HSP70 expression in blood cells in diploid and triploid rainbow trouts as short-term stress thermal and welfare statement model
DOI:
https://doi.org/10.33936/at.v4i1.4581Palabras clave:
Oncorhynchus mykiss, Aquaculture, Fish health, Heat stress, Heat shock proteinsResumen
In triploid fish physiology there is a lack of information about its molecular responses under stress and how to quantify the stress levels or intensity. Thus, the goals of this trial were to evaluate the pattern of HSP70 in the gills, heart and muscles of non-stressed diploid and triploid rainbow trouts, and in the blood cells after the exposure to heat stress in order to assess their stress levels. Similar HSP70 immunohistochemical detection in the gills, heart and muscles samples was seen in both ploidies. However, HSP70 expression in blood varied between ploidies over the experimental time. Control and stressed diploid trouts showed analogous HSP70 levels, but heat stressed triploid trouts showed lower HSP70 levels throughout the experiment with differences observable after 12h and 24h. It was expected higher HSP70 expression in both ploidies once this protein protects the cells against a wide range of disturbing agents. Recent evidences showed that triploid fishes have lower gene expression and this fact must be explored in future investigation in rainbow trouts. In conclusion, comparisons over time between diploid and triploid HSP70 levels in trouts could be used in stress evaluation and welfare statement.
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Adams C.J., Kopp M.C., Larburu N., Nowak P.R., Ali M.M. (2019). Structure and molecular mechanism of ER stress signaling by the unfolded protein response signal activator IRE1. Frontiers in Molecular Biosciences, 6: 11.
Akiyoshi H., Inoue A. (2004). Comparative histological study of teleost livers in relation to phylogeny. Zoological Science, 21: 841-850.
Arana S., Tabata Y.A., Sabino M., Rigolino M.G., Hernandez-Blazquez F.J. (2002). Differential effect of chronic aflatoxin B1 intoxication on the growth performance and incidence of hepatic lesions in triploid and diploid rainbow trout (Oncorhynchus mykiss). Archivos de Medicina Veterinaria, 34: 253-263.
Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., Iwama G.K. (2002). Heat shock protein genes and their functional significance in fish. Gene, 295: 173-183.
Benfey T.J., Sutterlin A.M. (1984). The haematology of triploid landlocked Atlantic salmon, Salmo solar L. Journal of Fish Biology, 24: 333-338.
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 - Part C, 132: 223-233.
Bradford M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Chatchaiphan S., Srisapoome P., Kim J.H., Devlin R.H., Na-Nakorn U. (2017). De novo transcriptome characterization and growth-related gene expression profiling of diploid and triploid bighead catfish (Clarias macrocephalus Günther, 1864). Marine Biotechnology, 19: 36-48.
Christensen K.A., Sakhrani D., Rondeau E.B., Richards J., Koop B.F., Devlin R.H. (2019). Effect of triploidy on liver gene expression in coho salmon (Oncorhynchus kisutch) under different metabolic states. BMC Genomics, 20: 1-14.
Clark M.S., Peck L.S. (2009). HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a mini-review. Marine Genomics, 1: 11-18.
Clarkson K., Kieffer J.D., Currie S. (2005). Exhaustive exercise and the cellular stress response in rainbow trout, Oncorhynchus mykiss. Comparative Biochemistry and Physiology - Part A, 140: 225-232.
Covelo‐Soto L., Leunda P.M., Pérez‐Figueroa A., Morán P. (2015). Genome‐wide methylation study of diploid and triploid brown trout (Salmo trutta L.). Animal Genetics, 46: 280-288.
Currie S., Tufts B. (1997). Synthesis of stress protein 70 (Hsp70) in rainbow trout (Oncorhynchus mykiss) red blood cells. Journal of Experimental Biology, 200: 607-614.
Currie S., Reddin K., McGinn P., McConnell T., Perry S.F. (2008). β-adrenergic stimulation enhances the heat-shock response in fish. Physiological and Biochemical Zoology, 81: 414-425.
