Physiological Role of Heat Shock Proteins, Molecular Function and Stress Removal in Fishes

  • Shib Sankar Sen
  • Sib Sankr Giri
Part of the Heat Shock Proteins book series (HESP, volume 12)


Depending on the size, the specific locations and physiological roles of molecular chaperones differ within the cell. However, to tolerate stress HSP drives molecular mechanisms in animals. These proteins interact with multiple systems in diverse ways regulated by the endocrine system. HSP have crucial physiological roles in fish. The important role of HSP is in thermo tolerance as well as tolerance to cytotoxic effects of environmental contaminants and other stressors which are non thermal. HSP enhances immune response through both intra- and extra-cellular activities. Similarly, many studies have proved that most HSP are molecular chaperones which funtion for other cell proteins, and have better cytoprotective effects. To know more about factors, both biotic and abiotic regulating heat shock proteins data has been collected rapidly. However, earlier reports are focused on the role of HSP in development and their importance in fish in nature. Functional genomic approaches will provide the tools necessary to gain a comprehensive understanding of the significance of heat shock proteins in the cellular stress response, in the physiological processes. Heat shock proteins are considerably adaptable and potent molecules, the significance of which to biological procedures is highlighted by the high degree to which their structure and function are phylogenetically preserved. Our knowledge regarding physiological role of heat shock proteins is presently partial; though, a better understanding of their function and thus the skills of the capacity to control their power may lead to their use as therapeutic agents.


Heavy metals HSF HSP Immunoregulation Pathogen Thermal window UV radiation 



Adenosine triphosphate


Gill-associated virus


Heat shock cognates


Heat shock transcription factors


Heat shock proteins


Heat shock response






Temperature-dependent sex determination


Ultra violet


White spot syndrome virus



SSS reviewed and wrote the manuscript. SSS designed and supervised the study. SSG critically read and edited the manuscript. This work was partially funded by Dr. D.S.Kothari post doctoral fellowship to SSS by UGC, GOI (BSR/ME/14-15/0002). SSG acknowledges KRF program of the National Research Foundation of Korea, Ministry of Science and ICT (2016H1D3A1909005).


