Heat shock protein expression in fish

Reviews in Fish Biology and Fisheries - Tập 8 Số 1 - Trang 35-56 - 1998
Iwama, George K.1, Thomas, Philip T.1, Forsyth, Robert B.1, Vijayan, Mathilakath M.1
1Department of Animal Science, and the Canadian Bacterial Diseases Network, University of British Columbia, Vancouver, Canada

Tóm tắt

Heat shock proteins (HSP) are a family of proteins expressed in response to a wide range of biotic and abiotic stressors. They are thus also referred to as stress proteins. Their extraordinarily high degree of identity at the amino acid sequence level and the fact that this cellular stress response has been described in nearly all organisms studied, make this group of proteins unique. We provide a brief historical overview of HSP research, as a background to summarizing what is known about HSP expression in fish. The expression of HSPs in fish has been described in cell lines, primary cultures of various cells, and in the tissues of whole organisms. Collectively, the data show that the expression of HSPs are affected in a wide variety of fish cells and tissues, in response both to biological stressors such as infectious pathogens, as well as to abiotic stressors such as heat and cold shock, and environmental contaminants. HSP research in fish is in its early stages and many studies are describing the expression of proteins in response to various stressors. Several studies have contributed to our understanding of the molecular nature and the molecular biology of HSPs in fish. Recent studies have shown a relationship between HSP expression and the generalized stress response in fish, but further research is needed to clarify the complex relationships between stress hormones and the cellular HSP response. In general, the HSP response seems to be related to the sensing of the stressor and the subsequent cellular effects which may adapt the cells to cope with the stressors. Consequently, such data may be of central importance in understanding the significance of HSP expression to the whole organism. We conclude with sections on laboratory methods used in HSP research and on potential applications of this knowledge in biomonitoring.

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citation_journal_title=Genes Dev.; citation_title=Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures; citation_author=K. Abravaya, B. Philips, R.I. Morimoto; citation_volume=5; citation_publication_date=1991; citation_pages=2117-2127; citation_id=CR1

citation_journal_title=Jap. J. Gen.; citation_title=Cloning and characterization of cDNAs for 70-kDa heat-shock proteins Hsp70 from two fish species of the genus Oryzias ; citation_author=A. Arai, K. Naruse, H. Mitani, A. Shima; citation_volume=70; citation_publication_date=1995; citation_pages=423-433; citation_id=CR2

citation_journal_title=Chromosoma; citation_title=Pattern of puffing activity in the salivary gland chromosomes of Drosophila. V. Response to environmental treatments; citation_author=M. Ashburner; citation_volume=31; citation_publication_date=1970; citation_pages=356-376; citation_id=CR3

citation_journal_title=J. Cell Biol.; citation_title=Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp 70 as a potential autoregulatory factor; citation_author=R. Baler, W.J. Welch, R. Voelling; citation_volume=117; citation_publication_date=1992; citation_pages=1151-1159; citation_id=CR4

citation_journal_title=Mol. Cell. Biol.; citation_title=Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1; citation_author=R. Baler, G. Dahl, R. Voellmy; citation_volume=13; citation_publication_date=1993; citation_pages=2486-2496; citation_id=CR5

citation_journal_title=Dev. Genet.; citation_title=Heat shock induced proteins in plant cells; citation_author=T. Barnett, M. Altschuler, C.N. McDaniel, J.P. Mascarenhas; citation_volume=1; citation_publication_date=1980; citation_pages=331-340; citation_id=CR6

citation_journal_title=Ann. Rev. Fish Diseases; citation_title=Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids; citation_author=B.A. Barton, G.K. Iwama; citation_volume=1; citation_publication_date=1991; citation_pages=3-26; citation_id=CR7

citation_title=Heat-shock induced protein modifications and modulation of enzyme activities; citation_inbook_title=Stress-Inducible Cellular Responses; citation_publication_date=1996; citation_pages=199-219; citation_id=CR8; citation_author=O. Bensaude; citation_author=S. Bellier; citation_author=M.F. Dubois; citation_author=F. Giannoni; citation_author=V.T. Nguyen; citation_publisher=Birkhäuser