DuBeau S.F., Pan F., Tremblay G.C., Bradley T.M. (1998). Thermal shock of salmon in vivo induces the heat shock protein hsp 70 and confers protection against osmotic shock. Aquaculture, 168: 311-323.
Dymowska A. K., Hwang P. P., Goss G. G. (2012). Structure and function of ionocytes in the freshwater fish gill. Respiratory Physiology & Neurobiology, 184: 282-292.
Evans D.H., Piermarini P.M., Choe K.P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85: 97-177.
Fazio F. (2019). Fish hematology analysis as an important tool of aquaculture: a review. Aquaculture, 500: 237-242.
Fulladosa E., Deane E., Ng A.H.Y., Woo N.Y.S., Murat J.C., Villaescusa I. (2006). Stress proteins induced by exposure to sublethal levels of heavy metals in sea bream (Sparus sarba) blood cells. Toxicology in vitro, 20: 96-100.
Goss G.G., Perry S.F., Fryer J.N., Laurent P. (1998). Gill morphology and acid-base regulation in freshwater fishes. Comparative Biochemistry and Physiology - Part A, 119: 107-115.
Ineno T., Tsuchida S., Kanda M., Watabe S. (2005). Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding. Fisheries Science, 71: 767-775.
Iwama G.K., Afonso L.O., Todgham A., Ackerman P., Nakano K. (2004). Are hsps suitable for indicating stressed states in fish?. Journal of Experimental Biology, 207: 15-19.
Kilemade M., Mothersill C. (2001). Heat shock protein 70 levels in rainbow trout primary epidermal cultures in response to 2, 4‐dichloroaniline exposure: A novel in vitro aquatic toxicity marker. Environmental Toxicology, 16: 253-259.
Köhler H.R., Bartussek C., Eckwert H., Farian K., Gränzer S., Knigge T., Kunz N. (2001). The hepatic stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution. Journal of Aquatic Ecosystem Stress and Recovery, 8: 261-279.
Leggatt R.A., Scheer K.W., Afonso L.O., Iwama G.K. (2006). Triploid and diploid rainbow trout do not differ in their stress response to transportation. North American Journal of Aquaculture, 68: 1-8.
Matos I.M., Coelho M.M., Schartl M. (2016). Gene copy silencing and DNA methylation in natural and artificially produced allopolyploid fish. Journal of Experimental Biology, 219: 3072-3081.
Matos I., Machado M.P., Schartl M., Coelho M.M. (2019). Allele-specific expression variation at different ploidy levels in Squalius alburnoides. Scientific Reports, 9: 1-12.
Ohtsuka K., Hata M. (2000). Molecular chaperone function of mammalian Hsp70 and Hsp40-a review. International Journal of Hyperthermia, 16: 231-245.
Otto S.P., Whitton J. (2000). Polyploid incidence and evolution. Annual Reviews of Genetics, 34: 401-437.
Pala I., Coelho M.M., Schartl M. (2008). Dosage compensation by gene-copy silencing in a triploid hybrid fish. Current Biology, 18: 1344-1348.
Peutz I.L.J.A., Oorschot R.W.A., Johnson G.R., Horney B.S., Boon J.H. (1996). The leucogram as an indicator off marine‐cultured rainbow trout, Oncorhynchus mykiss (Walbaum), health in The Netherlands. Aquaculture Research, 27: 437-445.
Pressinoti L.N. (2006). Efeito da triploidização na imunidade celular inespecífica de trutas arco-íris Oncorhynchus mykiss (Walbaum,1792). Master’s Thesis. University of São Paulo, Brazil.
Qiu X.B., Shao Y.M., Miao S., Wang L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cellular and Molecular Life Sciences, 63: 2560-2570.
Rolim G.S., Aparecido L.E.O. (2016). Camargo, Köppen and Thornthwaite climate classification systems in defining climatical regions of the state of São Paulo, Brazil. International Journal of Climatology, 36: 636-643.
