Abstract
Research efforts of elucidating the molecular mechanisms governing heat shock response which imparts thermo-tolerance ability to indigenous breeds are very scanty. Therefore, a study was conducted with the primary objective to determine the impact of heat stress on the expression pattern of different heat shock response genes in the hepatic tissues of indigenous Salem Black goat. The study was conducted for a period of 45 days in twelve 1-year-old female Salem Black breed goats. The animals were randomly allocated into two groups of six animals each, C (n = 6; Salem Black control) and HS (n = 6; Salem Black heat stress). The C animals were maintained in the shed in comfort condition while HS animals were exposed outside to summer heat stress between 10:00 h to 16:00 h during experimental period. The animals were slaughtered at the end of study and their liver samples were collected for assessing the different heat shock response genes. Based on the results obtained from the study it was established that the heat shock protein 70 (HSP70), HSP90, super oxide dismutase (SOD), nitrous oxide synthase 1 (NOS1) genes were significantly (P < 0.05) down regulated. However, heat stress did not influence the expression pattern of heat shock factor-1 (HSF1) gene. The lower level of expression of all heat shock response genes may be due to less magnitude of heat stress in the study to induce cellular stress response in Salem Black goats.
References
Abravaya, K., Phillips, B. and Morimoto, R. I. 1991. 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. Genes & development, 5(11), 2117–2127.
Aleena, J., Sejian, V., Bagath, M., Krishnan, G., Beena, V. and Bhatta, R. 2018. Resilience of three indigenous goat breeds to heat stress based on phenotypic traits and PBMC HSP70 expression. International Journal of Biometerology, 62, 1995–2005.
Amundson, J.L., Mader, T.L., Rasby, R.J. and Hu, Q.S. 2006. Environmental effects on pregnancy rate in beef cattle. Journal of Animal Science, 84, 3415–3420.
Archana, P.R., Aleena, J., Prana, P., Vidya, M.K., Niyas, P.A.A., Bagath, M., Krishnan, G., Manimaran, A., Beena, V., Kurien, E.K., Sejian, V. and Bhatta, R. 2017. Role of heat shock proteins in livestock adaptation to heat stress. Journal of Dairy, Veterinary and Animal Research, 5, 1–8.
Archana, P.R., Sejian, V., Ruban, W., Bagath, M., Krishnan, G., Aleena, J., Manjunathareddy, G.B., Beena, V. and Bhatta, R. 2018. Comparative assessment of heat stress induced changes in carcass traits, plasma leptin profile and skeletal muscle myostatin and HSP70 gene expression patterns between indigenous Osmanabadi and Salem Black goat breeds, Meat Science, 141, 66–80.
Bernabucci, U., Ronchi, B., Lacetera, N. and Nardone, A. 2002. Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of Dairy Science, 85, 2173–2179.
Bernabucci, U., Lacetera, N., Baumgard, L.H., Rhoads, R.P., Ronchi, B. and Nardone, A. 2010. Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal, 4, 1167–1183.
Bharati, J., Dangi, S.S., Mishra, S.R., Chouhan, V.S., Verma, V., Shankar, O., Bharti, M.K., Paul, A., Mahato, D.K., Rajesh, G. and Singh, G. 2017. Expression analysis of toll like receptors and interleukins in Tharparkar cattle during acclimation to heat stress exposure. Journal of Thermal Biology, 65, 48–56.
Chaidanya, K., Soren, N.M., Sejian, V., Bagath, M., Manjunathareddy, G.B., Kurien, E.K., Varma, G. and Bhatta, R. 2017. Impact of heat stress, nutritional stress and combined (heat and nutritional) stresses on rumen associated fermentation characteristics, histopathology and HSP70 gene expression in goats. Journal of Animal Behaviour and Biometeorology, 5, 36–48.
Chauhan, S.S., Celi, P., Fahri, F.T., Leury, B.J. and Dunshea, F.R. 2014. Dietary antioxidants at supranutritional doses modulate skeletal muscle heat shock protein and inflammatory gene expression in sheep exposed to heat stress. Journal of Animal Science, 92, 4897–4908.
Clos, J., Rabindran, S., Wisniewski, J. A. N. and Wu, C. 1993. Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment. Nature, 364(6434), 252.