citation_journal_title=Chromosoma; citation_title=Experimental puffs in salivary gland chromosomes of Drosophila hydei ; citation_author=H.D. Berendes, F.M.A. van Breugel, T.K.H. Holt; citation_volume=16; citation_publication_date=1965; citation_pages=35-46; citation_id=CR9

citation_journal_title=Mol. Brain Res.; citation_title=In vivo hyperthermia induces expression of HSP70 mRNA in brain regions controlling the neuroendocrine response to stress; citation_author=M.J. Blake, T.S. Nowak, N.J. Holbrook; citation_volume=8; citation_publication_date=1990; citation_pages=89-92; citation_id=CR10

citation_journal_title=Proc. Natn Acad. Sci. USA; citation_title=Stress-induced HSP70 expression in adrenal cortex: a glucocorticoid-sensitive, age-dependent response; citation_author=M.J. Blake, R. Udelsman, G.J. Feulner, D.D. Norton, N.J. Holbrook; citation_volume=88; citation_publication_date=1991; citation_pages=9873-9877; citation_id=CR11

citation_title=Modulation of steroid receptor signal transduction by heat shock proteins; citation_inbook_title=The Biology of Heat Shock Proteins and Molecular Chaperones; citation_publication_date=1994; citation_pages=313-334; citation_id=CR12; citation_author=S.P. Bohen; citation_author=K.R. Yamamoto; citation_publisher=Cold Spring Harbor Laboratory Press

citation_journal_title=Proc. Natn Acad. Sci. USA; citation_title=Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis ; citation_author=T.C.G. Bosch, S.M. Krylow, H.R. Bode, R.E. Steele; citation_volume=85; citation_publication_date=1988; citation_pages=7927-7931; citation_id=CR13

citation_title=Stress proteins: their detection and uses in biomonitoring; citation_inbook_title=Aquatic Toxicology and Risk Assessment: Thirteenth volume, ASTM STP 1096; citation_publication_date=1990; citation_pages=338-347; citation_id=CR14; citation_author=B.P. Bradley; citation_publisher=American Society for Testing and Materials

citation_journal_title=Microb. Path.; citation_title=Antibodies against Haemophilus ducreyi heat shock proteins; citation_author=T.J. Brown, J. Jardine, C.A. Isan; citation_volume=15; citation_publication_date=1992; citation_pages=131-139; citation_id=CR15

citation_journal_title=Cancer Res.; citation_title=Oxidative injury rapidly activates the heat shock transcription factor but fails to increase levels of heat shock proteins; citation_author=J.L. Bruce, B.D. Price, C.N. Coleman, S.K. Calderwood; citation_volume=53; citation_publication_date=1993; citation_pages=12-51; citation_id=CR16

citation_journal_title=Exp. Cell Res.; citation_title=Inducibility of heat shock polypeptides in cells containing hyperacetylated histones; citation_author=E.A. Burgess, R.K. Kotharg, E.P.M. Candido; citation_volume=155; citation_publication_date=1984; citation_pages=273-277; citation_id=CR17

citation_journal_title=J. Cell Physiol; citation_title=Activation of phospholipase C by heat shock requires GTP analogs and is resistant to pertussis toxin; citation_author=S.K. Calderwood, M.A. Stevenson, B.D. Price; citation_volume=156; citation_publication_date=1993; citation_pages=153-159; citation_id=CR18

citation_journal_title=Biochem. Biophys. Res. Comm.; citation_title=Rapid expression of novel proteins in goldfish retina following optic nerve crush; citation_author=K.A. Cauley, T.G. Sherman; citation_volume=138; citation_publication_date=1986; citation_pages=1177-1183; citation_id=CR19

citation_journal_title=Anal. Biochem.; citation_title=Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate; citation_author=J.P. Chamberlain; citation_volume=98; citation_publication_date=1979; citation_pages=132-135; citation_id=CR20

citation_journal_title=J. Cell. Physiol.; citation_title=Thermal adaptation and heat shock response of Tilapia ovary cells; citation_author=J.D. Chen, F.H. Yew, G.C. Li; citation_volume=134; citation_publication_date=1988; citation_pages=189-199; citation_id=CR21

