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Effect of Acute Heat Stress on Heat Shock Protein 70 and Its Corresponding mRNA Expression in the Heart, Liver, and Kidney of Broilers

  • Yu, Jimian (The Key Laboratory of Animal Pathology, College of Veterinary Medicine Nanjing Agricultural University) ;
  • Bao, Endong (The Key Laboratory of Animal Pathology, College of Veterinary Medicine Nanjing Agricultural University)
  • Received : 2007.11.29
  • Accepted : 2008.03.31
  • Published : 2008.08.01

Abstract

The objective of this study was to investigate the expression and localization of heat shock protein 70 (Hsp70) and its mRNA in the heart, liver, and kidney of acutely heat-stressed broilers at various stressing times. Male AA broilers (n = 100) were randomly divided into 5 groups of 20 birds per group. After 30 d of adaptive feeding at ambient temperature, 80 experimental broilers were suddenly heat stressed by increasing the environmental temperature from $22{\pm}1^{\circ}C$ to $37{\pm}1^{\circ}C$. The 4 groups were heat stressed for 2, 3, 5, and 10 h, respectively. The localizations of Hsp70 protein and mRNA, determined by immunohistochemical staining and in situ hybridization, respectively, were demonstrated to be tissue dependent, implying that different tissues have differential sensibilities to heat stress. Intense Hsp70 staining was identified in the vascular endothelial cell of heart, liver and kidney, suggesting an association between expression of Hsp70 in vascular endothelial cell and functional recovery of blood vessels after heat shock treatment. Ante-mortem heat stress had a significant effect on the expression of Hsp70 protein and mRNA. The quantitation of Hsp70 protein and mRNA were both time and tissue dependent. During the exposure to heat stress, the heart, liver and kidney of broiler chickens exhibited increased amounts of Hsp70 protein and mRNA. The expression of hsp70 mRNA in the heart, liver and kidney of heat-stressed broilers increased significantly and attained the highest level after a 2-h exposure to elevated temperatures. However, significant elevations in Hsp70 protein occurred after 2, 5, and 3 h of heat stressing, respectively, indicating that the stress-induced responses vary among different tissues.

Keywords

References

  1. Amrani, M., N. Latif, K. Morrison, C. C. Gray, J. Gray, J. Jayakumar, A. Corbett, M. Goodwin, Dunn and M. Yacoub. 1998. Relative induction of heat shock protein in coronary endothelial cells and cardiomyocytes: implications for myocardial protection. J. Thorac. Cardiovasc. Surg. 115:200-209. https://doi.org/10.1016/S0022-5223(98)70458-1
  2. Arrigo, A. P. 2000. HSPs as novel regulators of programmed cell death and tumorigenicity. Path. Bio. 48:280-288.
  3. Baqchi, M., M. Ireland, M. Katar and H. Maisel. 2001. Heat shock proteins of chicken lens. J. Cell. Biochem. 82(3):409-414. https://doi.org/10.1002/jcb.1168
  4. Belay, T. and R. G. Teeter. 1996. Effects of ambient temperature on broiler mineral balance partitioned into urinary and faecal loss. Br. Poult. Sci. 37:423-433. https://doi.org/10.1080/00071669608417873
  5. Bryantsev, A. L., S. A. Loktionova, O. P. Ilyinskaya, E. M. Tararak, H. H. Kampinga and A. E. Kabakov. 2002. Distribution, phosphorylation, and activities of Hsp25 in heat-stressed H9c2 myoblasts: a functional link to cytoprotection. Cell Stress Chaperones 7:146-155. https://doi.org/10.1379/1466-1268(2002)007<0146:DPAAOH>2.0.CO;2
  6. Bukau, B., E. Deuerling, C. Pfund and E. A. Craig. 2000. Getting Newly Synthesized Proteins into Shape. Cell 101(2):119-122. https://doi.org/10.1016/S0092-8674(00)80806-5
  7. Chee, K. M., M. K. Chung, J. H. Choi and Y. K. Chung. 2005. Effects of dietary vitamin C and E on egg shell quality of broiler breeder hens exposed to heat stress. Asian-Aust. J. Anim. Sci. 18:545-551. https://doi.org/10.5713/ajas.2005.545