Ross L.G., Ross B. (2008). Anaesthetic and sedative techniques for aquatic animals. Blackwell Science. Oxford, United Kingdom.
Roy S., Kumar V., Kumar V., Behera B.K. (2017). Acute phase proteins and their potential role as an indicator for fish health and in diagnosis of fish diseases. Protein & Peptides Letters, 24: 78-89.
Schreck C.B., Tort L. (2016). The concept of stress in fish. In: Schreck C.B., Tort L., Farrell A.P., Brauner C.J.(Eds). Fish Physiology. Elsevier Inc., USA. vol. 35, pp. 1-34.
Scofield E., Bowyer R.T., Duffy L.K. (1999). Baseline levels of Hsp 70, a stress protein and biomarker, in halibut from the Cook Inlet region of Alaska. Science of the Total Environment, 226: 85-88.
Segner H., Sundh H., Buchmann K., Douxfils J., Sundell K.S., Mathieu C., Ruane N., Jutfelt F., Toften H., Vaughan L. (2012). Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiology and Biochemistry, 38: 85-105.
Silva J.R.M.C., Hernandez-Blazquez F.J., Barbieri R.L. (1998). Induced inflammatory process in the Antarctic fish Notothenia neglecta. Polar Biology, 20: 206-212.
Stitt B.C., Burness G., Burgomaster K.A., Currie S., McDermid J.L., Wilson C.C. (2014). Intraspecific variation in thermal tolerance and acclimation capacity in brook trout (Salvelinus fontinalis): physiological implications for climate change. Physiological and Biochemical Zoology, 87: 15-29.
Strzyzewska E., Szarek J., Babinska I. (2016). Morphologic evaluation of the gills as a tool in the diagnostics of pathological conditions in fish and pollution in the aquatic environment: a review. Veterinárni Medicína, (Praha). 61: 123-132.
Sugito K., Yamane M., Hattori H., Hayashi Y., Tohnai I., Ueda M., Tsuchida N., Ohtsuka K. (1995). Interaction between hsp70 and hsp40, eukaryotic homologues of DnaK and DnaJ, in human cells expressing mutant‐type p53. FEBS Letters, 358: 161-164.
Thorgaard G.H., Arbogast D.N., Hendricks J.D., Pereira C.B., Bailey G.S. (1999). Tumor suppression in triploid trout. Aquatic Toxicology, 46: 121-126.
Triebskorn R., Köhler H.R., Honnen W., Schramm M., Adams S.M., Müller E.F. (1997). Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behavior: are these biomarkers related and are they useful to reflect the state of pollution in the field?. Journal of Aquatic Ecosystem Stress and Recovery, 6: 57-73.
Verhille C., Anttila K., Farrell A.P. (2013). A heart to heart on temperature: impaired temperature tolerance of triploid rainbow trout (Oncorhynchus mykiss) due to early onset of cardiac arrhythmia. Comparative Biochemistry and Physiology - Part A., 164: 653-657.
Vijayan M.M., Pereira C., Kruzynski G., Iwama G.K. (1998). Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquatic Toxicology, 40: 101-108.
Virtanen E., Forsman L., Sundby A. (1990). Triploidy decreases the aerobic swimming capacity of rainbow trout (Salmo gairdneri). Comparative Biochemistry and Physiology - Part A, 96: 117-121.
Wang Y., Xu J., Sheng L., Zheng Y. (2007a). Field and laboratory investigations of the thermal influence on tissue-specific Hsp70 levels in common carp (Cyprinus carpio). Comparative Biochemistry and Physiology - Part A, 148: 821-827.
Wang J., Wei Y., Li X., Cao H., Xu M., Dai J. (2007b). 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.
Washburn B.S., Moreland J.J., Slaughter A.M., Werner I., Hinton D.E., Sanders B.M. (2002). Effects of handling on heat shock protein expression in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry, 21: 557-560.
Wendelaar Bonga S.E. (1997). The stress response in fish. Physiological Reviews, 77: 591-625.