citation_journal_title=Biochem. Biophys. Res. Comm.; citation_title=A novel 90-kDa stress protein induced in fish cells by fish rhabdovirus infection; citation_author=W. Cho, S. Cha, J. Do, J. Choi, J. Lee, C. Jeong, K. Cho, W. Choi, H. Kang, H. Kim, J. Park; citation_volume=233; citation_publication_date=1997; citation_pages=316-319; citation_id=CR22

citation_journal_title=J. Biol. Chem.; citation_title=Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation; citation_author=J.J. Cotto, M. Kline, R.I. Morimoto; citation_volume=271; citation_publication_date=1996; citation_pages=3355-3358; citation_id=CR23

citation_journal_title=Cell; citation_title=Sequence organization of two recombinant plasmids containing genes for the major heat shock induced protein of Drosophila melanogaster ; citation_author=E.A. Craig, B.J. McCarthy, S.C. Wadsworth; citation_volume=16; citation_publication_date=1979; citation_pages=575-583; citation_id=CR24

citation_journal_title=J. Exp. Biol.; citation_title=Synthesis of stress protein 70 (Hsp 70) in rainbow trout (Oncorhynchus mykiss) red blood cells; citation_author=S. Currie, B.L. Tufts; citation_volume=200; citation_publication_date=1997; citation_pages=607-614; citation_id=CR25

citation_journal_title=Proc. Natn Acad. Sci. USA; citation_title=The threshold induction temperature of the 90 kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys); citation_author=T.J. Dietz, G.N. Somero; citation_volume=89; citation_publication_date=1992; citation_pages=3389-3393; citation_id=CR26

citation_journal_title=Physiol. Zool.; citation_title=Species-and tissue-specific synthesis patterns for heat-shock proteins HSP 70 and HSP 90 in several marine teleost fishes; citation_author=T.J. Dietz, G.N. Somero; citation_volume=66; citation_publication_date=1993; citation_pages=863-880; citation_id=CR27

citation_journal_title=Can. J. Zool.; citation_title=Tissue-specific patterns of synthesis of heat-shock proteins and thermal tolerance of the fathead minnow (Pimephales promelas); citation_author=S.D. Dyer, K.L. Dickson, E.G. Zimmerman; citation_volume=69; citation_publication_date=1991; citation_pages=2021-2027; citation_id=CR28

citation_journal_title=J. Aquat. Animal Health; citation_title=Stress protein expression in coho salmon with bacterial kidney disease; citation_author=R.B. Forsyth, E.P.M. Candido, S.L. Babich, G.K. Iwama; citation_volume=9; citation_publication_date=1997; citation_pages=18-25; citation_id=CR29

citation_journal_title=Rev. Fish Biol. Fish.; citation_title=Experimental control of stress hormone levels in fishes: techniques and applications; citation_author=A.K. Gamperl, M.M. Vijayan, R.G. Boutilier; citation_volume=4; citation_publication_date=1994; citation_pages=215-255; citation_id=CR30

citation_journal_title=Biosci. Rep.; citation_title=Analysis of the temperature-dependent temporal pattern of heat-shock protein synthesis in fish cells; citation_author=L. Gedamu, B. Culham, J.J. Heikkila; citation_volume=3; citation_publication_date=1983; citation_pages=647-658; citation_id=CR31

citation_journal_title=J. Mol. Evol.; citation_title=Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes; citation_author=R.S. Gupta, G.B. Golding; citation_volume=37; citation_publication_date=1993; citation_pages=573-582; citation_id=CR32

citation_journal_title=J. Biol. Chem.; citation_title=Expression of a set of fish genes following heat or metal ion exposure; citation_author=J.J. Heikkila, G.A. Schultz, K. Iatrou, L. Gedamu; citation_volume=257; citation_publication_date=1982; citation_pages=12000-12005; citation_id=CR33

citation_journal_title=J. Biol. Chem.; citation_title=Thiol reducing reagents inhibit the heat shock response; citation_author=L.E. Huang, H. Zhang, S.W. Bae, A.Y.C. Liu; citation_volume=269; citation_publication_date=1994; citation_pages=30718-30725; citation_id=CR34