  8. Craig, E. A. 1985. The heat shock response. CRC. Crit. Rev. Biochem. 16:135-140.
  9. Craig, E. A. and C. A. Gross. 1991. Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16:35-40.
  10. Dechesne, C. J., H. N. Kim, T. S. Nowak and R. J. Wenthold. 1992. Expression of heat shock protein, HSP72, in the guinea pig and rat cochlea after hyperthermia; immunochemical and in situ hybridization analysis. Hear Res. 59:195-204. https://doi.org/10.1016/0378-5955(92)90116-5
  11. Edens, F. W., C. H. Hill and S. Wang. 1992. Heat shock protein response in phosphorus-deficient heat-stressed broiler chickens. Comp. Biochem. Physiol. B 103:827-831. https://doi.org/10.1016/0305-0491(92)90200-B
  12. Gabriel, J. E., J. A. Ferro, R. M. P. Stefani, M. I. T. Ferro, S. L. Gomes and M. Macari. 1996. Effect of acute heat stress on heat shock protein 70 messenger RNA and on heat shock protein expression in the liver of broilers. Br. Poult. Sci. 37:443-449. https://doi.org/10.1080/00071669608417875
  13. Geraert, P. A., S. Guillaumin and B. Leclercq. 1993. Are genetically lean broilers more resistant to hot climate? Br. Poult. Sci. 34(4):643-653. https://doi.org/10.1080/00071669308417623
  14. Geraert, P. A., J. C. Padilha and S. Guillaumin. 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. https://doi.org/10.1079/BJN19960124
  15. Glover, J. R. and S. Lindquist. 1998. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94(1):73-82. https://doi.org/10.1016/S0092-8674(00)81223-4
  16. Guerrierojr, V. and D. A. Raynes. 1990. Synthesis of heat stress protein in lymphocytes from livestock. J. Anim. Sci. 68:2779-2783. https://doi.org/10.2527/1990.6892779x
  17. Gutierrez, J. A. and V. Guerrierojr. 1991. Quantitation of Hsp70 in tissues using a competitive enzyme-linked immunosorbent assay. J. Immunol. Meth. 143:81-88. https://doi.org/10.1016/0022-1759(91)90275-K
  18. Hartl, F. U. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-580. https://doi.org/10.1038/381571a0
  19. Hartl, F. U. and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Sci. 295(5561):1852-1858. https://doi.org/10.1126/science.1068408
  20. Heydari, A. R., B. Wu, R. Takahashi, R. Strong and A. Richardson. 1993. Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol. Cell. Biol. 13:2909-2918. https://doi.org/10.1128/MCB.13.5.2909
  21. Hickey, E., S. E. Brandon, R. Potter, G. Stein, J. Stein and L. A. Weber. 1986. Sequence and organization of genes encoding the human 27 kDa heat shock protein. Nucleic Acids Res. 14:4127-4145. https://doi.org/10.1093/nar/14.10.4127
  22. Hightower, L. E. 1991. Heat shock, stress proteins, chaperones and proteotoxicity. Cell 66:191-197. https://doi.org/10.1016/0092-8674(91)90611-2
  23. Ipek, A., O. Canbolat and A. Karabulut. 2007. The effect of vitamin E and vitamin C on the performance of Japanese Quails (Coturnix Coturnix Japonica) reared under heat stress during growth and egg production period. Asian-Aust. J. Anim. Sci. 20:252-256.
  24. Jakubowicz-Gil, J., B. Pawlikowska-Pawlega, T. Piersiak, J. Pawelec and A. Gawron. 2005. Quercetin suppresses heat shock-induced nuclear translocation of Hsp72. Folia Histochemi. Cytobiol. 43:123-128.
  25. King, Y. T., C. S. Lin, J. H. Lin and W. C. Lee. 2002. Whole-body hyperthermia-induced thermotolerance is associated with the induction of Heat Shock Protein 70 in mice. J. Exp. Biol. 205:273-278.