  1. Ait-Aıssa, S., Ausseil, O., Palluel, O., Vindimian, E., Garnier-Laplace, J., & Porcher, J. (2003). Biomarker responses in juvenile rainbow trout (Oncorhynchus mykiss) after single and combined exposure to low doses of cadmium, zinc, PCB77 and 17-oestradiol. Biomarkers, 8(6), 491–508.Google Scholar
  2. Amiard, J. C., Amiard-Triquet, C., Barka, S., Pellerin, J., & Rainbow, P. S. (2006). Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquatic Toxicology, 76(2), 160–202.PubMedCrossRefGoogle Scholar
  3. Ao, J., Mu, Y., Xiang, L. X., Fan, D., Feng, M., Zhang, S., et al. (2015). Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation. PLoS Genetics, 11, 1–25.CrossRefGoogle Scholar
  4. Baird, N. A., Turnbull, D. W., & Johnson, E. A. (2006). Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. The Journal of Biological Chemistry, 281(50), 38675–38681.PubMedCrossRefGoogle Scholar
  5. Bakthisaran, R., Tangirala, R., & Mohan Rao, C. (2015). Small heat shock proteins: Role in cellular functions and pathology. Biochemica et Biophysica Acta, 1854, 291–319.CrossRefGoogle Scholar
  6. Barnes, J. A., Collins, B. W., Dix, D. J., & Allen, J. W. (2002). Effects of heat shock protein 70 (HSP70) on arsenite-induced genotoxicity. Environmental and Molecular Mutagenesis, 40, 236–242.PubMedCrossRefGoogle Scholar
  7. Basu, N., Todgham, A. E., Ackerman, P. A., Bibeau, M. R., Nakano, K., Schulte, P. M., et al. (2002). Heat shock protein genes and their functional significance in fish. Gene, 295, 173–183.PubMedCrossRefGoogle Scholar
  8. Basu, N., Kennedy, C. J., & Iwama, G. K. (2003). The effects of stress on the association between Hsp70 and the glucocorticoid receptor in rainbow trout. Comparative Biochemistry and Physiology, 134, 655–663.PubMedCrossRefGoogle Scholar
  9. Bears, H., Richards, J. G., & Schulte, P. M. (2006). Arsenic exposure alters hepatic arsenic species composition and stress-mediated gene expression in the common killifish (Fundulus heteroclitus). Aquatic Toxicology, 77, 257–266.PubMedCrossRefGoogle Scholar
  10. Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Morimiti, R. I., Cohen, G. M., & Green, D. R. (2000). Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nature Cell Biology, 2, 469–475.PubMedCrossRefGoogle Scholar
  11. Blanco-Penedo, I., Cruz, J. M., Lopez-Alonse, M., Miranda, M., Castillo, C., Hernandez, J., & Benedito, J. L. (2006). Influence of copper status on the accumulation of toxic and essential metals in cattle. Environment International, 32, 901–906.PubMedCrossRefGoogle Scholar
  12. Boone, A. N., & Vijayan, M. M. (2002). Constitutive heat shock protein 70 (HSC70) expression in rainbow trout hepatocytes: Effect of heat shock and heavy metal exposure. Comparative Biochemistry and Physiology C: Toxicology and Pharmacology, 132(2), 223–233.PubMedGoogle Scholar
  13. Boulangé-Lecomte, C., Forget-Leray, J., & Xuereb, B. (2014). Sexual dimorphism in Grp78 and HSP90A heat shock protein expression in the estuarine copepod Eurytemora affinis. Cell Stress & Chaperones, 19(4), 591–597.CrossRefGoogle Scholar
  14. Brett, J. R. (1971). Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd). American Zoologist, 11, 99–113.CrossRefGoogle Scholar
  15. Bukau, B., & Horwich, A. L. (1998). The HSP70 and HSP60 chaperone machines. Cell, 92(3), 351–366.PubMedCrossRefGoogle Scholar
  16. Bukau, B., Deuerling, E., Pfund, C., & Craig, E. A. (2000). Getting newly synthesized proteins into shape. Cell, 101(2), 119–122.PubMedCrossRefGoogle Scholar
  17. Calabrese, V., Butterfield, D. A., Scapagnini, G., Stella, A. M., & Maines, M. D. (2006). Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: Relevance to brain aging, neurodegenerative disorders, and longevity. Antioxidants & Redox Signaling, 8, 444–477.CrossRefGoogle Scholar
  18. Candido, E. P., & Jones, D. (1996). Transgenic Caenorhabditis elegans strains as biosensors. Trends in Biotechnology, 14(4), 125–129.PubMedCrossRefGoogle Scholar
  19. Carrasco-Malio, A., Díaz, M., Mella, M., Montoya, M. J., Miranda, A., Landaeta, M. F., Sánchez, G., & Hidalgo, M. E. (2014). Are the intertidal fish highly resistant to UV-B radiation? A study based on oxidative stress in Girella laevifrons (Kyphosidae). Ecotoxicology and Environmental Safety, 100, 93–98.PubMedCrossRefGoogle Scholar
  20. Cechetto, J. D., Soltys, B. J., & Gupta, R. S. (2000). Localization of mitochondrial 60-kD heat shock chaperonin protein (HSP60) in pituitary growth hormone secretory granules and pancreatic zymogen granules. The Journal of Histochemistry and Cytochemistry, 48, 45–56.PubMedCrossRefGoogle Scholar
  21. Chale, F. M. M. (2002). Trace metal concentrations in water, sediments and fish tissue from Lake Tanganyika. The Science of the Total Environment, 299, 115–121.PubMedCrossRefGoogle Scholar
  22. Chen, Y. M., Kuo, C. E., Wang, T. Y., Shie, P. S., Wang, W. C., Huang, S. L., et al. (2010). Cloning of an orange-spotted grouper Epinephelus coioides heat shock protein 90AB (HSP90AB) and characterization of its expression in response to noda virus. Fish & Shellfish Immunology, 28, 895–904.CrossRefGoogle Scholar
  23. Chen, H. H., Zha, J. M., Liang, X. F., Bu, J. H., Wang, M., & Wang, Z. J. (2013). Sequencing and de novo assembly of the Asian clam (Corbicula fluminea) transcriptome using the Illumina GAIIx method. PLoS One, 8(11), e79516.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cheng, P., Liu, X., Zhang, G., & Deng, Y. (2006). Heat-shock protein 70 gene expression in four hatchery Pacific abalone Haliotis Discus Hannai Ino populations using for marker-assisted selection. Aquaculture Research, 37, 1290–1296.CrossRefGoogle Scholar
  25. Choi, Y. K., Jo, P. G., & Choi, C. Y. (2008). Cadmium affects the expression of heat shock protein 90 and metallothionein mRNA in the Pacific oysterCrassostrea gigas. Comparative Biochemistry Physiology Part C, 147, 286–292.PubMedGoogle Scholar
  26. Chowdhuri, D. K., Saxena, D. K., & Vishwanathan, P. N. (1999). Effect of hexachlorocyclohexane (HCH), its isomers, and metabolites on HSP70 expression in transgenic Drosophila melanogaster. Pesticide. Biochemistry & Physiology, 63(1), 15–25.Google Scholar
  27. Clark, M. S., & Peck, L. S. (2009). Triggers of the HSP70 stress response: Environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna). Cell Stress & Chaperones, 14, 649–660.CrossRefGoogle Scholar
  28. Cotto, J. J., & Morimoto, R. I. (1999). Stress-induced activation of the heat-shock response: Cell and molecular biology of heat-shock factors. Biochemical Society Symposium, 64, 105–118.PubMedGoogle Scholar
  29. Croute, F., Beau, B., Arrabit, C., Gaubin, Y., Delmas, F., Murat, J. C., & Soeilhavoup, J. P. (2000). Pattern of stress protein expression in human lung cell-line A549 after short or long term exposure to cadmium. Environmental Health Perspectives, 108(1), 55–60.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cui, Z., Liu, Y., Luan, W., Li, Q., Wu, D., & Whang, S. (2010). Molecular cloning and characterization of a heat shock protein 70 gene in swimming crab (Portunustri tuberculatus). Fish & Shellfish Immunology, 28, 56–64.CrossRefGoogle Scholar
  31. Dahms, H. U., & Lee, J. S. (2010). UV radiation in marine ectoderms: Molecular effects and response. Aquatic Toxicology, 97, 3–14.PubMedCrossRefGoogle Scholar
  32. Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., & Colombo, R. (2003). Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta, International Journal of Clinical Chemistry, 29(1–2), 23–38.CrossRefGoogle Scholar