Janz, D.M., McMaster, M.E., Munkittrick, K.R. and Van der Kraak, G. (1997) Elevated ovarian follicular apoptosis and heat shock protein-70 expression in white sucker exposed to bleached kraft pulp mill effluent. Toxicol. Appl. Pharmacol. (in press)

citation_journal_title=J. Biol. Chem.; citation_title=Dogfish-crystallin sequences: comparison with small heat shock proteins and Schistosoma egg antigen; citation_author=W.W. de Jong, J.A.M. Leunissen, P.J.M. Leenen, A. Zweers, M. Versteeg; citation_volume=263; citation_publication_date=1988; citation_pages=5141-5149; citation_id=CR36

citation_journal_title=Science; citation_title=Effect of sodium salicylate on the human heat shock response; citation_author=D.A. Jurvich, L. Sistonen, R.A. Kroes, R.I. Morimoto; citation_volume=255; citation_publication_date=1992; citation_pages=1243-1245; citation_id=CR37

citation_journal_title=Cell; citation_title=The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts; citation_author=P.M. Kelly, M.J. Schlesinger; citation_volume=15; citation_publication_date=1978; citation_pages=1277-1286; citation_id=CR38

citation_journal_title=Am. J. Physiol.; citation_title=Effect of heat shock, (Ca2+)i, and cAMP on inositol tris-phosphate in human epidermoid A-431 cells; citation_author=J.G. Kiang, D.E. McClain; citation_volume=264; citation_publication_date=1993; citation_pages=C1561-C1569; citation_id=CR39

citation_journal_title=J. Comp. Physiol.; citation_title=The 65-kDa cytosolic protein associated with warm temperature acclimation in goldfish, Carassius auratus ; citation_author=K. Kikuchi, S. Watabe, Y. Suzuki, K. Aida, H. Nakajima; citation_volume=163B; citation_publication_date=1993; citation_pages=349-354; citation_id=CR40

citation_journal_title=Physiol. Zool.; citation_title=Induction of heat-shock protein synthesis in teleost hepatocytes: effects of acclimation temperature; citation_author=M. Koban, G. Graham, C.L. Prosser; citation_volume=60; citation_publication_date=1987; citation_pages=290-296; citation_id=CR41

citation_journal_title=Mol. Mar. Biol. Biotech.; citation_title=Molecular adaptation to environmental temperature: heat-shock response of the eurythermal teleost Fundulus heteroclitus ; citation_author=M. Koban, A.A. Yup, L.B. Agellon, D.A. Powers; citation_volume=1; citation_publication_date=1991; citation_pages=1-17; citation_id=CR42

citation_journal_title=Can. J. Biochem.; citation_title=Induction of a novel set of polypeptides by heat shock or sodium arsenite in cultured cells of rainbow trout, Salmo gairdneri ; citation_author=R.K. Kothary, E.P.M. Candido; citation_volume=60; citation_publication_date=1982; citation_pages=347-355; citation_id=CR43

citation_journal_title=Biochim. Biophys. Acta; citation_title=The heat-shock phenomenon in cultured cells of rainbow trout: hsp 70 mRNA synthesis and turnover; citation_author=R.K. Kothary, E.A. Burgess, E.P.M. Candido; citation_volume=783; citation_publication_date=1984; citation_pages=137-143; citation_id=CR44

citation_journal_title=Mol. Cell. Biol.; citation_title=70-Kilodalton heat shock polypeptides from rainbow trout: characterization of cDNA sequences; citation_author=R.K. Kothary, D. Jones, E.P.M. Candido; citation_volume=4; citation_publication_date=1984; citation_pages=1785-1791; citation_id=CR45

citation_journal_title=Eur. J. Biochem.; citation_title=Quantitative film detection of 3H and 14C in polyacrylamide gels by fluography; citation_author=R.A. Laskey, A.D. Mills; citation_volume=56; citation_publication_date=1975; citation_pages=335-341; citation_id=CR46

citation_journal_title=Cell; citation_title=Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts; citation_author=P.G. Lemeux, S.L. Herendeen, P.L. Bloch, F.C. Neidhardt; citation_volume=13; citation_publication_date=1978; citation_pages=427-434; citation_id=CR47

citation_journal_title=Proc. Natn Acad. Sci. USA; citation_title=Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster ; citation_author=S.L. Lindquist-McKenzie, S. Henikoff, M. Meselson; citation_volume=75; citation_publication_date=1975; citation_pages=1117-1121; citation_id=CR48