Wilson J.M., Laurent P. (2002). Fish gill morphology: inside out. Journal of Experimental Zoology, 293: 192-213.
Wolf J.C., Wheeler J.R. (2018). A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquatic Toxicology, 197: 60-78.
Wu J., Liu T., Rios Z., Mei Q., Lin X., Cao S. (2017). Heat shock proteins and cancer. Trends in Pharmacological Sciences, 38: 226-256.
Yamamoto A., Iida T. (1994). Hematological characteristics of triploid rainbow trout. Fish Pathology, 29: 239-243.
Yamamoto A., Iida T. (1995). Non-specific defense activities of triploid rainbow trout. Fish Pathology, 30: 107-110.
Zarate J., Bradley T.M. (2003). Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture, 223: 175-187.
Akiyoshi H., Inoue A. (2004). Comparative histological study of teleost livers in relation to phylogeny. Zoological Science, 21: 841-850.
Arana S., Tabata Y.A., Sabino M., Rigolino M.G., Hernandez-Blazquez F.J. (2002). Differential effect of chronic aflatoxin B1 intoxication on the growth performance and incidence of hepatic lesions in triploid and diploid rainbow trout (Oncorhynchus mykiss). Archivos de Medicina Veterinaria, 34: 253-263.
Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., Iwama G.K. (2002). Heat shock protein genes and their functional significance in fish. Gene, 295: 173-183.
Benfey T.J., Sutterlin A.M. (1984). The haematology of triploid landlocked Atlantic salmon, Salmo solar L. Journal of Fish Biology, 24: 333-338.
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 - Part C, 132: 223-233.
Bradford M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Chatchaiphan S., Srisapoome P., Kim J.H., Devlin R.H., Na-Nakorn U. (2017). De novo transcriptome characterization and growth-related gene expression profiling of diploid and triploid bighead catfish (Clarias macrocephalus Günther, 1864). Marine Biotechnology, 19: 36-48.
Christensen K.A., Sakhrani D., Rondeau E.B., Richards J., Koop B.F., Devlin R.H. (2019). Effect of triploidy on liver gene expression in coho salmon (Oncorhynchus kisutch) under different metabolic states. BMC Genomics, 20: 1-14.
Clark M.S., Peck L.S. (2009). HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a mini-review. Marine Genomics, 1: 11-18.
Clarkson K., Kieffer J.D., Currie S. (2005). Exhaustive exercise and the cellular stress response in rainbow trout, Oncorhynchus mykiss. Comparative Biochemistry and Physiology - Part A, 140: 225-232.
Covelo‐Soto L., Leunda P.M., Pérez‐Figueroa A., Morán P. (2015). Genome‐wide methylation study of diploid and triploid brown trout (Salmo trutta L.). Animal Genetics, 46: 280-288.
Currie S., Tufts B. (1997). Synthesis of stress protein 70 (Hsp70) in rainbow trout (Oncorhynchus mykiss) red blood cells. Journal of Experimental Biology, 200: 607-614.
Currie S., Reddin K., McGinn P., McConnell T., Perry S.F. (2008). β-adrenergic stimulation enhances the heat-shock response in fish. Physiological and Biochemical Zoology, 81: 414-425.
DuBeau S.F., Pan F., Tremblay G.C., Bradley T.M. (1998). Thermal shock of salmon in vivo induces the heat shock protein hsp 70 and confers protection against osmotic shock. Aquaculture, 168: 311-323.
Dymowska A. K., Hwang P. P., Goss G. G. (2012). Structure and function of ionocytes in the freshwater fish gill. Respiratory Physiology & Neurobiology, 184: 282-292.
Evans D.H., Piermarini P.M., Choe K.P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85: 97-177.
Fazio F. (2019). Fish hematology analysis as an important tool of aquaculture: a review. Aquaculture, 500: 237-242.
Fulladosa E., Deane E., Ng A.H.Y., Woo N.Y.S., Murat J.C., Villaescusa I. (2006). Stress proteins induced by exposure to sublethal levels of heavy metals in sea bream (Sparus sarba) blood cells. Toxicology in vitro, 20: 96-100.