  26. Knowlton, A. A. 1994. Heat-shock proteins, stress and the heart. Ann. NY. Acad. Sci. 723:128-137. https://doi.org/10.1111/j.1749-6632.1994.tb36722.x
  27. Knowlton, A. A. 1995. The role of heat shock proteins in the heart. J. Mol. Cell. Cardiol. 27:121-131. https://doi.org/10.1016/S0022-2828(08)80012-0
  28. Lavoie, J. N., H. Lambert, E. Hickey, L. A. Weber and J. Landry. 1995. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol. Cell. Biol. 15:505-516. https://doi.org/10.1128/MCB.15.1.505
  29. Lepore, D. A., J. V. Hurley, A. G. Stewart, W. A. Morrison and R. L. Anderson. 2000. Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle Nerve 23: 1847-1855. https://doi.org/10.1002/1097-4598(200012)23:12<1847::AID-MUS8>3.0.CO;2-U
  30. Levy, E., Y. Hasin, G. Navon and M. Horowitz. 1997. Chronic heat improves mechanical and metabolic response of trained rat heart on ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 272:H2085-H2094. https://doi.org/10.1152/ajpheart.1997.272.5.H2085
  31. Lin, W. Q., R. A. Vandyke, H. M. Marsh and J. R. Trudell. 1994. Nuclear translocation of heat shock protein 72 in liver cells of halothane-exposed rats. Biochem. Biophys. Res. Commun. 199:647-652. https://doi.org/10.1006/bbrc.1994.1277
  32. Mahmoud, K. Z., M. M. Beck, S. E. Scheideler, K. P. Anderson and S. D. Kachman. 1996. Acute high environmental temperature and calcium-estrogen relationships in hen. Poult. Sci. 75:1555-1562. https://doi.org/10.3382/ps.0751555
  33. Mahmoud, K. Z., F. W. Edens, E. J. Eisen and G. B. Havenstein. 2004. The effect of dietary phosphorus on heat shock protein mRNAs during acute heat stress in male broiler chickens (Gallus gallus). Comp. Biochem. Physiol. C 137:11-18. https://doi.org/10.1016/S1095-6433(03)00178-8
  34. Maloyan, A., A. Palmon and M. Horwitz. 1999. Heat acclimation increase the basal HSP72 level and alters its production dynamics during heat stress. Am. J. Physiol. Regul. Integr. Comp. Physiol. 276:R1505-R1515.
  35. Marder, J. and Z. Arad. 1983. Acid-base regulation during thermal panting in the fowl (Gallus domesticus): Comparison between breeds. Comp. Biochem. Physiol. A 74:125-130. https://doi.org/10.1016/0300-9629(83)90722-3
  36. Marder, J. and Z. Arad. 1989. Panting and acid-base regulation in heat stressed birds. Comp. Biochem. Physiol. A 94:395-400. https://doi.org/10.1016/0300-9629(89)90112-6
  37. Mariethoz, E., M. R. Jacquier-Sarlin, G. Multhoff, A. M. Healy, F. Tacchini-Cottier and B. S. Polla. 1997. Heat shock and proinflammatory stressors induce differential localization of heat shock proteins in human monocytes. Inflammation 21(6):629-642. https://doi.org/10.1023/A:1027338323296
  38. Martin, F., J. M. Requena, J. Martin, C. Alonso and M. C. Lopez. 1993. Cytoplasmic-Nuclear translocation of the HSP70 protein during environmental stress in Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 196:1155-1162. https://doi.org/10.1006/bbrc.1993.2372
  39. Mashaly, M. M., G. L. Hendricks, M. A. Kalama, A. E. Gehad, A. O. Abbas and P. H. Patterson. 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult. Sci. 83(6):889-894. https://doi.org/10.1093/ps/83.6.889
  40. Mayer, M. P. and B. Bukau. 2004. Hsp70 chaperones: Cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62:670-684. https://doi.org/10.1007/s00018-004-4464-6
  41. McCormick, P. H., G. Chen, S. Tierney, C. J. Kelly and D. J. Bouchier-Hayes. 2003a. Clinically applicable thermal preconditioning attenuates leukocyte-endothelial interactions. J. Am. Coll. Surg. 197:71-78. https://doi.org/10.1016/S1072-7515(03)00392-2
  42. McCormick, P. H., G. Chen, S. Tlerney, C. J. Kelly and D. J. Bouchier-Hayes. 2003b. Clinically relevant thermal preconditioning attenuates ischemia-reperfusion injury. J. Surg. Res. 109:24-30. https://doi.org/10.1016/S0022-4804(02)00035-5