citation_journal_title=Comp. Biochem. Physiol.; citation_title=Indentification and characterization of a heat shock protein 70 family member in channel catfish (Ictalurus punctatus); citation_author=J.C. Luft, M.R. Wilson, J.E. Bly, N.W. Miller, L.W. Clem; citation_volume=113B; citation_publication_date=1996; citation_pages=169-174; citation_id=CR49

citation_journal_title=Biochem. Biophys. Res. Commun.; citation_title=Heat shock proteins and thermal resistance in yeast; citation_author=L. McAlister, D.B. Finkelstein; citation_volume=93; citation_publication_date=1980; citation_pages=819-824; citation_id=CR50

citation_journal_title=J. Endocrinol.; citation_title=Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha); citation_author=A.G. Maule, R.A. Tripp, S.L. Kattari, C.B. Schreck; citation_volume=120; citation_publication_date=1989; citation_pages=135-142; citation_id=CR51

citation_journal_title=Trans. Am. Fish. Soc.; citation_title=Primary and secondary effects of stress in fish: some new data with a general review; citation_author=M.M. Mazeaud, F. Mazeaud, E.M. Donaldson; citation_volume=106; citation_publication_date=1977; citation_pages=201-212; citation_id=CR52

Mazur, C.F. (1996) The heat shock protein response and physiological stress in aquatic organisms. Doctoral thesis, Univ. British Columbia. 175 pp.

citation_journal_title=J. Therm. Biol.; citation_title=Two types of heat tolerance in FHM-cells: induction by heat-shock versus elevated culturing temperature; citation_author=R. Merz, H. Laudien; citation_volume=12; citation_publication_date=1987; citation_pages=281-288; citation_id=CR54

citation_journal_title=Cold Spring Harbor Symp. Quant. Biol.; citation_title=The effect of heat shock on gene expression in Drosophila melanogaster ; citation_author=M.E. Mirault, M. Goldschmidt-Clermont, L. Moran, A.P. Arrigo, A. Tissieres; citation_volume=42; citation_publication_date=1978; citation_pages=819-827; citation_id=CR55

citation_journal_title=Biochim. Biophys. Acta; citation_title=Analysis of stress-induced gene expression in fish cell lines exposed to heavy metals and heat shock; citation_author=S. Misra, M. Zafarullah, J. Price-Haughey, L. Gedamu; citation_volume=1007; citation_publication_date=1989; citation_pages=325-333; citation_id=CR56

citation_journal_title=J. Cell Sci.; citation_title=Eurythermic and stenothermic growth of cultured fish cells and their thermosensitivity; citation_author=H. Mitani, K. Naruse, A. Shima; citation_volume=93; citation_publication_date=1989; citation_pages=731-737; citation_id=CR57

citation_journal_title=Dev. Gen.; citation_title=Developmental abnormalities in Drosophila induced by heat shock; citation_author=H.K. Mitchell, N.S. Peterson; citation_volume=3; citation_publication_date=1982; citation_pages=91-102; citation_id=CR58

citation_journal_title=J. Mol. Biol.; citation_title=Protein synthesis in salivary-glands of Drosophila melanogaster — relation to chromosome puffs; citation_author=H.K. Mitchell, A. Tissieres, U.M. Tracy; citation_volume=84; citation_publication_date=1974; citation_pages=389-398; citation_id=CR59

citation_title=The Biology of Heat Shock Proteins and Molecular Chaperones; citation_publication_date=1994; citation_id=CR60; citation_author=R.I. Morimoto; citation_author=A. Tissieres; citation_author=C. Georgopoulos; citation_publisher=Cold Spring Harbor Laboratory Press

citation_title=The transcriptional regulation of heat shock genes: a plethora of heat shock factors and regulatory conditions; citation_inbook_title=Stress-Inducible Cellular Responses; citation_publication_date=1996; citation_pages=139-164; citation_id=CR61; citation_author=R.I. Morimoto; citation_author=P.E. Kroeger; citation_author=J.J. Cotto; citation_publisher=Birkhäuser

citation_journal_title=J. Comp. Physiol.; citation_title=Relationship between heat-shock protein synthesis and thermotolerance in rainbow trout fibroblasts; citation_author=D.D. Mosser, N.C. Bols; citation_volume=158B; citation_publication_date=1988; citation_pages=457-467; citation_id=CR62