  33. Deane, E. E., & Woo, N. Y. (2006). Impact of heavy metals and organochlorines on hsp70 and hsc70 gene expression in black sea bream fibroblasts. Aquatic Toxicology, 79, 9–15.PubMedCrossRefGoogle Scholar
  34. De Maio, A. (1999). Heat shock proteins: Facts, thoughts, and dreams. Shock, 11, 1–12.PubMedCrossRefGoogle Scholar
  35. De Maio, A., Santoro, M. G., Tanguay, R. M., & Hightower, L. E. (2012). Ferruccio Ritossa’s scientific legacy 50 years after his discovery of the heat shock response: A new view of biology, a new society, and a new journal. Cell Stress & Chaperones, 17, 139–143.CrossRefGoogle Scholar
  36. Didier, P. (2006). Chaperoning steroid hormone action. Trends in Endocrinology and Metabolism, 17(6), 229–235.CrossRefGoogle Scholar
  37. Dimauro, I., Mercatelli, N., & Caporossi, D. (2016). Exercise-induced ROS in heat shock proteins response. Free Radical Biology & Medicine, 98, 46–55.CrossRefGoogle Scholar
  38. Diniz, M. S., Santos, H. M., Costa, P. M., Peres, I., Costa, M. H., & Capelo, J. L. (2007). Metallothionein responses in the Asiatic clam (Corbicula fluminea) after exposure to trivalent arsenic. Biomarkers, 12, 589–598.PubMedCrossRefGoogle Scholar
  39. Dix, D. J., Allen, J. W., Collins, B. W., Mori, C., Nakamura, N., Poorman-Allen, P., Goulding, E. H., & Eddy, E. M. (1996). Targeted gene disruption of HSP70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proceedings of the National Academy of Sciences of the United States of America, 93(8), 3264–3268.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Downs, C. A., Richmond, R. H., Mendiola, W. J., Rougée, L., & Ostrander, G. K. (2006). Cellular physiological effects of the MV Kyowa violet fuel-oil spill on the hard coral Porites lobata. Environmental Toxicology and Chemistry, 25(12), 3171–3180.PubMedCrossRefGoogle Scholar
  41. Du, S. J., Li, H., Bian, Y., & Zhong, Y. (2008). Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proceedings of the National Academy of Sciences of the United States of America, 105, 554–559.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dube, V., Grigull, J., DeSouza, L. V., Ghanny, S., Colgan, T. J., Romaschin, A. D., & Siu, K. W. (2007). Verification of endometrial tissue biomarkers previously discovered using mass spectrometry-based proteomics by means of immunohistochemistry in a tissue microarray format. Journal of Proteome Research, 6, 2648–2655.PubMedCrossRefGoogle Scholar
  43. Ehrnsperger, M., Gräber, S., Gaestel, M., & Buchner, J. (1997). Binding of non-native protein to HSP25 during heat shock creates a reservoir of folding intermediates for reactivation. The EMBO Journal, 16, 221–229.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Eliason, E. J., Clark, T. D., Hague, M. J., Hanson, L. M., Gallagher, Z. S., Jeffries, K. M., et al. (2011). Differences in thermal tolerance among sockeye salmon populations. Science, 332, 109–112.PubMedCrossRefGoogle Scholar
  45. Feder, M. E., & Hofmann, G. E. (1999). Heat shock proteins, molecular chaperons, and the stress response: Evolutionary and ecological physiology. Annual Review of Physiology, 61, 243–282.PubMedCrossRefGoogle Scholar
  46. Feng, J., Guan, R., Guo, S., Lin, P., & Zadlock, F. (2014). Molecular cloning of Japanese eel Anguilla japonica TNF-αand characterization of its expression in response to LPS, poly I:C and Aeromonas hydrophila infection. Chinese Journal of Oceanology and Limnology, 32, 1046–1059.CrossRefGoogle Scholar
  47. Forsyth, R. B., Candido, E. P. M., Babich, S. L., & Iwama, G. K. (1997). Stress protein expression in coho salmon with bacterial kidney disease. Journal of Aquatic Animal Health, 9, 18–25.CrossRefGoogle Scholar
  48. Gao, Q., Zhao, J., Song, L., Qiu, L., Yu, Y., Zhang, H., et al. (2008). Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish & Shellfish Immunology, 24, 379–385.CrossRefGoogle Scholar
  49. Garrido, C., Gurbuxani, S., Ravagnan, L., & Kroemer, G. (2001). Heat shock proteins: Endogenous modulators of apoptotic cell death. Biochemical and Biophysical Research Communications, 286(3), 433–442.PubMedCrossRefGoogle Scholar
  50. Gething, M. J., & Sambrook, J. (1992). Protein folding in the cell. Nature, 355, 35–45.CrossRefGoogle Scholar
  51. Ghosh, J. G., Estrada, M. R., & Clark, J. I. (2005). Interactive domains for chaperone activity in the small heat shock protein, human alpha B crystallin. The Biochemist, 44, 14854–14869.CrossRefGoogle Scholar
  52. Giri, S. S., Sen, S. S., & Sukumaran, V. (2014). Role of HSP70 in cytoplasm protection against thermal stress in rohu, Labeo rohita. Fish & Shellfish Immunology, 41, 294–299.CrossRefGoogle Scholar
  53. Giri, S. S., Sen, S. S., Jun, J. W., Sukumaran, V., & Park, S. C. (2016). Immunotoxicological effects of cadmium on Labeo rohita, with emphasis on the expression of HSP genes. Fish & Shellfish Immunology, 54, 164–171.CrossRefGoogle Scholar
  54. Govin, J., Caron, C., Escoffier, E., Ferro, M., Kuhn, L., Rousseaux, S., et al. (2006). Post meiotic shifts in HSPA2/HSP70.2 chaperone activity during mouse spermatogenesis. The Journal of Biological Chemistry, 281, 37888–37892.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Groff, A. A., da Silva, J., Nunes, E. A., Ianistcki, M., Guecheva, T. N., de Oliveira, A. M., et al. (2010). UVA/UVB induced genotoxicty and lesion repair in Colossoma macropomum and Arapaima gigas Amazonian fish. Journal of Photochemistry Photobiology Part B, 99, 93–99.CrossRefGoogle Scholar
  56. Grosvik, B. E., & Goksoy, A. (1996). Biomarker protein expression in primary cultures of salmon (Salmo salar) hepatocytes exposed to environmental pollutants. Biomarkers, 1, 45–53.PubMedCrossRefGoogle Scholar
  57. Guo, S. L., Feng, J. J., Yang, Q. H., Guan, R. Z., Wang, Y., & Lu, P. P. (2014). Immune effects of bathing European eels in live pathogenic bacteria, Aeromonas hydrophila. Aquaculture Research, 45, 913–921.CrossRefGoogle Scholar
  58. Gupta, S. C., Siddique, H. R., Mathur, N., Mishra, R. K., Mitra, K., Saxena, D. K., et al. (2007). Adverse effect of organophosphate compounds dichlorvos and chlorpyrifos in the reproductive tissues of transgenic Drosophila Melanogaster: 70 kDa heat shock protein as a marker of cellular damage. Toxicology, 238(1), 1–14.PubMedCrossRefGoogle Scholar
  59. Hader, D. P., Kumar, H. D., Smith, R. C., & Worrest, R. C. (2007). Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Sciences, 6, 267–285.CrossRefGoogle Scholar
  60. Hallare, A. V., Köhler, H. R., & Triebskorn, R. (2004). Developmental toxicity and stress protein responses in zebrafish embryos after exposure to diclofenac and its solvent, DMSO. Chemospher, 56, 659–666.CrossRefGoogle Scholar
  61. Han, D., Huang, S. S. Y., Wang, W.-F., Deng, D.-F., & Hung, S. S. O. (2011). Starvation reduces the heat shock protein responses in white sturgeon larvae. Environmental Biology of Fishes, 93, 333–342.CrossRefGoogle Scholar
  62. Han, Y. L., Hou, C. C., Du, C., & Zhu, J. Q. (2017). Molecular cloning and expression analysis of five heat shock protein 70 (HSP70) family members in Lateolabrax maculatus with Vibro harveyi infection. Fish & Shellfish Immunology, 60, 299–310.CrossRefGoogle Scholar
  63. Harms, L., Frickenhaus, S., Schiffer, M., Mark, F. C., Storch, D., Held, C., et al. (2014). Gene expression profiling in gills of the great spider crab Hyas araneus in response to ocean acidification and warming. BMC Genomics, 15, 789.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Hartl, F. U. (1996). Molecular chaperones in cellular protein folding. Nature, 381, 571–579.PubMedCrossRefGoogle Scholar