  43. McCully, J. D., T. Myrmel, M. Lotz, I. B. Krukenkamp and S. Levitsky. 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. https://doi.org/10.1016/0022-2828(95)90037-3
  44. Michael, L., Goodson and K. D. Sarge. 1995. Regulated expression of heat shock factor 1 isoforms with distinct leucine zipper arrays via tissue-dependent alternative splicing. Biochem. Biophys. Res. Commun. 211:943-949. https://doi.org/10.1006/bbrc.1995.1903
  45. Miron, T., K. Vancompernolle, J. Vandekerckhove, M. Wilchek and B. Geiger. 1991. A 25-kD inhibitor of actin polymerization: Is a low molecular mass heat shock protein. J. Cell. Biol. 114:255-261. https://doi.org/10.1083/jcb.114.2.255
  46. Morimoto, R. I. 1993. Cells in stress: transcriptional activation of heat shock genes. Sci. 259:1409-1410. https://doi.org/10.1126/science.8451637
  47. Morimoto, R. I. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788-3796. https://doi.org/10.1101/gad.12.24.3788
  48. Northcutt, J. K., E. A. Foegeding and F. W. Edens. 1994. Waterholding properties of thermally preconditioned chicken breast and leg meat. Poult. Sci. 73:308-316. https://doi.org/10.3382/ps.0730308
  49. Ogura, Y., Y. Naito, T. Tsurukawa, N. Ichinoseki-Sekine, N. Saga, T. Sugiura and S. Katamoto. 2007. Microwave hyperthermia treatment increases heat shock proteins in human skeletal muscle. Br. J. Sports Med. 41:453-455. https://doi.org/10.1136/bjsm.2006.032938
  50. Park, H., I. Y. Ahn and H. E. Lee. 2007. Expression of heat shock protein 70 in the thermally stressed antarctic clam Laternula elliptica. Cell Stress Chaperones 12(3):275-282. https://doi.org/10.1379/CSC-271.1
  51. Pivovarova, A. V., V. V. Mikhailova, I. S. Chernik, N. A. Chebotareva, D. I. Levitsky and N. B. Gusev. 2005. Effects of small heat shock proteins on the thermal denaturation and aggregation of F-actin. Biochem. Biophys. Res. Commun. 331:1548-1553. https://doi.org/10.1016/j.bbrc.2005.04.077
  52. Pratt, W. B. 1993. The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268:21455-21458.
  53. Ryan, M. T. and N. Pfanner. 2001. Hsp70 proteins in protein translocation. Adv. Protein Chem. 59:223-242. https://doi.org/10.1016/S0065-3233(01)59007-5
  54. Sandercock, D. A., R. R. Hunter, G. R. Nute, M. A. Mitchell and P. M. Hocking. 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. https://doi.org/10.1093/ps/80.4.418
  55. Shabtay, A. and Z. Arad. 2005. Ectothermy and endothermy: evolutionary perspectives of thermoprotection by HSPs. J. Exp. Biol. 208:2773-2781. https://doi.org/10.1242/jeb.01705
  56. Shabtay, A. and Z. Arad. 2006. Reciprocal activation of HSF1 and HSF3 in brain and blood tissues: is redundancy developmentally related? Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R566-R572. https://doi.org/10.1152/ajpregu.00685.2005
  57. Shaila, S., S. Angshuman, K. Abhijeet, M. Samindranath, Pal and K. Jayanta. 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. https://doi.org/10.1016/j.pestbp.2005.10.006
  58. Shim, K. S., K. T. Hwang, M. W. Son and G. H. Park. 2006. Lipid metabolism and peroxidation in broiler chickens under chronic heat stress. Asian-Aust. J. Anim. Sci. 19:1206-1211. https://doi.org/10.5713/ajas.2006.1206
  59. Sun, P. M., Y. T. Liu, Y. G. Zhao, E. D. Bao and Z. L. Wang. 2007. Relationship between heat damages and HSPs mRNA in persistent heat stressed broilers. Agric. Sci. China 6:227-233. https://doi.org/10.1016/S1671-2927(07)60039-X
  60. Tankson, J. D., Y. Vizzier-Thaxton, J. P. Thaxton, J. D. May and J. A. Cameron. 2001. Stress and nutritional quality of broilers. Poult. Sci. 80:1384-1389. https://doi.org/10.1093/ps/80.9.1384
  61. Tao, X., Z. Y. Zhang, H. Dong, H. Zhang and H. Xin. 2006. Responses of thyroid hormones of market-size broilers to thermoneutral constant and warm cyclic temperatures. Poult. Sci. 85:1520-1528.