citation_journal_title=J. Cell Physiol.; citation_title=Temperature ranges over which rainbow trout fibroblasts survive and synthesize heat-shock proteins; citation_author=D.D. Mosser, J.J. Heikkila, N.C. Bols; citation_volume=128; citation_publication_date=1986; citation_pages=432-440; citation_id=CR63

citation_journal_title=J. Cell Physiol.; citation_title=Development and decay of thermotolerance by rainbow trout fibroblasts; citation_author=D.D. Mosser, J. van Oostrom, N.C. Bols; citation_volume=132; citation_publication_date=1987; citation_pages=155-160; citation_id=CR64

citation_journal_title=Mol. Biol. Evol.; citation_title=Variation in heat shock proteins within tropical and desert species of Poeciliid fishes; citation_author=C.E. Norris, P.J. DiIorio, R.J. Schultz, L.E. Hightower; citation_volume=12; citation_publication_date=1995; citation_pages=1048-1062; citation_id=CR65

citation_journal_title=Comp. Biochem. Physiol.; citation_title=Synthesis of heat shock proteins in the isolated fin of the medaka, Oryzias latipes, acclimated to various temperatures; citation_author=S. Oda, H. Mitani, K. Naruse, A. Shima; citation_volume=98B; citation_publication_date=1991; citation_pages=587-591; citation_id=CR66

citation_journal_title=Science; citation_title=Regulation of heat shock factor trimerization: role of a conserved leucine zipper; citation_author=S.K. Rabindran, R.I. Haroun, J. Clos, J. Wisniewski, C. Wu; citation_volume=259; citation_publication_date=1993; citation_pages=230-234; citation_id=CR67

citation_journal_title=Proc. Natl Acad. Sci. USA; citation_title=Molecular cloning and expression of a human heat shock factor, HSF1; citation_author=S.K. Rabindran, G. Giorgi, J. Clos, J. Wisniewshki, C. Wu; citation_volume=88; citation_publication_date=1997; citation_pages=6906-6910; citation_id=CR68

citation_journal_title=Mol. Cell Biol.; citation_title=Interaction between heat shock factor and hsp 70 is insufficient to suppress induction of DNA-binding activity in-vivo ; citation_author=S.K. Rabindran, J. Wisniewski, L. Li, G.C. Li, C. Wu; citation_volume=14; citation_publication_date=1994; citation_pages=6557-6561; citation_id=CR69

citation_title=Catecholamine; citation_inbook_title=Fish Physiology; citation_publication_date=1992; citation_pages=255-300; citation_id=CR70; citation_author=D.J. Randall; citation_author=S.F. Perry; citation_publisher=Academic Press

citation_journal_title=J. Comp. Physiol.; citation_title=Modulation of catecholamine storage and release by the pituitary-interrenal axis in the rainbow trout (Oncorhynchus mykiss); citation_author=S.G. Reid, M.M. Vijayan, S.F. Perry; citation_volume=165B; citation_publication_date=1996; citation_pages=665-676; citation_id=CR71

citation_journal_title=J. Pharmacol. Exp. Therap.; citation_title=Relationship of thermal and chemical tolerance to transepithelial transport by cultured flounder renal epithelium; citation_author=J.L. Renfro, M.A. Brown, S.L. Parker, L.E. Hightower; citation_volume=265; citation_publication_date=1993; citation_pages=992-1000; citation_id=CR72

citation_journal_title=Experientia; citation_title=A new puffing pattern induced by a temperature shock and DNP in Drosophila ; citation_author=F.M. Ritossa; citation_volume=18; citation_publication_date=1962; citation_pages=571-573; citation_id=CR73

citation_title=Stress proteins: potential as multitired biomarkers; citation_inbook_title=Biomarkers of Environmental Contamination; citation_publication_date=1990; citation_pages=165-191; citation_id=CR74; citation_author=B.M. Sanders; citation_publisher=Lewis Publishers

citation_journal_title=Crit. Rev. Toxicol.; citation_title=Stress proteins in aquatic organisms: an environmental perspective; citation_author=B.M. Sanders; citation_volume=23; citation_publication_date=1993; citation_pages=49-75; citation_id=CR75