  65. Hartl, F. U., & Hartl-Meyer, M. (2002). Molecular chaperones in the cytosol: From nascent chain to folded protein. Science, 295, 1852–1858.PubMedCrossRefGoogle Scholar
  66. Hassanein, H. M. A., Banhawy, M. A., Soliman, F. M., Abdel- Rehim, S. A., & Muller, W. E. G. (1999). Induction of HSP70 by the herbicide oxyfluoren in the Egyptian Nile fish, Oreochromis niloticus. Archives Environ Contamin. Toxicology, 37, 78–84.Google Scholar
  67. Hatfield, M. P., & Lovas, S. (2012). Role of HSP70 in cancer growth and survival. Protein and Peptide Letters, 19, 616–624.PubMedCrossRefGoogle Scholar
  68. Hawkins, T. A., Haramis, A. P., Etard, C., Prodromou, C., Vaughan, C. K., Ashworth, R., et al. (2008). The ATPase-dependent chaperoning activity of HSP90a regulates thick filament formation and integration during skeletal muscle myofibrillogenesis. Development, 135, 1147–1156.PubMedPubMedCentralCrossRefGoogle Scholar
  69. He, Y., Luo, M., Yi, M., Sheng, Y., Cheng, Y., Zhou, R., et al. (2013). Identification of a testis enriched heat shock protein and fourteen members of HSP70 family in the swamp eel. PLoS One, 8, e65269.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Heath, A. G. (1987). Water pollution and fish physiology. Florida: CRC Press.Google Scholar
  71. Henderson, B. (2003). Chaperonins: Chameleon proteins that influence myeloid cells. In W. van Eden (Ed.), Heat shock proteins and inflammation (pp. 175–192). Basle: Birkhauser.CrossRefGoogle Scholar
  72. Henderson, B., Allan, E., & Coates, A. R. (2006). Stress wars: The direct role of host and bacterial molecular chaperones in bacterial infection. Infection and Immunity, 74, 3693–3706.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hendrikson, Ronald G., and Zenoble, Robert D. (1983). Vibriosis in fish: A review, Iowa state university Veterinarian: 45(1), Article 5.Google Scholar
  74. Hermesz, E., Abraham, M., & Nemcsok, J. (2001). Identification of two HSP90 genes in carp. Comparative Biochemistry Physiology Part C, 129, 397–407.PubMedGoogle Scholar
  75. Hightower, L. E., Sadis, S. E., & Takenaka, I. O. (1994). Interactions of vertebrate hsc70 and HSP70 with unfolded proteins and peptides. In R. I. Morimoto, A. Tissieres, & C. Georgopoulos (Eds.), The biology of heat shock proteins and molecular Chaperones (pp. 109–208). New York: Cold Spring Harbor Laboratory Press.Google Scholar
  76. Holm, K., Hernroth, B., & Thorndyke, M. (2008). Coelomocyte numbers and expression of HSP70 in wounded sea stars during hypoxia. Cell Tissue Research, 334, 319–325.PubMedCrossRefGoogle Scholar
  77. Hook, S. E., Skillman, A. D., Small, J. A., & Schultz, I. R. (2006). Gene expression patterns in rainbow trout, Oncorhynchus mykiss, exposed to a suite of model toxicants. Aquatic Toxicology, 77(4), 372–385.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Huang, P., Kang, S., Chen, W., Hsu, T., Lo, C., Liu, K., & Chen, L. (2008). Identification of the small heat shock proteins HSP21, of shrimp Penaeus monodon and the gene expression of HSP21 is inactivated after white spot syndrome virus (WSSV) infection. Fish & Shellfish Immunology, 25, 250–257.CrossRefGoogle Scholar
  79. Huang, W. J., Leu, J. H., Tsau, M. T., Chen, J. C., & Chen, L. L. (2011). Differential expression of LvHSP60 in shrimp in response to environmental stress. Fish & Shellfish Immunology, 30, 576–582.CrossRefGoogle Scholar
  80. Hughes, M. F. (2002). Arsenic toxicity and potential mechanisms of action. Toxicology Letters, 133, 1–16.PubMedCrossRefGoogle Scholar
  81. Imlay, J. A., & Linn, S. (1988). DNA damage and oxygen radical toxicity. Science, 240, 1302–1309.PubMedCrossRefGoogle Scholar
  82. Ingolia, T. D., & Craig, E. A. (1982). Drosophila gene related to the major heat shock induced gene is transcribed at normal temperatures and not induced by heat shock. Proceedings of the National Academy of Sciences of the United States of America, 79, 525–529.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Iwama, G. K., Vijayan, M. M., Forsyth, R. B., & Ackerman, P. A. (1999). Heat shock proteins and physiological stress in fish. Integrative and Comparative Biology, 39(6), 901–909.Google Scholar
  84. Iwama, G. K., Afonso, L. O. B., Todgham, A., Ackerman, P., & Nakano, K. (2004). Are HSP suitable for indicating stressed states in fish. The Journal of Experimental Biology, 207, 15–19.PubMedCrossRefGoogle Scholar
  85. Jackson, S. E. (2013). HSP90: Structure and function. Topics in Current Chemistry, 328, 155–240.PubMedCrossRefGoogle Scholar
  86. Jacquier-Sarlin, M. R., & Polla, B. S. (1996). Dual regulation of heat-shock transcription factor (HSF) activation and DNA-binding activity by H2O2: Role of thioredoxin. The Biochemical Journal, 318, 187–193.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Jee, H. (2016). Size dependent classification of heat shock proteins: A mini-review. Journal of Exercise Rehabilitation, 12(4), 255–259.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Jiang, S., Qiu, L., Zhou, F., Huang, J., Guo, Y., & Yang, K. (2009). Molecular cloning and expression analysis of a heat shock protein (HSP90) gene from black tiger shrimp (Penaeus monodon). Molecular Biology Reports, 36, 127–134.PubMedCrossRefGoogle Scholar
  89. Jing, J., Liu, H., Chen, H., Hu, S., Xiao, K., & Ma, X. (2013). Acute effect of copper and cadmium exposure on the expression of heat shock protein 70 in the Cyprinidae fish Tanichthys albonubes. Chemosphere, 91, 1113–1122.PubMedCrossRefGoogle Scholar
  90. Jiravanichpaisal, P., Lee, B. L., & Söderhäll, K. (2006). Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology, 211, 213–236.PubMedCrossRefGoogle Scholar
  91. Jonak, C., Klosner, G., & Trautinger, F. (2006). Heat shock proteins in the skin. International Journal of Cosmetic Science, 28, 233–241.PubMedCrossRefGoogle Scholar
  92. Juo, L. Y., Liao, W. C., Shih, Y. L., Yang, B. Y., Liu, A. B., & Yan, Y. T. (2016). HSPB7 interacts with dimerized FLNC and its absence results in progressive myopa thy in skeletal muscles. Journal of Cell Science, 129, 1661–1670.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Kaarniranta, K., Elo, M., Sironen, R., Lammi, M. J., Goldring, M. B., Eriksson, J. E., et al. (1998). HSP70 accumulation in chondrocytic cells exposed to high continuous hydrostatic pressure coincides with mRNA stabilization rather than transcriptional activation. Proceedings of the National Academy of Sciences of the United States of America, 95, 2319–2324.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Kaarniranta, K., Oksala, N., Karjalainen, H. M., Suuronen, T., Sistonen, L., Helminen, H. J., et al. (2002). Neuronal cells show regulatory differences in the HSP70 gene response. Brain Research, 101, 136–140.PubMedCrossRefGoogle Scholar
  95. Kampinga, H. H., Hageman, J., Vos, M. J., Kubota, H., Tanguay, R. M., Bruford, E. A., et al. (2009). Guidelines for the nomenclature of the human heat shock proteins. Cell Stress & Chaperones, 14, 105–111.CrossRefGoogle Scholar
  96. Kappe, G., Verschuure, P., Philipsen, R. L., Staalduinen, A. A., Van de Boogaart, P., Boelens, W. C., et al. (2001). Characterization of two novel human small heat shock proteins: Protein kinase-related HSPB8 and testis-specific HSPB9. Biochimica et Biophysica Acta, 1520, 1–6.PubMedCrossRefGoogle Scholar
  97. Katersky, R. S., & Carter, C. G. (2007). High growth efficiency occurs over a wide temperature range for juvenile barramundi Lates calcarifer fed a balanced diet. Aquaculture, 272, 444–450.CrossRefGoogle Scholar