Collier, R.J., Collier, J.L., Rhoads, R.P. and Baumgard, L.H. 2008. Invited review: Genes involved in the bovine heat stress response. Journal of Dairy Science, 91, 445–454.
da Silva, A.C., Simão, R.C., Susin, M.F., Baldini, R.L., Avedissian, M. and Gomes, S.L. 2003. Downregulation of the heat shock response is independent of DnaK and sigma32 levels in Caulobacter crescentus. Molecular Microbiology, 49, 541–53.
Das, R., Sailo, L., Verma, N., Bharti, P. and Saikia, J. 2016. Impact of heat stress on health and performance of dairy animals: A review. Veterinary World 9: 260–268.
Flanagan, S. W., Ryan, A. J., Gisolfi, C. V. and Moseley, P. L. 1995. Tissue-specific HSP70 response in animals undergoing heat stress. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 268(1), R28-R32.
Gaughan, J.B., Bonner, S.L., Loxton, I. and Mader, T.L. 2013. Effects of chronic heat stress on plasma concentration of secreted heat shock protein 70 in growing feedlot cattle. Journal of Animal Science, 91, 120–129.
Gaughan, J.B., Sejian, V., Mader, T. and Dunshea, F.R. 2018. Adaptation strategies: ruminants. Animal Frontiers, vfy029, https://doi.org/10.1093/af/vfy029
Kaushik, R., Dige, M., Dass, G., Ramachandran, N. and Rout, P.K. 2018. Superoxide dismutase activity in response to heat stress in Jamunapari goats. Indian Journal of Biochemistry & Biophysics, 55, 39–43.
Kregel, K. C. 2002. Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Journal of applied physiology, 92(5), 2177–2186.
Kumar, A., Ashraf, S., Goud, T.S., Grewal, A., Singh, S.V., Yadav, B.R. and Upadhyay, R.C. 2015. Expression profiling of major heat shock protein genes during different seasons in cattle (Bos indicus) and buffalo (Bubalus bubalis) under tropical climatic condition. Journal of Thermal Biology, 51, 55–64.
Li, Q.L., Ju, Z.H., Huang, J.M., Li, J.B., Li, R.L., Hou, M.H., Wang, C.F. and Zhong, J.F. 2011. Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA and Cell Biology, 30, 247–254.
Mader, T.L. 2003. Environmental stress in confined beef cattle. Journal of Animal Science. 81, 110–119.
Manjari, R., Yadav, M., Uniyal, S., Rastogi, S.K., Sejian, V. and Hyder, I. 2015. HSP70 as a marker of heat and humidity stress in Tarai Buffalo. Tropical Animal Health and Production, 47, 111–116.
McDowell, R.E. 1972. Improvement of livestock production in warm climate. WH Freeman and Co, San Fransisco, USA.
Mondal, T., Banjare, C.S., Dangi, S.S., Bag, S., Sarkar, M. and Das, BC. 2018. The Effect of Exogenous HSP70 on Expression Kinetics of HSP70, HSP90, HSP110 and IL2 and IL6 in Peripheral Blood Mononuclear Cells and Possible Crosstalk between Them in Black Bengal Goat. International Journal of Current Microbiology and Applied Sciences, 7, 506–517.
Niyas, P.A.A., Sejian, V., Bagath, M., Parthipan, S., Selvaraju, S., Manjunathareddy, G., Kurien, E.K., Varma, G. and Bhatta, R. 2017. Effect of heat and nutritional stress on growth and testicular HSP70 expression in goats. Journal of Agrometeorology, 19, 189–194.
Pragna, P., Sejian, V., Soren, N.M., Bagath, M., Krishnan, G., Beena, V., Devi, P.I. and Bhatta, R. 2017. Summer season induced rhythmic alterations in metabolic activities to adapt to heat stress in three indigenous (Osmanabadi, Malabari and Salem Black) goat breeds. Biological Rhythm Research. 49, 551–565.
Pragna, P., Sejian, V., Bagath, M., Krishnan, G., Archana, P.R., Soren, N.M., Beena, V. and Bhatta, R. 2018. Comparative assessment of growth performance of three different indigenous goat breeds exposed to summer heat stress. Journal of Animal Physiology and Animal Nutrition, 102, 825–836.