Goss G.G., Perry S.F., Fryer J.N., Laurent P. (1998). Gill morphology and acid-base regulation in freshwater fishes. Comparative Biochemistry and Physiology - Part A, 119: 107-115.
Ineno T., Tsuchida S., Kanda M., Watabe S. (2005). Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding. Fisheries Science, 71: 767-775.
Iwama G.K., Afonso L.O., Todgham A., Ackerman P., Nakano K. (2004). Are hsps suitable for indicating stressed states in fish?. Journal of Experimental Biology, 207: 15-19.
Kilemade M., Mothersill C. (2001). Heat shock protein 70 levels in rainbow trout primary epidermal cultures in response to 2, 4‐dichloroaniline exposure: A novel in vitro aquatic toxicity marker. Environmental Toxicology, 16: 253-259.
Köhler H.R., Bartussek C., Eckwert H., Farian K., Gränzer S., Knigge T., Kunz N. (2001). The hepatic stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution. Journal of Aquatic Ecosystem Stress and Recovery, 8: 261-279.
Leggatt R.A., Scheer K.W., Afonso L.O., Iwama G.K. (2006). Triploid and diploid rainbow trout do not differ in their stress response to transportation. North American Journal of Aquaculture, 68: 1-8.
Matos I.M., Coelho M.M., Schartl M. (2016). Gene copy silencing and DNA methylation in natural and artificially produced allopolyploid fish. Journal of Experimental Biology, 219: 3072-3081.
Matos I., Machado M.P., Schartl M., Coelho M.M. (2019). Allele-specific expression variation at different ploidy levels in Squalius alburnoides. Scientific Reports, 9: 1-12.
Ohtsuka K., Hata M. (2000). Molecular chaperone function of mammalian Hsp70 and Hsp40-a review. International Journal of Hyperthermia, 16: 231-245.
Otto S.P., Whitton J. (2000). Polyploid incidence and evolution. Annual Reviews of Genetics, 34: 401-437.
Pala I., Coelho M.M., Schartl M. (2008). Dosage compensation by gene-copy silencing in a triploid hybrid fish. Current Biology, 18: 1344-1348.
Peutz I.L.J.A., Oorschot R.W.A., Johnson G.R., Horney B.S., Boon J.H. (1996). The leucogram as an indicator off marine‐cultured rainbow trout, Oncorhynchus mykiss (Walbaum), health in The Netherlands. Aquaculture Research, 27: 437-445.
Pressinoti L.N. (2006). Efeito da triploidização na imunidade celular inespecífica de trutas arco-íris Oncorhynchus mykiss (Walbaum,1792). Master’s Thesis. University of São Paulo, Brazil.
Qiu X.B., Shao Y.M., Miao S., Wang L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cellular and Molecular Life Sciences, 63: 2560-2570.
Rolim G.S., Aparecido L.E.O. (2016). Camargo, Köppen and Thornthwaite climate classification systems in defining climatical regions of the state of São Paulo, Brazil. International Journal of Climatology, 36: 636-643.
Ross L.G., Ross B. (2008). Anaesthetic and sedative techniques for aquatic animals. Blackwell Science. Oxford, United Kingdom.
Roy S., Kumar V., Kumar V., Behera B.K. (2017). Acute phase proteins and their potential role as an indicator for fish health and in diagnosis of fish diseases. Protein & Peptides Letters, 24: 78-89.
Schreck C.B., Tort L. (2016). The concept of stress in fish. In: Schreck C.B., Tort L., Farrell A.P., Brauner C.J.(Eds). Fish Physiology. Elsevier Inc., USA. vol. 35, pp. 1-34.
Scofield E., Bowyer R.T., Duffy L.K. (1999). Baseline levels of Hsp 70, a stress protein and biomarker, in halibut from the Cook Inlet region of Alaska. Science of the Total Environment, 226: 85-88.