  98. Kayhan, F. E., & Duman, B. S. (2010). Heat shock protein genes in fish. Turkish Journal of Fisheries and Aquatic Sciences, 10, 287–293.CrossRefGoogle Scholar
  99. Ke, L, Meijering, R.A., Hoogstra-Berends, F, Mackovicova, K., Vos, M.J., Van Gelder, I.C., Henning, R.H., Kampinga, H.H., & Brundel, B.J. (2011). HSPB1, HSPB6, HSPB7 and HSPB8 protect against RhoA GTP aseinduced remodeling in tachypaced atrial myocytes. PLoS One, 6, e20395.Google Scholar
  100. Keller, J. M., Escara-Wilke, F., & Keller, E. T. (2008). Heat stress induced heat shock protein 70 expression is dependent on ERK activation in zebrafish (Danio rerio) cells. Comparative Biochemistry and Physiology. A, Comparative Physiology, 150, 307–314.CrossRefGoogle Scholar
  101. Kelly, P.D., Chu, F., Woods, I.G., Ngo-Hazelett, P., Cardozo, T., Huang, H. et al. (2000). Genetic linkage mapping of zebrafish genes and ESTs. Cold Spring Harbor Laboratory Press. ISSN 1088-9051/0.Google Scholar
  102. Kim, J. H., & Kang, J. C. (2015). The arsenic accumulation and its effect on oxidativestress responses in juvenile rockfish, Sebastes schlegelii, exposed to water borne arsenic (As3+). Environmental Toxicology and Pharmacology, 39, 668–676.PubMedCrossRefGoogle Scholar
  103. Kim, J. H., & Kang, J. C. (2016). The immune responses and expression of metallothionein (MT) gene and heat shock protein 70 (HSP70) in juvenile rockfish, Sebates schlegelii, exposed to water born arsenic (As3+). Environmental Toxicology Phormocol, 47, 136–141.CrossRefGoogle Scholar
  104. Kobayashi, H., Iwamatsu, T., Shibata, Y., Ishihara, M., & Kobayashi, Y. (2011). Effects of co-administration of estrogen and androgen on induction of sex reversal in the medaka Oryzias latipes. Zoological Science, 28(5), 355–359.PubMedCrossRefGoogle Scholar
  105. Kohno, S., Katsu, Y., Urushitani, H., Ohta, Y., Iguchi, T., & Guillette, L. J., Jr. (2010). Potential contributions of heat shock proteins to temperature-dependent sex determination in the American alligator. Sexual Development, 4(1–2), 73–87.PubMedCrossRefGoogle Scholar
  106. Lanneau, D., Brunet, M., Frisan, E., Solary, E., Fontenay, M., & Garrido, C. (2008). Heat shock proteins: Essential proteins for apoptosis regulation. Journal of Cellular and Molecular Medicine, 12(3), 743–761.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Lauritano, C., Orefice, I., Procaccini, G., Romano, G., & Ianora, A. (2015). Key genes as stress indicators in the ubiquitous diatom Skeletonema marinoi. BMC Genomics, 16, 411.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Lauritano, C., Romano, G., Roncalli, V., Amoresano, A., Fontanarosa, C., Bastianini, M., et al. (2016). New oxylipins produced at the end of a diatom bloom and their effects on copepod reproductive success and gene expression levels. Harmful Algae, 55, 221–229.PubMedCrossRefGoogle Scholar
  109. Lee, J. Y., Cho, W. J., Do, J. W., Kim, H. J., & Park, J. W. (1996). Monoclonal antibodies raised against Infectious Haematopoietic Necrosis Virus (IHNV) G protein and a cellular 90 kDa protein neutralize IHNV infection in vitro. The Journal of General Virology, 77, 1731–1737.PubMedCrossRefGoogle Scholar
  110. Li, F. J., Luan, W., Zhang, C. S., Zhang, J. Q., Wang, B., Xie, Y. S., et al. (2009). Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress & Chaperones, 14, 161–172.CrossRefGoogle Scholar
  111. Li, Z. H., Chen, L., Wu, Y. H., Li, P., Li, Y. F., & Ni, Z. H. (2014). Effects of waterborne cadmium on thyroid hormone levels and related gene expression in Chinese rare minnow larvae. Comparative Biochemistry and Physiology Part C Toxicology and Pharmacology, 161, 53–57.PubMedCrossRefGoogle Scholar
  112. Li, J., Zhang, H., Zhang, X., Yang, S., Yan, T., & Song, Z. (2015). Molecular cloning and expression of two heat-shock protein genes (HSC70/HSP70) from Prenant’s schizothoracin (Schizothorax prenanti). Fish Physiology and Biochemistry, 41, 573–585.PubMedCrossRefGoogle Scholar
  113. Liang, F., Zhang, G., Yin, S., Wang, L. (2016). The role of three heat shock protein genes in the immune response to Aeromonas hydrophila challenge in marbled eel, Anguilla marmorata. Royal Society Open Science 3(10), 160375.Google Scholar
  114. Lindquist, S., & Craig, E. A. (1988). The heat shock proteins. Annual Review of Genetics, 22, 631–677.PubMedCrossRefGoogle Scholar
  115. Liu, J., Yang, W. J., Zhu, X. J., Karounarenier, N. K., & Rao, R. K. (2004). Molecular cloning and expression of two HSP70 genes in the prawn, Macrobrachium rosenbergii. Cell Stress and Chaperones, 9, 313–323.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Liu, H., Zheng, F., Sun, X., Hong, X., Dong, S., Wang, B., et al. (2010). Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). Journal of Invertebrate Pathology, 105, 236–242.PubMedCrossRefGoogle Scholar
  117. Liu, T., Pan, L., Cai, Y., & Miao, J. (2014). Molecular cloning and sequence analysis of heat shock proteins 70 (HSP70) and 90 (HSP90) and their expression analysis when exposed to benzo(a)pyrene in the clam Ruditapes philippinarum. Gene, 555(2), 108–118.PubMedCrossRefGoogle Scholar
  118. Mahmood, K., Jadoon, S., Mahmood, Q., Irshad, M., & Hussain, J. (2014). Synergistic effects of toxic elements on heat shock proteins. BioMed Research International, 2014, 1–17.Google Scholar
  119. Manfrin, C., Dreos, R., Battistella, S., Beran, A., Gerdol, M., Varotto, L., et al. (2010). Mediterranean mussel gene expression profile induced by okadaic acid expressure. Environmental Science & Technology, 44, 8276–8283.CrossRefGoogle Scholar
  120. Meyer, A. S., Gillespie, J. R., Walther, D., Millet, I. S., Doniach, S., & Frydman, J. (2003). Closing the folding chamber of the eukaryotic chaperon in requires the transition state of ATP hydrolysis. Cell, 113, 369–381.PubMedCrossRefGoogle Scholar
  121. MiCoviC, V., Bulog, A., KuciC, V., Jakovac, H., & StasiC, B. R. (2009). Metallothioneins and heat shock proteins 70 in marine mussels as sensors of environmental pollution in northern Adriatic Sea. Environmental Toxicology and Pharmacology, 28, 439–447.PubMedCrossRefGoogle Scholar
  122. Ming, J., Xie, J., Xu, P., Liu, W., Ge, X., Liu, B., et al. (2010). Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala Yih). Fish & Shellfish Immunology, 28, 407–418.CrossRefGoogle Scholar
  123. Mirkes, P. E., Doggett, B., & Cornel, L. (1994). Induction of a heat shock response (HSP72) in rat embryos exposed to selected chemical teratogens. Teratology, 49(2), 135–142.PubMedCrossRefGoogle Scholar
  124. Mitchell, D. L., Nairn, R. S., Jhonston, D. A., Byrom, M., Kazianis, S., & Walter, R. B. (2004). Decreased level of (6–4) photoproduct excision repair in hybrid fish of genus Xiphophorus. Photochemistry and Photobiology, 79, 447–452.PubMedCrossRefGoogle Scholar
  125. Mock, A., & Peters, G. (1990). Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handling, transport and water pollution. Journal of Fish Biology, 37, 873–885.CrossRefGoogle Scholar
  126. Moczko, M., Schönfisch, B., Voos, W., Pfanner, N., & Rassow, J. (1995). The mitochondrial ClpB homolog HSP78 cooperates with matrix HSP70 in maintenance of mitochondrial function. Journal of Molecular Biology, 254, 538–543.PubMedCrossRefGoogle Scholar
  127. Morimoto, R. I. (1993). Cells in stress: Transcriptional activation of heat shock genes. Science, 259(5100), 1409–1410.PubMedCrossRefGoogle Scholar
  128. Mork, L., Czerwinski, M., & Capel, B. (2014). Predetermination of sexual fate in a turtle with temperature-dependent sex determination. Developmental Biology, 386(1), 264–271.PubMedCrossRefGoogle Scholar
