170682, 30571400) from the National Natural Science Foundation of China and grants (20050307008) from the Specialized Research Fund for the Doctoral Program of Higher Education of China.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yu, J., Bao, E., Yan, J. et al. Expression and localization of Hsps in the heart and blood vessel of heat-stressed broilers. Cell Stress and Chaperones 13, 327–335 (2008). https://doi.org/10.1007/s12192-008-0031-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-008-0031-7