Segner H., Sundh H., Buchmann K., Douxfils J., Sundell K.S., Mathieu C., Ruane N., Jutfelt F., Toften H., Vaughan L. (2012). Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiology and Biochemistry, 38: 85-105.
Silva J.R.M.C., Hernandez-Blazquez F.J., Barbieri R.L. (1998). Induced inflammatory process in the Antarctic fish Notothenia neglecta. Polar Biology, 20: 206-212.
Stitt B.C., Burness G., Burgomaster K.A., Currie S., McDermid J.L., Wilson C.C. (2014). Intraspecific variation in thermal tolerance and acclimation capacity in brook trout (Salvelinus fontinalis): physiological implications for climate change. Physiological and Biochemical Zoology, 87: 15-29.
Strzyzewska E., Szarek J., Babinska I. (2016). Morphologic evaluation of the gills as a tool in the diagnostics of pathological conditions in fish and pollution in the aquatic environment: a review. Veterinárni Medicína, (Praha). 61: 123-132.
Sugito K., Yamane M., Hattori H., Hayashi Y., Tohnai I., Ueda M., Tsuchida N., Ohtsuka K. (1995). Interaction between hsp70 and hsp40, eukaryotic homologues of DnaK and DnaJ, in human cells expressing mutant‐type p53. FEBS Letters, 358: 161-164.
Thorgaard G.H., Arbogast D.N., Hendricks J.D., Pereira C.B., Bailey G.S. (1999). Tumor suppression in triploid trout. Aquatic Toxicology, 46: 121-126.
Triebskorn R., Köhler H.R., Honnen W., Schramm M., Adams S.M., Müller E.F. (1997). Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behavior: are these biomarkers related and are they useful to reflect the state of pollution in the field?. Journal of Aquatic Ecosystem Stress and Recovery, 6: 57-73.
Verhille C., Anttila K., Farrell A.P. (2013). A heart to heart on temperature: impaired temperature tolerance of triploid rainbow trout (Oncorhynchus mykiss) due to early onset of cardiac arrhythmia. Comparative Biochemistry and Physiology - Part A., 164: 653-657.
Vijayan M.M., Pereira C., Kruzynski G., Iwama G.K. (1998). Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquatic Toxicology, 40: 101-108.
Virtanen E., Forsman L., Sundby A. (1990). Triploidy decreases the aerobic swimming capacity of rainbow trout (Salmo gairdneri). Comparative Biochemistry and Physiology - Part A, 96: 117-121.
Wang Y., Xu J., Sheng L., Zheng Y. (2007a). Field and laboratory investigations of the thermal influence on tissue-specific Hsp70 levels in common carp (Cyprinus carpio). Comparative Biochemistry and Physiology - Part A, 148: 821-827.
Wang J., Wei Y., Li X., Cao H., Xu M., Dai J. (2007b). 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.
Washburn B.S., Moreland J.J., Slaughter A.M., Werner I., Hinton D.E., Sanders B.M. (2002). Effects of handling on heat shock protein expression in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry, 21: 557-560.
Wendelaar Bonga S.E. (1997). The stress response in fish. Physiological Reviews, 77: 591-625.
Wilson J.M., Laurent P. (2002). Fish gill morphology: inside out. Journal of Experimental Zoology, 293: 192-213.
Wolf J.C., Wheeler J.R. (2018). A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquatic Toxicology, 197: 60-78.
Wu J., Liu T., Rios Z., Mei Q., Lin X., Cao S. (2017). Heat shock proteins and cancer. Trends in Pharmacological Sciences, 38: 226-256.
Yamamoto A., Iida T. (1994). Hematological characteristics of triploid rainbow trout. Fish Pathology, 29: 239-243.
Yamamoto A., Iida T. (1995). Non-specific defense activities of triploid rainbow trout. Fish Pathology, 30: 107-110.
Zarate J., Bradley T.M. (2003). Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture, 223: 175-187.
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2022-03-07
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Derechos de autor 2022 André Luiz Veiga Conrado
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial-CompartirIgual 4.0.