  129. Mounier, N., & Arrigo, A. P. (2002). Actin cytoskelaton and small heat shock proteins: How do they interact? Cell Stress & Chaperones, 7, 167–176.CrossRefGoogle Scholar
  130. Moya, A., Huisman, L., Foret, S., Gattuso, J. P., Hayward, D. C., Ball, E. E., et al. (2015). Rapid acclimation of juvenile corals to CO-mediated acidification by up regulation of heat shock protein and Bcl-2 genes. Molecular Ecology, 24, 438–452.PubMedCrossRefGoogle Scholar
  131. Mu, W., Wen, H., Li, J., & He, F. (2013). Cloning and expression analysis of a HSP70 gene from Korean rockfish (Sebastes schlegeli). Fish & Shellfish Immunology, 35, 1111–1121.CrossRefGoogle Scholar
  132. Multhoff, G. (2007). Heat shock protein 70 (HSP70): Membrane location, export and immunological relevance. Methods, 43, 229–237.PubMedCrossRefGoogle Scholar
  133. Mutwakil, M. H., Reader, J. P., Holdich, D. M., Smithurst, P. R., Candido, E. P. M., Jones, D., et al. (1997). Use of stress-inducible transgenic nematodes as biomarkers of heavy-metal pollution in water samples from english river system. Archives of Environmental Contamination and Toxicology, 32(2), 146–153.PubMedCrossRefGoogle Scholar
  134. Nakamura, H. (2005). Thioredoxin and its related molecules: Update. Antioxidant and Redox Signalling, 7, 823–828.CrossRefGoogle Scholar
  135. Nakamura, H., Nakamura, K., & Yodoi, J. (1997). Redox regulation of cellular activation. Annual Review of Immunology, 15, 351–369.PubMedCrossRefGoogle Scholar
  136. Nazir, A., Mukhopadhyay, I., Saxena, D. K., & Chowdhuri, D. K. (2006). HSP70 expression in Drosophila melanogaster: Toxicological perspective. In A. S. Sreedhar & U. K. Srinivas (Eds.), Stress response: A molecular biology approach (pp. 207–226). Trivandrum: Research Singpost Press.Google Scholar
  137. Neckers, L. (2007). Heat shock protein 90: The cancer chaperone. Journal of Biosciences, 32, 517–530.PubMedCrossRefGoogle Scholar
  138. Nilsson, G. E., Crawley, N., Lunde, I. G., & Munday, P. L. (2009). Elevated temperature reduces the respiratory scope of coral reef fishes. Global Change Biology, 15, 1405–1412.CrossRefGoogle Scholar
  139. Noonan, F. P., Halliday, W. J., Morton, H., & Clunie, G. J. (1979). Early pregnancy factor is immunosuppressive. Nature, 278, 649–651.PubMedCrossRefGoogle Scholar
  140. Ogawa, K., Seta, R., Shimizu, T., Shinkai, S., Calderwood, S. K., Nakazato, K., & Takahashi, K. (2011). Plasma adenosine triphosphate and heat shock protein 72 concentrations after aerobic and eccentric exercise. Exercise Immunology Review, 17, 136–149.PubMedGoogle Scholar
  141. Olla, B. L., Studholme, A. L., Bejda, A. J., Samet, C., & Martin, A. D. (1978). Effect of temperature on activity and social behavior of the adult tautog Tautoga onitis under laboratory conditions. Marine Biology, 45, 369–378.CrossRefGoogle Scholar
  142. Orosz, A., Wisniewski, J., & Wu, C. (1996). Regulation of drosophila heat shock factor trimerization: Global sequence requirements and independence of nuclear localization. Molecular Cellular Biology, 16(12), 7018–7030.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Padmini, E., & Usha Rani, M. (2008). Impact of seasonal variation on HSP70 expression quantitated in stressed fish hepatocytes. Comparative Biochemistry and Physiology Part B, 151, 278–285.CrossRefGoogle Scholar
  144. Padmini, E., & Usha Rani, M. (2009). Seasonal influence on heat shock protein 90α and heat shock factor 1 expression during oxidative stress in fish hepatocytes from polluted estuary. Journal of Experimental Marine Biology and Ecology, 372, 1–8.CrossRefGoogle Scholar
  145. Padmini, E., & Rani, M. U. (2010). Thioredoxin and HSP90 alpha modulate ASK1-JNK1/2 signaling in stressed hepatocytes of Mugil cephalus. Comparative Biochemistry and Physiology C Toxicology and Pharmacology, 151(2), 187–193.PubMedCrossRefGoogle Scholar
  146. Padmini, E., & Vijaya Geetha, B. (2012). Mitochondrial HSP70 cognate-mediated differential expression of JNK1/2 in the pollution stressed grey mullets, Mugil cephalus. Fish Physiology and Biochemistry, 38(5), 1257–1271.PubMedCrossRefGoogle Scholar
  147. Padmini, E., Lavanya, S., & Uthra, V. (2009). Preeclamptic placental stress and over expression ofmitochondrial HSP70. Clinical Chemistry and Laboratory Medicine, 47(9), 1073–1080.Google Scholar
  148. Parcellier, A., Gurbuxani, S., Schmitt, E., Solary, E., & Garrido, C. (2003). Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways. Biochemical and Biophysical Research Communications, 304(3), 505–512.PubMedCrossRefGoogle Scholar
  149. Park, H., Ahn, I. Y., & Lee, H. E. (2007). Expression of heat shock protein 70 in the thermally stressed Antarctic clam Laternula elliptica. Cell Stress & Chaperones, 12, 275–282.CrossRefGoogle Scholar
  150. Parsell, D. A., & Lindquist, S. (1993). The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annual Review of Genetics, 27, 437–496.PubMedCrossRefGoogle Scholar
  151. Parsell, D. A., Taulien, J., & Lindquist, S. (1993). The role of heat-shock proteins in thermotolerance. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 339, 279–285.PubMedCrossRefGoogle Scholar
  152. Pearl, L. H., & Prodromou, C. (2000). Structure and in vivo function of HSP90. Current Opinion in Structural Biology, 10, 46–51.PubMedCrossRefGoogle Scholar
  153. Peck, L. S. (2011). Organisms and responses to environmental change. Marine Genomics, 4, 237–243.PubMedCrossRefGoogle Scholar
  154. Pelham, H. R. (1982). A regulatory upstream promoter element in the Drosophila HSP 70 heat-shock gene. Cell, 30, 517–528.PubMedCrossRefGoogle Scholar
  155. Picard, D. (2002). Heat shock protein 90, a chaperone for folding and regulation. Cellular and Molecular Life Sciences, 59, 1640–1648.PubMedCrossRefGoogle Scholar
  156. Pinto, E., Sigaud-Kutner, T. C. S., Leitao, M. A. S., Okamoto, O. K., Morse, D., & Colepicolo, P. (2003). Heavy metal-induced oxidative stress in algae. Journal of Phycology, 39, 1008–1018.CrossRefGoogle Scholar
  157. Pirkkala, L., Nykanen, P., & Sistonen, L. (2001). Roles of the heat shock transcprition factors in regulation of the heat shock response and beyond. Federation of American Societies for Experimental Biology, 15, 1118–1131.CrossRefGoogle Scholar
  158. Ponomarenko, M., Stepanenko, I., & Kolchanov, N. (2013). Heat shock proteins in Brenner’s encyclopedia of genetics (2nd ed.pp. 402–405).CrossRefGoogle Scholar
  159. Portner, H. O., & Farrell, A. P. (2008). Physiology and climate change. Science, 322, 690–692.PubMedCrossRefGoogle Scholar
  160. Portner, H. O., & Knust, R. (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science, 315, 95–97.PubMedCrossRefGoogle Scholar
  161. Pretto, A., Loro, V. L., Morsch, V. M., Moraes, B. S., Menezes, C., & Clasen, B. (2010). Acetylcholinesterase activity, lipid peroxidation, and bioaccumulation in silver catfish (Rhamdia quelen) exposed to cadmium. Archives of Environmental Contamination and Toxicology, 58, 1008–1014.PubMedCrossRefGoogle Scholar
  162. Qi, J., Liu, X., Liu, J., Yu, H., Wang, W., Wang, Z., & Zhang, Q. (2014). Molecular characterization of heat shock protein 70 (HSP70) promoter in Japanese flounder (Paralichthys olivaceus), and the association of PoHSP70 SNPs with heat-resistant trait. Fish & Shellfish Immunology, 39, 503–511.CrossRefGoogle Scholar
  163. Quinn, K. A., & Morton, H. (1992). Effect of monoclonal antibodies to Early Pregnancy Factor (EPF) on the in vivo growth of transplantable murine tumours. Cancer Immunology, Immunotherapy, 34, 265–271.PubMedCrossRefGoogle Scholar