  62. van der Hel, W., M. W. Versteqen, L. Pijls and M. van Kampen. 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. https://doi.org/10.3382/ps.0712014
  63. Van Laack, R. L. J. M., C. Faustman and J. G. Sebranek. 1993. Pork quality and the expression of stress protein Hsp70 in swine. J. Anim. Sci. 71:2958-2964. https://doi.org/10.2527/1993.71112958x
  64. Velazquez, J. M. and S. Lindquist. 1984. hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36:655-662. https://doi.org/10.1016/0092-8674(84)90345-3
  65. Wang, J. H., H. P. Redmond, R. W. Watson, C. Condron and D. Bouchier-Hayes. 1995. Induction of heat shock protein 72 prevents neutrophil-mediated human endothelial cell necrosis. Arch. Surg. 130(12):1260-1265. https://doi.org/10.1001/archsurg.1995.01430120014002
  66. Wang, S. and F. W. Edens. 1993. Stress-induced heat-shock protein synthesis in peripheral leukocytes of turkeys, Meleagris Gallopavo. Comp. Biochem. Physiol. 106B:621-628.
  67. Wang, S. and F. W. Edens. 1998. Heat conditioning induces heat shock proteins in broiler chickens and turkey poults. Poult. Sci. 77:1636-1645. https://doi.org/10.1093/ps/77.11.1636
  68. Wang, S. C., J. Chen, Y. Huang, X. F. Li and D. J. Zhang. 2007. Effect of heat stress on production performance and blood biochemical indices in broiler. China Poult. 15:11-13.
  69. Wang, T. T., A. S. Chiang, J. J. Chu, T. J. Cheng, T. M. Chen and Y. K. Lai. 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. https://doi.org/10.1016/S1357-2725(97)00133-7
  70. White, F. P. 1980. The synthesis and possible transport of specific proteins by cells associated with brain capillaries. J. Neurochem. 35(1):88-94. https://doi.org/10.1111/j.1471-4159.1980.tb12492.x
  71. Wu, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell. Biol. 11:441-469. https://doi.org/10.1146/annurev.cb.11.110195.002301
  72. Yahav, S., A. Shamay, G. Horev, D. Bar-ilan, O. Genina and M. Friedman-einat. 1997. Effect of acquisition of improved thermotolerance on the induction of heat shock proteins in broiler chickens. Poult. Sci. 76:1428-1434. https://doi.org/10.1093/ps/76.10.1428
  73. Zhang, S. L., M. Guo, X. S. Zhang, W. X. Zhang, X. Y. Li and C. S. Xu. 2000. Study on the expression of HSP70 induced by heat shock in mouse hepatocytes. Chinese J. Anat. 123:4.
  74. Zietkiewicz, S., J. Krzewska and K. Liberek. 2004. Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem. 279:44376-44383. https://doi.org/10.1074/jbc.M402405200
  75. Zulkifli, I., Nwe New Htin, A. R. Alimon, T. C. Loh and M. Hair-Bejo. 2007. Dietary selection of fat by heat-stressed broiler chickens. Asian-Aust. J. Anim. Sci. 20:245-251.
  76. Zulkifli, I., S. A. Mysahra and L. Z. Jin. 2004. Dietary supplementation of Betaine (Betafin) and response to high temperature stress in male broiler chickens. Asian-Aust. J. Anim. Sci. 17:244-249. https://doi.org/10.5713/ajas.2004.244

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