Skip to main content
Log in

Differential expression pattern of heat shock protein 70 gene in tissues and heat stress phenotypes in goats during peak heat stress period

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

It has been established that the synthesis of heat shock protein 70 (Hsp70) is temperature-dependent. The Hsp70 response is considered as a cellular thermometer in response to heat stress and other stimuli. The variation in Hsp70 gene expression has been positively correlated with thermotolerance in Drosophila melanogaster, Caenorhabditis elegans, rodents and human. Goats have a wide range of ecological adaptability due to their anatomical and physiological characteristics; however, the productivity of the individual declines during thermal stress. The present study was carried out to analyze the expression of heat shock proteins in different tissues and to contrast heat stress phenotypes in response to chronic heat stress. The investigation has been carried out in Jamunapari, Barbari, Jakhrana and Sirohi goats. These breeds differ in size, coat colour and production performance. The heat stress assessment in goats was carried out at a temperature humidity index (THI) ranging from 85.36–89.80 over the period. Phenotyping for heat stress susceptibility was carried out by combining respiration rate (RR) and heart rate (HR). Based on the distribution of RR and HR over the breeds in the population, individual animals were recognized as heat stress-susceptible (HSS) and heat stress-tolerant (HST). Based on their physiological responses, the selected animals were slaughtered for tissue collection during peak heat stress periods. The tissue samples from different organs such as liver, spleen, heart, testis, brain and lungs were collected and stored at −70 °C for future use. Hsp70 concentrations were analyzed from tissue extract with ELISA. mRNA expression levels were evaluated using the SYBR green method. Kidney, liver and heart had 1.5–2.0-fold higher Hsp70 concentrations as compared to other organs in the tissue extracts. Similarly, the gene expression pattern of Hsp70 in different organs indicated that the liver, spleen, brain and kidney exhibited 5.94, 4.96, 5.29 and 2.63-fold higher expression than control. Liver and brain tissues showed the highest gene expression at mRNA levels as compared to kidney, spleen and heart. HST individuals had higher levels of mRNA level expression than HSS individuals in all breeds. The Sirohi breed showed the highest (6.3-fold) mRNA expression levels as compared to the other three breeds, indicating the better heat stress regulation activity in the breed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Airaksinen S, Jokilehto T, Rabergh CMI, Nikinmaa M (2003) Heat- and cold-inducible regulation of HSP70 expression in zebrafish ZF4. Comp Biochem Physiol 36:275–282

    Article  Google Scholar 

  • Al-Tamimi HJ (2007) Thermoregulatory response of goat kids subjected to heat stress. Small Rumin Res 71:280–285

    Article  Google Scholar 

  • Banerjee D, Upadhyay RC, Chaudhary UB, Kumar R, Singh S, Ashutosh GJM, Polley S, Mukherjee A, Das TK, De S (2014) Seasonal variation in expression pattern of genes under HSP70. Cell Stress Chaperones 19:401–408

    Article  CAS  PubMed  Google Scholar 

  • Barbe MF, Tytell M, Gower DJ, Welch WJ (1998) Hyperthermia protects against light damage in the rat retina. Science 241:1817–1820

    Article  Google Scholar 

  • Basirico L, Morera P, Primi V, Lacetera N, Nardone A, Bernabucci U (2011) Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperones 16(4):441–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A (2010) Metabolic and hormonal adaptations to heat stress in domesticated ruminants. Animal 4:1167–1183

    Article  CAS  PubMed  Google Scholar 

  • Chirico WJ, Waters MG, Blobel G (1998) 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332:805–810

    Article  Google Scholar 

  • Collier RJ, Stiening CM, Pollard BC, VanBaale MJ, Baumgard LH, Gentry PC, Coussens PM (2006) Use of gene expression microarrays for evaluating environmental stress tolerance at the cellular level in cattle. J Anim Sci 84(E Suppl):E1–E13