  164. Raina, S., & Missiakas, D. (1997). Making and breaking disulfide bonds. Annual Review of Microbiology, 51, 179–202.PubMedCrossRefGoogle Scholar
  165. Rajeshkumar, S., & Munuswamy, N. (2011). Impact of metals on histopathology and expression of HSP 70 in different tissues of milk fish (Chanos chanos) of Kattuppalli Island, South east coast, India. Chemosphere, 83, 415–421.PubMedCrossRefGoogle Scholar
  166. Rajeshkumar, S., Mini, J., & Munuswamy, N. (2013). Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. Ecotoxicology and Environmental Safety, 98, 8–18.PubMedCrossRefGoogle Scholar
  167. Ramaglia, V., Harapa, G. M., White, N., & Buck, L. T. (2004). Bacterial infection and tissue-specific Hsp72, 73 and −90 expression in western painted turtles. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 138(2), 139–148.Google Scholar
  168. Reports, B., & Kumar, T. C. A. (1962). Shock and DNP in Drosophila, 55, 571–573.Google Scholar
  169. Rietsch, A., & Beckwith, J. (1998). The genetics of disulfide bond metabolism. Annual Review of Genetics, 32, 163–184.PubMedCrossRefGoogle Scholar
  170. Roberts, R. J., Agius, C., Saliba, C., Bossier, P., & Sung, Y. Y. (2010). Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: A review. Journal of Fish Diseases, 33, 789–801.PubMedCrossRefGoogle Scholar
  171. Rodius, F., Doyen, P., & Vasseur, P. (2005). cDNA cloning and expression pattern of pi-class glutathione S-transferase in the freshwater bivalves Unio tumidus and Corbicula fluminea. Comparative Biochemistry and Physiology Part C, Toxicology & Pharmacology, 140, 300–308.CrossRefGoogle Scholar
  172. Romani, W. A., & Russ, D. W. (2013). Acute effects of sex-specific sex hormones on heat shock proteins in fast muscle of male and female rats. European Journal of Applied Physiology, 113(10), 2503–2510.PubMedCrossRefGoogle Scholar
  173. Rosario, M. O., Perkins, S. L., O’Brien, D. A., Allen, R. L., & Eddy, E. M. (1992). Identification of the gene for the developmentally expressed 70 kDa heat-shock protein (P70) of mouse spermatogenic cells. Developmental Biology, 150, 1–11.PubMedCrossRefGoogle Scholar
  174. Rosenfeld, G. E., Mercer, E. J., Mason, C. E., & Evans, T. (2013). Small heat shock proteins Hspb7 and Hspb12 regulate early steps of cardiac morphogenesis. Developmental Biology, 381, 389–400.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Rungrassamee, W., Leelatanawit, R., Jiravanichpaisal, P., Klinbunga, S., & Karoonuthaisiri, N. (2010). Expression and distribution of three heat shock protein genes under heat shock stress and under exposure to Vibrio harveyi in Penaeus monodon. Developmental and Comparative Immunology, 34, 1082–1089.PubMedCrossRefGoogle Scholar
  176. Ryan, J. A., & Hightower, L. E. (1996). Stress proteins as molecular biomarkers for environmental toxicology. In U. Feige, I. Yahara, R. I. Morimoto, & B. S. Polla (Eds.), Stess-Indrucible cellular responses. EXS (Vol. 77). Basel: Birkhäuser.Google Scholar
  177. Saluja, A. & Dudeja, V. (2008). Heat shock proteins in pancreatic diseases. Journal of Gastroenterology and Hepatology, 23 (1), 42-45.Google Scholar
  178. Samali, A., & Orrenius, S. (1998). Heat shock proteins: Regulations of stress response and apoptosis. Cell & Stress Chaperones, 3, 228–236.CrossRefGoogle Scholar
  179. Sampaio, F. G., Boijink, C. L., Oba, E. T., Santos, L. R. B., Kalinin, A. L., & Rantin, F. T. (2008). Antioxidant defenses and biochemical changes in pacu (Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comparative Biochemistry and Physiology. Part C, 147, 43–51.Google Scholar
  180. Sanders, B. M. (1993). Stress proteins in aquatic organisms: An environmental perspective. Critical Reviews in Toxicology, 23, 49–75.PubMedCrossRefGoogle Scholar
  181. Sandrini, J. Z., Trinade, G. S., Nery, L. E. M., & Marins, L. F. (2009). Time-course expression of DNA repair-related genes in hepatocytes of zebrafish after UV-B exposure. Photochemistry and Photobiology, 85, 220–226.PubMedCrossRefGoogle Scholar
  182. Schlenk, D., Wolford, L., Chelius, M., Steevens, J., & Chan, K. M. (1997). Effect of arsenite, arsenate, and the herbicide monosodium methyl arsenate (MSMA) on hepatic metallothionein expression and lipid peroxidation in channel catfish. Comparative Biochemistry and Physiolo Part C Pharmacology, Toxicol & Endocrinology, 118, 177–183.CrossRefGoogle Scholar
  183. Schlesinger, M. J. (1990). Heat shock proteins. The Journal of Biological Chemistry, 265(21), 12111–12114.PubMedGoogle Scholar
  184. Seveso, D., Montano, S., Strona, G., Orlandi, I., Galli, P., & Vai, M. (2014). The susceptibility of corals to thermal stress by analyzing HSP60 expression. Marine Environmental Research, 99, 69–75.PubMedCrossRefGoogle Scholar
  185. Sherman, M. Y., & Goldberg, A. L. (2001). Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron, 29, 15–32.PubMedCrossRefGoogle Scholar
  186. Siddique, H. R., Gupta, S. C., Mitra, K., Murthy, R. C., Saxena, D. K., & Chowdhuri, D. K. (2007). Induction of biochemical stress markers and apoptosis in transgenic Drosophila melanogaster against complex chemical mixtures: Role of reactive oxygen species. Chemico-Biological Interactions, 169(3), 171–188.PubMedCrossRefGoogle Scholar
  187. Siddique, H. R., Mitra, K., Bajpai, V. K., Ravi Ram, K., Saxena, D. K., & Chowdhuri, D. K. (2009). Hazardous effect of tannery solid waste leachates on development and reproduction in Drosophila Melanogaster: 70 kDa heat shock protein as a marker of cellular damage. Ecotoxicology and Environmental Safety, 72(6), 1652–1662.PubMedCrossRefGoogle Scholar
  188. Sikora, A., & Grzesiuk, E. (2007). Heat shock response in gastrointestinal tract. Journal of Physiology and Pharmacology, 58(3), 43–62.PubMedGoogle Scholar
  189. Silver, J. T., & Noble, E. G. (2012). Regulation of survival gene HSP70. Cell Stress & Chaperones, 17, 1–9.CrossRefGoogle Scholar
  190. Simone, F., Adrienne, M. G., Osamu, H., & Afshin, S. (2010). Cellular stress responses: Cell survival and cell death. International Journal of Cell Biology, 2010, 1–23.Google Scholar
  191. Singh, A. K. (2013). Introduction ofmodern endocrine techniques for the production of monosex population of fishes. General and Comparative Endocrinology, 181, 146–155.PubMedCrossRefGoogle Scholar
  192. Singh, M. P., Reddy, M. M., Mathur, N., Saxena, D. K., & Chowdhuri, D. K. (2009). Induction of HSP70, HSP60, HSP83 and HSP26 and oxidative stress markers in benzene, toluene and xylene exposed Drosophila Melanogaster: Role of ROS generation. Toxicology and Applied Pharmacology, 235(2), 226–243.PubMedCrossRefGoogle Scholar
  193. Singh, M. K., Sharma, J. G., & Chakrabarti, R. (2013). Effect of UV-B radiation on the defence system of Labeo rohita (Actinopterygii: Cypriniformes: Cyprinidae) larvae and its modulation by seed of Devil’s horsewhip Achyranthes aspera. Acta Ichthyologica et Piscatoria, 43, 119–126.CrossRefGoogle Scholar
  194. Somero, G. (1995). Proteins and temperature. Annual Review of Physiology, 57, 43–68.PubMedCrossRefGoogle Scholar
  195. Sorensen, J. G., & Kristensen, T. N. (2003). The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6, 1025–1037.CrossRefGoogle Scholar
  196. Soti, C. S., Nagy, E., Giricz, Z., Vigh, L., Csermely, P., & Ferdinandy, P. (2005). Heat shock proteins as emerging therapeutic targets. British Journal of Pharmacology, 146, 769–780.PubMedPubMedCentralCrossRefGoogle Scholar
  197. Spann, N., Aldridge, D. C., Griffin, J. L., & Jones, O. A. H. (2011). Size-dependent effects of low level cadmium and zinc exposure on the metabolome of the Asian clam, Corbicula fluminea. Aquatic Toxicology, 105, 589–599.PubMedCrossRefGoogle Scholar