citation_journal_title=Sci. Total Environ.; citation_title=Stress proteins as biomarkers of contaminant exposure in archived environmental samples; citation_author=B.M. Sanders, L.S. Martin; citation_volume=139/140; citation_publication_date=1993; citation_pages=459-470; citation_id=CR76

citation_journal_title=Mol. Cell. Biol.; citation_title=Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress; citation_author=K.D. Sarge, S.P. Murphy, R.I. Morimoto; citation_volume=13; citation_publication_date=1993; citation_pages=1392-1407; citation_id=CR77

citation_journal_title=J. Mol. Biol.; citation_title=Messenger RNA in heat shocked Drosophila cells; citation_author=A. Spradling, M.L. Pardue, S. Penman; citation_volume=109; citation_publication_date=1977; citation_pages=559-587; citation_id=CR78

citation_journal_title=Br. J. Radiol.; citation_title=Heat shock proteins and thermotolerance; a comparison of induction kinetics; citation_author=J.R. Subjeck, J.J. Sciandra, R.J. Johnson; citation_volume=55; citation_publication_date=1982; citation_pages=579-584; citation_id=CR79

citation_journal_title=Am. J. Physiol.; citation_title=Heat-shock-stimulated transepithelial daunomycin secretion by flounder renal proximal tubule primary cultures; citation_author=C. Sussman-Turner, J.L. Renfro; citation_volume=267; citation_issue=36; citation_publication_date=1995; citation_pages=F135-F144; citation_id=CR80

citation_journal_title=J. Mol. Biol.; citation_title=Protein synthesis in salivary glands of Drosophila melanogaster. Relation to chromosome puffs; citation_author=A. Tissieres, H.K. Mitchell, V.M. Tracy; citation_volume=84; citation_publication_date=1974; citation_pages=389-398; citation_id=CR81

citation_journal_title=J. Clin. Invest.; citation_title=Vascular heat shock protein expression in response to stress; citation_author=R. Udelsman, M.J. Blake, C.A. Stagg, D. Li, D.J. Putney, N. Holbrook; citation_volume=91; citation_publication_date=1993; citation_pages=465-473; citation_id=CR82

citation_journal_title=Surgery; citation_title=Adrenergic regulation of adrenal and aortic heat shock protein; citation_author=R. Udelsman, D. Li, C.A. Stagg, C.B. Gordon, R. Kvetnasky; citation_volume=116; citation_publication_date=1994; citation_pages=177-182; citation_id=CR83

citation_journal_title=Surgery; citation_title=Endocrine control of stress-induced heat shock protein 70 in vivo; citation_author=R. Udelsman, M.J. Blake, C.A. Stagg, N. Holbrook; citation_volume=115; citation_publication_date=1994; citation_pages=611-616; citation_id=CR84

citation_journal_title=Gen. Comp. Endocrinol.; citation_title=The effects of cortisol on hepatocyte metabolism in rainbow trout: a study using the steroid analogue RU486; citation_author=M.M. Vijayan, P.K. Reddy, J.F. Leatherland, T.W. Moon; citation_volume=96; citation_publication_date=1994; citation_pages=75-84; citation_id=CR85

citation_journal_title=J. Exp. Biol.; citation_title=Metabolic effects of cortisol treatment in a marine teleost, the sea raven; citation_author=M.M. Vijayan, T.P. Mommsen, H.C. Glemet, T.W. Moon; citation_volume=199; citation_publication_date=1996; citation_pages=1509-1514; citation_id=CR86

citation_journal_title=Life Sci.; citation_title=Handling stress does not affect the expression of hepatic heat shock protein 70 and conjugation enzymes in rainbow trout treated with β-naphthoflavone; citation_author=M.M. Vijayan, C. Pereira, R.B. Forsyth, C.J. Kennedy, G.K. Iwama; citation_volume=61; citation_publication_date=1997; citation_pages=117-127; citation_id=CR87

citation_journal_title=Comp. Biochem. Physiol.; citation_title=Metabolic responses associated with confinement stress in tilapia: the role of cortisol; citation_author=M.M. Vijayan, C. Pereira, E.G. Grau, G.K. Iwama; citation_volume=116C; citation_publication_date=1997; citation_pages=89-95; citation_id=CR88

