Effects of heat stress on biochemical parameters and heat shock protein family A (Hsp70) member 5 (HSPA5) mRNA expression in rainbow trout (Oncorhynchus mykiss)
Binpeng Xia A , Zhe Liu A B , Yanjing Zhou A , Yongjie Wang A , Jinqiang Huang A , Yongjuan Li A , Yujun Kang A , Jianfu Wang A and Xiaoxia Liu AA College of Animal Science and Technology, Gansu Agricultural University, 1 Yingmencun, Anning District, Lanzhou, 730070, Gansu, P.R. China.
B Corresponding author. Email: liuz@gsau.edu.cn
Marine and Freshwater Research 69(11) 1674-1680 https://doi.org/10.1071/MF18029
Submitted: 1 June 2017 Accepted: 11 April 2018 Published: 20 August 2018
Abstract
Rainbow trout (Oncorhynchus mykiss) is a cold-water species of salmonid, and high temperatures are a significant threat to its aquaculture. In order to understand the degree of the heat stress response and the mechanisms involved, full-sibling inbred O. mykiss individuals were sampled at 18, 21, 23, 24, 25 and 26°C to investigate changes in some serum biochemical parameters, as well as in the mRNA expression of heat shock protein family A (Hsp70) member 5 (HSPA5; also known as glucose regulated protein 78 (GRP78)) in different tissues (liver, mid-kidney, heart, spleen and brain). At 21°C, there was a significant increase in the spleen macrophage respiratory burst and a significant decrease in superoxide dismutase activity compared with 18°C (P < 0.05). Malondialdehyde peaked at 23°C, whereas alanine transaminase and aspartate aminotransferase activity were both twofold higher at 25 and 26°C compared with that at 18°C. The Ca2+, Mg2+, PO43– and glucose (Glu) content of serum declined significantly at 21°C relative to 18°C (P < 0.05). The expression of HSPA5 mRNA responded in a temperature- and tissue-specific manner to heat stress. Except for in the spleen, HSPA5 mRNA expression was significantly higher in all tissues at 25 and 26°C than that at 18°C (P < 0.05). These results indicate that heat stress causes oxidative damage, decreases the Ca2+, Mg2+, PO43– and Glu content of serum and induces HSPA5 mRNA expression.
References
Amemiya, S., Kamiya, T., Nito, C., Inaba, T., Kato, K., Ueda, M., Shimazaki, K., and Katayama, Y. (2005). Anti-apoptotic and neuroprotective effects of edaravone following transient focal ischemia in rats. European Journal of Pharmacology 516, 125–130.| Anti-apoptotic and neuroprotective effects of edaravone following transient focal ischemia in rats.Crossref | GoogleScholarGoogle Scholar |
Barton, B. A., and Iwama, G. K. (1991). Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases 1, 3–26.
| Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids.Crossref | GoogleScholarGoogle Scholar |
Burrells, C., Williams, P. D., Southgate, P. J., and Crampton, V. O. (1999). Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Veterinary Immunology and Immunopathology 72, 277–288.
| Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins.Crossref | GoogleScholarGoogle Scholar |
Casas, C. (2017). GRP78 at the centre of the stage in cancer and neuroprotection. Frontiers in Neuroscience 11, 1–15.
| GRP78 at the centre of the stage in cancer and neuroprotection.Crossref | GoogleScholarGoogle Scholar |
Caspersen, C., Pedersen, P. S., and Treiman, M. (2000). The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein. The Journal of Biological Chemistry 275, 22363–22372.
| The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein.Crossref | GoogleScholarGoogle Scholar |
Das, S., Mohapatra, A., and Sahoo, P. K. (2015). Expression analysis of heat shock protein genes during Aeromonas hydrophila infection in rohu, Labeo rohita, with special reference to molecular characterization of GRP78. Cell Stress & Chaperones 20, 73–84.
| Expression analysis of heat shock protein genes during Aeromonas hydrophila infection in rohu, Labeo rohita, with special reference to molecular characterization of GRP78.Crossref | GoogleScholarGoogle Scholar |
Feder, M. E., and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperons, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243–282.
| Heat-shock proteins, molecular chaperons, and the stress response: evolutionary and ecological physiology.Crossref | GoogleScholarGoogle Scholar |
Feng, G. P., Zhuang, P., Zhang, L. Z., Liu, J. Y., Duan, M., Zhao, F., and Yan, W. G. (2012). Effects of water temperature on metabolic enzyme and antioxidase activities in juvenile Chinese sturgeon (Acipenser sinensis). Shui Sheng Sheng Wu Hsueh Bao 93, 137–142.
He, F. L., Xiang, J. G., Li, C. J., Li, Z. Z., and Chen, K. J. (2007). Preliminary study on the effect of water temperature on hematology indices of rainbow trout. Shui Sheng Sheng Wu Hsueh Bao 31, 363–369.