    PubMed  Google Scholar 

  • Dangi SS, Gupta M, Maurya D, Yadav VP, Panda RP, Singh G, Mohan NH, Bhure SK, Das BC, Bag S, Mahapatra R, Sharma GT, Sarkar M (2012) Expression profile of HSP genes during different seasons in goats (Capra hircus). Trop Anim Health Prod 44(8):1905–1912

    Article  PubMed  Google Scholar 

  • Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710

    Article  CAS  PubMed  Google Scholar 

  • Derveaux S, Vandesompele J, Hellemans J (2010) How to do successful gene expression analysis using real-time PCR. Methods 50:227–230

    Article  CAS  PubMed  Google Scholar 

  • Devendra C, Devendra C, Imazumi E (1990) Comparative aspects of digestive physiology and nutrition in goats and sheep. In: Ruminant nutrition and physiology in Asia. Japan Society of Zootechnical Science Ed, Sendai, pp 45–60

    Google Scholar 

  • Gallagher DS, Grosz MD, Womack JE, Skow LC (1993) Chromosomal localization of HSP70 genes in cattle. Mamm Genome 4:388–390

    Article  CAS  PubMed  Google Scholar 

  • Garret AT, Goosen NG, Rehrer NG, Rehrer NG, Patterson MJ, Cotter JD (2009) Induction and decay of short-term heat acclimation. Eur J Appl Physiol 107:659–670

    Article  Google Scholar 

  • Gaughan JB, Bonner SL, Loxton I, Mader TL (2013) Effects of chronic heat stress on plasma concentration of secreted heat shock protein 70 in growing feedlot cattle. J Anim Sci 91(1):120–129

    Article  CAS  PubMed  Google Scholar 

  • Grosz MD, Womack JE, Skow LC (1992) Syntenic conservation of HSP70 genes in cattle and humans. Genomics 14:863–868

    Article  CAS  PubMed  Google Scholar 

  • Hansen PJ (2004) Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci 82:349–360

    Article  PubMed  Google Scholar 

  • Harvey WR (1990) User’s guide for LSMLMW. PC-Version 2, mixed model least squares and maximum likelihood computer program, mimeograph. Ohio State University press, Columbus

    Google Scholar 

  • Hashmi G, Hashmi S, Selvan S, Grewal P, Gaugler R (1997) Polymorphism in heat shock protein gene (Hsp70) in entomopathogenic nematodes (rhabditida). J Therm Biol 22:143–149

    Article  CAS  Google Scholar 

  • Hecker JG, McGarvey M (2011) Heat shock proteins as biomarkers for the rapid detection of brain and spinal cord ischemia: a review and comparison to other methods of detection in thoracic aneurysm repair. Cell Stress Chaperones 16:119–131

    Article  CAS  PubMed  Google Scholar 

  • Hecker JG, Sundram H, Zou S, Praestgaard A, Bavaria JE, Ramchandren S, McGarvey M (2008) Heat shock proteins HSP70 and HSP27 in the cerebral spinal fluid of patients undergoing thoracic aneurysm repair correlate with the probability of postoperative paralysis. Cell Stress Chaperones 13(4):435–446

    Article  PubMed  PubMed Central  Google Scholar 

  • Hightower LE, Norris CE, di Iorio PJ, Fielding E (1999) Heat shock responses of closely related species of tropical and desert fish. Integr Comp Biol 39:877–888

    Google Scholar 

  • Horowitz M (2002) From molecular and cellular to integrative heat defense during exposure to chronic heat. Comp Biochem Physiol Part A, Mol Intergr Physiol 131:475–483

    Article  Google Scholar 

  • Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111

    Article  CAS  PubMed  Google Scholar 

  • King JM (1983) Livestock water needs in pastoral Africa in relation to climate and forage. Res report no. 7. Int. Lives Center Africa (ILCA), Addis Ababa

    Google Scholar 

  • King YT, Lin CS, Lin JH, Lee WC (2002) Whole-body hyperthermia-induced thermo tolerance is associated with the induction of heat shock protein 70 in mice. J Exp Biol 205:273–278

    CAS  PubMed  Google Scholar 

  • Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermo tolerance. J Appl Physiol 92:2177–2186