  198. Sreedhar, A. S., Kalmar, E., Csermely, P., & Shen, Y. F. (2004). HSP90 isoforms: Functions, expression and clinical importance. FEBS Letters, 562, 11–15.PubMedCrossRefGoogle Scholar
  199. Stringham, E. G., & Candido, E. P. M. (1994). Transgenic HSP16-lacZ strains of the soil nematode Caenorhabditis Elegans as biological monitors of environmental stress. Environmental Toxicology and Chemistry, 13(8), 1211–1220.CrossRefGoogle Scholar
  200. Stringham, E. G., Dixon, D. K., Jones, D., & Candido, E. P. M. (1992). Temporal and spatial expression patterns of small heat shock (HSP16) genes in transgenic Caenorhabditis Elegans. Molecular Biology of the Cell, 3(2), 221–233.PubMedPubMedCentralCrossRefGoogle Scholar
  201. Sucre, E., Vidussi, F., Mostajir, B., Charmantier, G., & Lorin-Nebel, C. (2012). Impact of ultraviolet-B radiation on planktonic fish larvae: Alteration of the osmoregulatory function. Aquatic Toxicology, 109, 194–201.PubMedCrossRefGoogle Scholar
  202. Sung, Y. Y., & Mac Rae, T. H. (2011). Heat shock proteins and disease control in aquatic organisms. Journal of Aquaculture Research and Development. S2:006.Google Scholar
  203. Tavaria, M., Gabriele, T., Kola, I., & Anderson, R. L. (1996). A hitchhiker’s guide to the human HSP 70 family. Cell Stress Chaperon, 1, 23–28.CrossRefGoogle Scholar
  204. Tissieres, A., Mitchell, H. K., & Tracy, V. M. (1974). Protein synthesis in salivary glands of Drosophila melanogaster. Relation to chromosome puffs. Journal of Molecular Biology, 84, 389–398.PubMedCrossRefGoogle Scholar
  205. Tomanek, L. (2010). Variation in the heat shock response and its implication for predicting the effect of global climate change on species biogeographical distribution ranges and metabolic costs. The Journal of Experimental Biology, 213, 971–979.PubMedCrossRefGoogle Scholar
  206. Triantafilou, K., Triantafilou, M., & Dedrick, R. L. (2001). A CD14-independent LPS receptor cluster. Nature Immunology, 2, 338–345.PubMedCrossRefGoogle Scholar
  207. Ulloa, V. S., Tajes, J. F., Manfrin, C., Gerdol, M., Venier, P., & Lopez, J. M. E. (2013). Bivalve omics: State of the art and potential applications for the biomonitoring of harmful marine compounds. Marine Drugs, 11, 4370–4389.CrossRefGoogle Scholar
  208. Val, A. L., Castro-Perez, C. A., & Almeida-Val, V. M. F. (2004). UV an environmental challenge for fish of Amazon. In S. Dee (Ed.), VI International congress on biology of fishes, Manaus, advance in fish biology (pp. 1–5). Vancouver: American Fisheries Society- Physiology Section 1.Google Scholar
  209. Vasconcelos, V., Martins, J. C., & Leao, P. N. (2009). Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain. Toxicon, 53, 409–416.PubMedCrossRefGoogle Scholar
  210. Vega, E., Hall, M., Degnan, B., & Wilson, K. (2006). Short-term hyperthermic treatment of Penaeus monodon increases expression of heat shock protein 70 (HSP70) and reduces replication of Gill Associated Virus (GAV). Aquaculture, 253, 82–90.CrossRefGoogle Scholar
  211. Vehniainen, E. R., Vahakangas, K., & Oikari, A. O. J. (2012). UV-B exposure causes DNA damages and changes in protein expression in Northern pike (Esox lucius) post hatched embryo. Photochemistry and Photobiology, 88, 363–370.PubMedCrossRefGoogle Scholar
  212. Vijayan, M. M., Pereira, C., Kruzynski, G., & Iwama, G. K. (1998). Sublethal concentrations of contaminant induce the expression of hepatic HSP70 in two salmonids. Aquatic Toxicology, 40, 101–108.CrossRefGoogle Scholar
  213. Vogel, M., Bukau, B., & Mayer, M. P. (2006). Allosteric regulation of HSP70 chaperones by a proline switch. Molecular Cell, 21, 359–367.PubMedCrossRefGoogle Scholar
  214. Wang, T., & Overgaard, J. (2007). The heart break of adapting to global warming. Science, 315, 49–50.PubMedCrossRefGoogle Scholar
  215. Wang, J., Wei, Y., Li, X., Cao, H., Xu, M., & Dai, J. (2007). The identification of heat shock protein genes in goldfish (Carassius auratus) and their expression in a complex environment in Gaobeidian Lake, Beijing, China. Comparative Biochemistry and Physiology - Part C, 145, 350–362.PubMedGoogle Scholar
  216. Wei, T., Gao, Y., Wang, R., & Xu, T. (2013). A heat shock protein 90 beta isoform involved in immune response to bacteria challenge and heat shock from Miichthys miiuy. Fish & Shellfish Immunology, 35, 429–437.CrossRefGoogle Scholar
  217. Whitley, D. M. D., Steven, P., Goldberg, M. D., William, D., & Jordan, M. D. (1999). Heat shock proteins: A review of the molecular chaperones. Journal of Vascular Surgery, 29, 748–751.PubMedCrossRefGoogle Scholar
  218. Williams, J. H., Farag, A. M., Stansbury, M. A., Young, P. A., Bergman, H. L., & Peterson, N. S. (1996). Accumulation of HSP70 in juvenile and adult rainbow trout gill exposed to metal contaminated water and/or diet. Environmental Toxicology and Chemistry, 15, 1324–1328.CrossRefGoogle Scholar
  219. Woo, S., Yum, S., Park, H. S., Lee, T. K., & Ryu, J. C. (2009). Effects of heavy metals on antioxidants and stress responsive gene expression in Javanese medaka (Oryzias javanicus). Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 149, 289–299.Google Scholar
  220. Wu, C. (1995). Heat shock transcription factors: Structure and regulation. Annual Review of Cell and Developmental Biology, 11, 441–469.PubMedCrossRefGoogle Scholar
  221. Wu, X., Tan, J., Cai, M., & Liu, X. (2014). Molecular cloning, characterization, and expression analysis of a Heat Shock Protein (HSP) 70 gene from Paphia undulata. Gene, 543, 275–285.PubMedCrossRefGoogle Scholar
  222. Xu, Y., & Lindquist, S. (1993). Heat-shock protein HSP 90 governs the activity of pp 60v-src kinase. Proceedings of the National Academy of Sciences of the United States of America, 90, 7074–7078.PubMedPubMedCentralCrossRefGoogle Scholar
  223. Yamashita, M., Yabu, T., & Ojima, N. (2010). Stress protein HSP70 in fish. Aqua Biology Sc Mono, 3, 111–141.Google Scholar
  224. Yokoyama, N., Hirata, M., Ohtsuka, K., Nishiyama, Y., Fujii, K., Fujita, M., et al. (2000). Co-expression of human chaperone HSP70 and Hsdj or HSP40 co-factor increases solubility of overexpressed target proteins in insect cells. Biochimica et Biophysica Acta, 1493, 119–124.PubMedCrossRefGoogle Scholar
  225. Young, J. C., Moarefi, I., & Hartl, F. U. (2001). HSP90: A specialized but essential protein-folding tool. The Journal of Cell Biology, 154, 267–273.PubMedPubMedCentralCrossRefGoogle Scholar
  226. Zhang, X. Y., Zhang, M. Z., Zheng, C. J., Liu, J., & Hu, H. J. (2009). Identification of two HSP90 genes from the marine crab, Portunus trituberculatus and their specific expression profiles under different environmental conditions. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 150, 465–473.Google Scholar
  227. Zhang, Z., & Zhang, Q. (2012). Molecular cloning, characterization and expression of heat shock protein 70 gene from the oyster Crassostrea hongkongensis responding to thermal stress and exposure of Cu and malachite green. Gene, 497, 172–180.PubMedCrossRefGoogle Scholar
  228. Zuo, D., Subjeck, J., & Wang, X. Y. (2016). Unfolding the role of large heat shock proteins: New insights and therapeutic implications. Frontiers in Immunology, 7, 75.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia
  2. 2.Laboratory of Aquatic BiomedicineCollege of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National UniversitySeoulSouth Korea

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