Vijayan, M.M., Pereira, C., Kruzynski, G. and Iwama, G.K. (1997c) Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquat. Toxicol. (in press)

citation_title=Sensing stress and responding to stress; citation_inbook_title=Stress-Inducible Cellular Responses; citation_publication_date=1996; citation_pages=121-138; citation_id=CR90; citation_author=R. Voellmy; citation_publisher=Birkhäuser

citation_journal_title=J. Cell Sci.; citation_title=Characterization of a heat-resistant strain of Tilapia ovary cells; citation_author=H.C. Wang, J.D. Chen, G.C. Li, F.H. Yew; citation_volume=92; citation_publication_date=1989; citation_pages=353-359; citation_id=CR91

citation_title=Stress and acclimation; citation_inbook_title=Methods for Fish Biology; citation_publication_date=1990; citation_pages=451-489; citation_id=CR92; citation_author=G.A. Wedemeyer; citation_author=B.A. Barton; citation_author=D.J. McLeay; citation_publisher=American Fisheries Society

citation_journal_title=Scient. Am.; citation_title=How cells respond to stress; citation_author=W.J. Welch; citation_volume=268; citation_publication_date=1993; citation_pages=56-64; citation_id=CR93

citation_journal_title=Curr. Top. Microbiol. Immunol.; citation_title=Response of mammalian cells to metabolic stress; changes in cell physiology and structure/function of stress proteins; citation_author=W.J. Welch, H.S. Kang, R.P. Beckmann, L.A. Mizzen; citation_volume=167; citation_publication_date=1991; citation_pages=31-55; citation_id=CR94

citation_journal_title=Physiol. Rev.; citation_title=The stress response in fish; citation_author=S.E. Wendelaar Bonga; citation_volume=77; citation_publication_date=1997; citation_pages=591-625; citation_id=CR95

citation_journal_title=Nature; citation_title=Stress-induced oligomerization and chromosomal relocalization of heat-shock factor; citation_author=J.T. Westwood, J. Clos, C. Wu; citation_volume=253; citation_publication_date=1991; citation_pages=822-827; citation_id=CR96

citation_journal_title=Mol. Biol. Evol.; citation_title=Variation in heat-shock proteins among species of desert fishes (Poeciliidae, Poeciliopsis); citation_author=C.N. White, L.E. Hightower, R.J. Schultz; citation_volume=11; citation_publication_date=1994; citation_pages=106-119; citation_id=CR97

citation_journal_title=Env. Toxicol. Chem.; citation_title=Accumulation of hsp70 in juvenile and adult rainbow trout gill exposed to metal-contaminated water and/or diet; citation_author=J.H. Williams, A.M. Farag, M.A. Stansbury, P.A. Young, H.L. Bergman, N.S. Petersen; citation_volume=15; citation_publication_date=1996; citation_pages=1324-1328; citation_id=CR98

citation_journal_title=J. Bacteriol.; citation_title=Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature; citation_author=T. Yamamori, K. Ito, Y. Nakamura, T. Tura; citation_volume=134; citation_publication_date=1978; citation_pages=1133-1140; citation_id=CR99

citation_journal_title=Fed. Eur. Biochem. Soc. Letters; citation_title=Induction of proteins in response to cold acclimation of rainbow trout cells; citation_author=M. Yamashita, N. Ojima, T. Sakamoto; citation_volume=382; citation_publication_date=1996; citation_pages=261-264; citation_id=CR100

citation_journal_title=J. Thermal Biol.; citation_title=Monoclonal antibody ELISA test indicates that large amounts of constitutive HSP-70 are present in salamanders, turtle and fish; citation_author=Z. Yu, W.E. Magee, J.R. Spotila; citation_volume=19; citation_publication_date=1994; citation_pages=41-53; citation_id=CR101

citation_journal_title=Eur. J. Biochem.; citation_title=Molecular cloning and characterization of a constitutively expressed heat-shock cognate hsc 71 gene from rainbow trout; citation_author=M. Zafarullah, J. Wisniewski, N.W. Shworak, S. Schieman, S. Misra, L. Gedamu; citation_volume=204; citation_publication_date=1992; citation_pages=893-900; citation_id=CR102