Hokanson, K. E. F., Kleiner, C. F., and Thorslund, T. W. (1977). Effects of constant temperatures and diel temperature fluctuations on specific growth and mortality rates and yield of juvenile rainbow trout, Salmo gairdneri. Journal of the Fisheries Research Board of Canada 34, 639–648.
| Effects of constant temperatures and diel temperature fluctuations on specific growth and mortality rates and yield of juvenile rainbow trout, Salmo gairdneri.Crossref | GoogleScholarGoogle Scholar |
Hong, M. L., Chen, L. Q., Gu, S. Z., Liu, C., Zhang, L., and Li, E. C. (2007). Effect of temperature change on immunochemical indexes of Eriocheir sinensis. Chinese Journal of Applied and Environmental Biology 13, 818–822.
Huang, Z. H., Ma, A. J., and Wang, X. A. (2011). The immune response of turbot Scophthalmus maximus (L.), skin to high water temperature. Journal of Fish Diseases 34, 619–627.
| The immune response of turbot Scophthalmus maximus (L.), skin to high water temperature.Crossref | GoogleScholarGoogle Scholar |
Ineno, T., Tsuchida, S., Kanda, M., and Watabe, S. (2005). Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding. Fisheries Science 71, 767–775.
| Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding.Crossref | GoogleScholarGoogle Scholar |
Iwama, G. K., Thomas, P. T., Forsyth, R. B., and Vijayan, M. M. (1998). Heat shock protein expression in fish. Reviews in Fish Biology Fisheries 8, 35–56.
| Heat shock protein expression in fish.Crossref | GoogleScholarGoogle Scholar |
Kagawa, N. (2004). A drastic reduction in the basal level of heat-shock protein 90 in the brain of goldfish (Carassius auratus) after administration of geldanamycin. Zoological Science 21, 1085–1089.
| A drastic reduction in the basal level of heat-shock protein 90 in the brain of goldfish (Carassius auratus) after administration of geldanamycin.Crossref | GoogleScholarGoogle Scholar |
Kant Misra, U., Gonzalez-Gronow, M., Gawdi, G., Wang, F., and Pizzo, S. V. (2004). A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates alpha2M*-induced signalling. Cellular Signalling 16, 929–938.
| A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates alpha2M*-induced signalling.Crossref | GoogleScholarGoogle Scholar |
Kaufman, R. J. (1999). Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translation controls. Genes & Development 13, 1211–1233.
| Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translation controls.Crossref | GoogleScholarGoogle Scholar |
Kiang, J. G., and Tsokos, G. C. (1998). Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacology & Therapeutics 80, 183–201.
| Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology.Crossref | GoogleScholarGoogle Scholar |
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Arozena, A. A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., Adhihetty, P. J., Adler, S. G., Agam, G., Agarwal, R., Aghi, M. K., Agnello, M., Agostinis, P., Aguilar, P. V., Aguirre-Ghiso, J., Airoldi, E. M., et al. (2016). Guidelines for use and interpretation of assays for monitoring autophagy (3rd edn). Autophagy 12, 1–222.
| Guidelines for use and interpretation of assays for monitoring autophagy (3rd edn).Crossref | GoogleScholarGoogle Scholar |
Lee, A. S. (2001). The glucose-regulated proteins: stress induction and clinical applications. Trends in Biochemical Sciences 26, 504–510.
| The glucose-regulated proteins: stress induction and clinical applications.Crossref | GoogleScholarGoogle Scholar |
Li, D. P., Liu, S. Y., Xie, C. X., and Zhang, X. Z. (2008). Effects of water temperature on serum content of reactive oxygen species and antioxidant defense system in Chinese sturgeon, Acipenser sinensis. Shui Sheng Sheng Wu Hsueh Bao 32, 327–332.
| Effects of water temperature on serum content of reactive oxygen species and antioxidant defense system in Chinese sturgeon, Acipenser sinensis.Crossref | GoogleScholarGoogle Scholar |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method.Crossref | GoogleScholarGoogle Scholar |
Lushchak, V. I., and Bagnyukova, T. V. (2006). Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comparative Biochemistry and Physiology – C. Toxicology & Pharmacology 143, 36–41.
| Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes.Crossref | GoogleScholarGoogle Scholar |
Ma, Y., and Hendershot, L. M. (2004). ER chaperone functions during normal and stress conditions. Journal of Chemical Neuroanatomy 28, 51–65.
| ER chaperone functions during normal and stress conditions.Crossref | GoogleScholarGoogle Scholar |
Mancino, R., Pierro, D. D., Varesi, C., Cerulli, A., Feraco, A., Cedrone, C., Pinazo-Duran, M. D., Coletta, M., and Nucci, C. (2011). Lipid peroxidation and total antioxidant capacity in vitreous, aqueous humor, and blood samples from patients with diabetic retinopathy. Molecular Vision 17, 1298–1304.