Rashamol, V.P., Sejian, V., Bagath, M., Krishnan, G., Archana, P.R. and Bhatta, R. 2018. Physiological adaptability of livestock to heat Stress: an updated review. Journal of Animal Behaviour and Biometeorology, 6, 62–71.
Rout, P.K., Kaushik, R. and Ramachandran, N. 2016. Differential expression pattern of heat shock protein 70 gene in tissues and heat stress phenotypes in goats during peak heat stress period. Cell Stress Chaperones, 21, 645–651.
Sejian, V., Bhatta, R., Gaughan, J.B., Dunshea, F.R. and Lacetera, N. 2018. Review: Adaptation of animals to heat stress. Animal, 12, s431-s444.
Sharma, S., Ramesh, K., Hyder, I., Uniyal, S., Yadav, V.P., Panda, R.P., Maurya, V.P., Singh, G., Kumar, P., Mitra, A. and Sarkar, M. 2013. Effect of melatonin administration on thyroid hormones, cortisol and expression profile of heat shock proteins in goats (Capra hircus) exposed to heat stress. Small Ruminant Research, 112, 216–223.
Shilja, S., Sejian, V., Bagath, M., Mech, A., David, I.C.G., Kurien, E.K., Varma, G. and Bhatta, R. 2016. Adaptive capability as indicated by behavioral and physiological responses, plasma HSP70 level and PBMC HSP70 mRNA expression in Osmanabadi goats subjected to combined (heat and nutritional) stressors. International Journal of Biometeorology, 60, 1311–1323.
Shilja, S., Sejian, V., Bagath, M., Manjunathareddy, G.B., Kurien, E.K., Varma, G. and Bhatta, R. 2017. Summer season related heat and nutritional stresses on the adaptive capability of goats based on blood biochemical response and hepatic HSP70 gene expression. Biological Rhythms Research, 48, 65–83.
Silva, C.F., Sartorelli, E.S., Castilho, A.C., Satrapa, R.A., Puelker, R.Z., Razza, E.M., Ticianelli, J.S., Eduardo, H.P., Loureiro, B. and Barros, C.M. 2013. Effects of heat stress on development, quality and survival of Bos indicus and Bos taurus embryos produced in vitro. Theriogenology, 79, 351–357.
Singh, A.K. 2013. Effect of heat stress on the behaviour of in vitro cultured dermal fibroblast of cattle and buffalo. Doctoral dissertation, NDRI, Karnal.
Slimen, I.B., Najar, T., Ghram, A. and Abdrrabba, M. (2016). Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. Journal of Animal Physiology and Animal Nutrition, 100, 401–412.
Tomanek, L. and Somero, G. N. 2002. Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. Journal of Experimental Biology, 205(5), 677–685.
Wang, L., Xue, B., Wang, K., Li, S. and Li, Z. 2010. Effect of heat stress on endotoxin flux across mesenteric-drained and portal-drained viscera of dairy goat. Journal of Animal Physiology and Animinal Nutrition, 95, 468–477.
Xu, Q., Wang, Y.C., Hu, L.R. and Kang, L. 2018. The effect of temperature stress on milk production traits and blood biochemical parameters of Chinese Holstein cows. Proceedings of the World Congress on Genetics Applied to Livestock Production, Volume Electronic Poster Session - Genetic Gain - In Challenging Environments, , 95.
Yadav, V.P., Dangi, S.S., Chouhan, V.S., Gupta, M., Dangi, S.K., Singh, G., Maurya, V.P., Kumar, P. and Sarkar, M. 2016. Expression analysis of NOS family and HSP genes during thermal stress in goat (Capra hircus). International Journal of Biometeorology, 60, 381–389.
Yamashita, M., Hirayoshi, K., and Nagata, K. 2004. Characterization of multiple members of the HSP70 family in platyfish culture cells: molecular evolution of stress protein HSP70 in vertebrates. Gene, 336(2), 207–218.
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The authors are also highly thankful to the Director, ICAR-National Institute of Animal Nutrition and Physiology for providing the research facilities to complete the experiment.
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Madhusoodan, A.P., Bagath, M., Sejian, V. et al. Summer season induced changes in quantitative expression patterns of different heat shock response genes in Salem black goats. Trop Anim Health Prod 52, 2725–2730 (2020). https://doi.org/10.1007/s11250-020-02242-5
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DOI: https://doi.org/10.1007/s11250-020-02242-5