    Article  CAS  PubMed  Google Scholar 

  • Lacetera N, Bernabucci U, Scalia D, Basiricò L, Morera P, Nardone A (2006) Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J Dairy Sci 89:4606–4612

    Article  CAS  PubMed  Google Scholar 

  • Latchman DS (2001) Heat shock protein and cardiac protection. Cardiovasc Res 51:637–646

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−_ʌʌCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • McDowell RE, Hooven NW, Camoens JK (1976) Effects of climate on performance of Holsteins in first lactation. J Dairy Sci 59:965–973

    Article  Google Scholar 

  • Mizzen L, Welch W (1988) Effects on protein synthesis activity and the regulation of heat shock protein 70 expression. J Cell Biol 106:1105–1116

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI, Tissieres A, Georgopoulos C (1994) Progress and perspectives on the biology of heat shock proteins and molecular chaperones In: Morimoto, R.I., Tissieres, A, Georgopoulos, C. (Eds.), The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbour Laboratory Press, Cold Spring Harbour 1–30

  • Paula-Lopes FF, Chase CC Jr, Al-Katanani YM, Krininger CE 3rd, Rivera RM, Tekin S, Majewski AC, Ocon OM, Olson TA, Hansen PJ (2003) Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction 125(2):285–294

    Article  CAS  PubMed  Google Scholar 

  • Rout PK, Saxena VK, Khan BU, Roy R, Mandal A, Singh SK, Singh LB (2000) Characterization of Jamunapari goats in their home tract. Anim Genet Resource Inf 27:43–52

    Article  Google Scholar 

  • Silanikove N, Koluman N (2015) Impact of climate change on the dairy industry in temperate zones: predications on the overall negative impact and on the positive role of dairy goats in adaptation to earth warming. Small Rumin Res 123:27–34

    Article  Google Scholar 

  • Sonna LA, Fujita J, Gaffin SL, Lilly CM (1985) Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92(4):1725–1742

    Article  Google Scholar 

  • Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72:1063–1081

    CAS  PubMed  Google Scholar 

  • Wrenzycki C, Wells D, Herrmann D, Miller A, Oliver J, Tervit R, Niemann H (2001) Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol Reprod 65:309–317

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M, Hirayoshi K, Nagata K (2004) Characterization of multiple members of the HSP70 family in platy fish culture cells: molecular evolution of stress protein HSP70 in vertebrates. Gene 336:207–218

    Article  CAS  PubMed  Google Scholar 

  • Zulkifi I, Liew PK, Israf DA, Omar AR, Hair-Bejo M (2003) Effect of early age feed restriction and thermal conditioning on heterophil/lymphocyte ratio, heat shock 70 and body temperature of male broiler chickens subjected to acute heat stress. J Therm Biol 28:217–222

    Article  Google Scholar 

  • Zulkifli I, Al-Aqil A, Omar AR, Sazili AQ, Rajion MA (2008) Housing system affects stress and fear reaction and meat quality of broiler chickens subjected to road transportation. In proceeding of XXIII world’s poultry congress. World’s Poultry Science Association, Odijk, The Netherlands 380

  • Zulkifli I, Norbaiyah B, Cheah YW, Soleimani AF, Sazli AQ, Goh YM, Rajion MA (2010) A note on heat shock protein 70 expression in goats subjected to road transportation hot, humid tropical conditions. Animal 4:973–976

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work was funded through project no. C4/C-30033(comp-IV) by the NAIP, Indian Council of Agricultural Research, New Delhi, India. The authors thank Helen Neumann of the Cell Stress & Chaperones editorial office for the English language help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. K. Rout.

Ethics declarations

Institute Animal Ethics Committee (IAEC), Central Institute for Research on Goats (CIRG), Makhdoom, approved the experimental procedures.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rout, P.K., Kaushik, R. & Ramachandran, N. Differential expression pattern of heat shock protein 70 gene in tissues and heat stress phenotypes in goats during peak heat stress period. Cell Stress and Chaperones 21, 645–651 (2016). https://doi.org/10.1007/s12192-016-0689-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-016-0689-1

Keywords

Navigation