Miliukiené, V., Biziuleviciené, G., and Pilinkiené, A. (2003). Quantitative evaluation of macrophage phagocytosing capacity by a fluorometric assay. Acta Biologica Hungarica 54, 347–356.
| Quantitative evaluation of macrophage phagocytosing capacity by a fluorometric assay.Crossref | GoogleScholarGoogle Scholar |
Mulero, I., García-Ayala, A., Meseguer, J., and Mulero, V. (2007). Maternal transfer of immunity and ontogeny of autologous immunocompetence of fish: a minireview. Aquaculture 268, 244–250.
| Maternal transfer of immunity and ontogeny of autologous immunocompetence of fish: a minireview.Crossref | GoogleScholarGoogle Scholar |
Munro, S., and Pelham, H. R. B. (1986). An hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291–300.
| An hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein.Crossref | GoogleScholarGoogle Scholar |
Nikoskelainen, S., Bylund, G., and Lilius, E. M. (2004). Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Developmental and Comparative Immunology 28, 581–592.
| Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity.Crossref | GoogleScholarGoogle Scholar |
Ojima, N., Yamashita, M., and Watabe, S. (2005). Quantitative mRNA expression profiling of heat-shock protein families in rainbow trout cells. Biochemical and Biophysical Research Communications 329, 51–57.
| Quantitative mRNA expression profiling of heat-shock protein families in rainbow trout cells.Crossref | GoogleScholarGoogle Scholar |
Ortiz, C., and Cardemil, L. (2001). Heat-shock responses in two leguminous plants: a comparative study. Journal of Experimental Botany 52, 1711–1719.
| Heat-shock responses in two leguminous plants: a comparative study.Crossref | GoogleScholarGoogle Scholar |
Paschen, W. (2004). Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis. Current Neurovascular Research 1, 173–181.
| Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis.Crossref | GoogleScholarGoogle Scholar |
Podrabsky, J. E., and Somero, G. N. (2004). Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. The Journal of Experimental Biology 207, 2237–2254.
| Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus.Crossref | GoogleScholarGoogle Scholar |
Press, C. M., and Evensen, Ø. (1999). The morphology of the immune system in teleost fishes. Fish & Shellfish Immunology 9, 309–318.
| The morphology of the immune system in teleost fishes.Crossref | GoogleScholarGoogle Scholar |
Qian, Y., Zheng, Y., Ramos, K. S., and Tiffany-Castiglioni, E. (2005). GRP78 compartmentalized redistribution in Pb-treated glia: role of GRP78 in lead-induced oxidative stress. Neurotoxicology 26, 267–275.
| GRP78 compartmentalized redistribution in Pb-treated glia: role of GRP78 in lead-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Roberts, R. J., Agius, C., Saliba, C., Bossier, P., and 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.
| Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review.Crossref | GoogleScholarGoogle Scholar |
Shi, H. N., Liu, Z., Zhang, J. P., Kang, Y. J., Wang, J. F., Huang, J. Q., and Wang, W. M. (2015). Short communication: effect of heat stress on heat-shock protein (Hsp60) mRNA expression in rainbow trout Oncorhynchus mykiss. Genetics and Molecular Research 14, 5280–5286.
| Short communication: effect of heat stress on heat-shock protein (Hsp60) mRNA expression in rainbow trout Oncorhynchus mykiss.Crossref | GoogleScholarGoogle Scholar |
Shiu, R. P., Pouyssegur, J., and Pastan, I. (1977). Glucose depletion accounts for the induction of two transformation-sensitive membrane proteins in Rous sarcoma virus-transformed chick embryo fibroblasts. Proceedings of the National Academy of Sciences of the United States of America 74, 3840–3844.
| Glucose depletion accounts for the induction of two transformation-sensitive membrane proteins in Rous sarcoma virus-transformed chick embryo fibroblasts.Crossref | GoogleScholarGoogle Scholar |
Tang, M., Guang, M. A., and Jun, X. U. (2002). Advances in research of fish immunology. Immunological Journal 2, 97–106.
Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions 160, 1–40.
| Free radicals, metals and antioxidants in oxidative stress-induced cancer.Crossref | GoogleScholarGoogle Scholar |
Varfolomeeva, E. Y., Ivanov, E. I., Drobchenko, E. A., Semenova, E. V., and Filatov, M. V. (2010). Detection of inflammatory processes during various diseases by the method of flow cytofluorometry. Bulletin of Experimental Biology and Medicine 149, 485–489.
| Detection of inflammatory processes during various diseases by the method of flow cytofluorometry.Crossref | GoogleScholarGoogle Scholar |
Wendelaar Bonga, S. E. (1997). The stress response in fish. Physiological Reviews 77, 591–625.
| The stress response in fish.Crossref | GoogleScholarGoogle Scholar |