Skip to main content
SpringerLink
Log in

Expression of HSPs: an adaptive mechanism during long-term heat stress in goats (Capra hircus)

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

Menacing global rise in surface temperature compelled more focus of research over understanding heat stress response mechanism of animals and mitigation of heat stress. Twenty-four goats divided into four groups (n = 6) such as NHS (non-heat-stressed), HS (heat-stressed), HS + VC (heat-stressed administered with vitamin C), and HS + VE + Se (heat-stressed administered with vitamin E and selenium). Except NHS group, other groups were exposed to repeated heat stress (42 °C) for 6 h on 16 consecutive days. Blood samples were collected at the end of heat exposure on days 1, 6, 11, and 16. When groups compared between days, expression of all heat shock proteins (HSPs) showed a similar pattern as first peak on day 1, reached to basal level on the sixth day, and followed by second peak on day 16. The relative messenger RNA (mRNA) and protein expression of HSP 60, HSP70, and HSP90 was observed highest (P < 0.05) in HS group, followed by antioxidant-administered group on days 1 and 16, which signifies that antioxidants have dampening effect on HSP expression. HSP105/110 expression was highest (P < 0.05) on day 16. We conclude that HSP expression pattern is at least two-peak phenomenon, i.e., primary window of HSP protection on the first day followed by second window of protection on day 16. HSP60, HSP70, and HSP90 play an important role during the initial phase of heat stress acclimation whereas HSP105/110 joins this cascade at later phase. Antioxidants may possibly attenuate the HSP expression by reducing the oxidative stress.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahn SG, Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17:516–528

    Article  CAS  Google Scholar 

  • Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, Vreugdenhil D et al (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896

    Article  CAS  Google Scholar 

  • Ananthan J, Goldberg AL, Voellmy R (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232:522–524

    Article  CAS  Google Scholar 

  • Ayo JO, Oladele SB, Fayomi A, Jumbo SD, Hambolu JO (1998) Body temperature, respiration and heart rate in the Red Sokoto goat during the harmattan season. Bull Anim Health Prod Afr 46:161–166

    Google Scholar 

  • Bianca W (1965) Reviews of the progress of dairy science. Section A. Physiology: cattle in a hot environment. J Dairy Res 32:291–345

    Article  Google Scholar 

  • Collier RJ, Collier JL, Rhoads RP, Baumgard LH (2008) Invited review: genes involved in the bovine stress response. J Dairy Sci 91:445–454

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Dangi SS, Gupta M, Nagar V, Yadav VP, Dangi SK, Shankar OM, Chouhan VS, Kumar P, Singh G, Sarkar M (2014) Impact of short-term heat stress on physiological responses and expression profile of HSPs in Barbari goats. Int J Biometeorol. doi:10.1007/s00484-014-0809-5

    Google Scholar 

  • De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11(1):1–12

    Article  Google Scholar 

  • Deb R, Sajjanar B, Singh U, Kumar S, Singh R, Sengar G, Sharma A (2014) Effect of heat stress on the expression profile of Hsp90 among Sahiwal (Bos indicus) and Frieswal (Bos indicus × Bos taurus) breed of cattle: a comparative study. Gene 536(2):435–440

    Article  CAS  Google Scholar 

  • DiDomenico BJ, Bugaisky GE, Lindquist S (1982) The heat shock response is self regulated at both at both the transcriptional and posttranscriptional levels. Cell 31(3 pt 2):593–603

    Article  CAS  Google Scholar 

  • Fazeli P, Zamiri MJ, Farshad A, Khalili B (2010) Effects of vitamin C on testicular and seminal characteristics of Markhoz goats. Iran J Vet Res 11(32):267–272

    Google Scholar 

  • Fiege U, Morimoto RI, Yahara I, Polla BS (1996) Stress-inducible cellular responses. Birckhauser Verlag, Basle

    Google Scholar 

  • Gorman AM, Heavey B, Creagh E, Cotter TG, Samali A (1999) Antioxidant-mediated inhibition of the heat shock response leads to apoptosis. FEBS Lett 445:98–102

    Article  CAS  Google Scholar 

  • Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275:2–12

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580

    Article  CAS  Google Scholar 

  • Hatayama T, Yasuda K, Nishiyama E (1994) Characterization of high-molecular-mass heat shock proteins and 42 degrees C-specific heat shock proteins of murine cells. Biochem Biophys Res Commun 204:357–365

    Article  CAS  Google Scholar 

  • Ishihara K, Yasuda K, Hatayama T (1999) Molecular cloning, expression and localization of human 105 kDa heat shock protein, hsp105. Biochim Biophys Acta 1444:138–142

    Article  CAS  Google Scholar 

  • Ishihara K, Yamagishi N, Hatayama T (2003) Protein kinase CK2 phosphorylates Hsp105 alpha at Ser509 and modulates its function. Biochem J 371:917–925

    Article  CAS  Google Scholar 

  • Khassaf M, McArdle A, Esanu C, Vasilaki A, McArdle F, Griffiths RD, Brodie DA, Jackson MJ (2003) Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J Physiol 549(2):645–652

    Article  CAS  Google Scholar 

  • Kishore A, Sodhi M, Kumari P, Mohanty AK, Sadana DK, Kapila N, Khate K, Shandilya U, Kataria RS, Mukesh M (2013) Peripheral blood mononuclear cells: a potential cellular system to understand differential heat shock response across native cattle (Bos indicus), exotic cattle (Bos taurus), and riverine buffaloes (Bubalus bubalis) of India. Cell Stress Chaperones 19(5):613–621

    Article  Google Scholar 

  • Kregel KC (2002) Molecular biology of thermoregulation. Invited review: heat shock protein: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2218

    Article  CAS  Google Scholar 

  • Lacetera N, Bernabucci U, Scalia D, Basirico 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  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Lauridsen C, Bertelsen G, Jakobsen K (1997) Will supplementation of vitamin C to poultry feed improve the quality of poultry meat? Meat Focus Int 54(11):185–186

    Google Scholar 

  • Lefcourt AM, Bitman J, Wood DL, Stroud B (1986) Radiotelemetry system for continuously monitoring temperature in cows. J Dairy Sci 69:237–242

    Article  CAS  Google Scholar 

  • Lei L, Yu J, Bao E (2009) Expression of heat shock protein 90 (Hsp90) and transcription of its corresponding mRNA in broilers exposed to high temperature. Br Poult Sci 50:504–511

    Article  CAS  Google Scholar 

  • Lin H, Decuypere E, Buyse J (2006) Acute heat stress induces oxidative stress in broiler chickens. Comp Biochem Physiol A Mol Integr Physiol 144:11–17

    Article  Google Scholar 

  • Lindquist S (1980) Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol 77(2):463–479

    Article  CAS  Google Scholar 

  • Mahmoud KZ, Edens FW, Eisen EJ, Havenstein GB (2004) Ascorbic acid decreases heat shock protein 70 and plasma corticosterone response in broilers (Gallus gallus domesticus) subjected to cyclic heat stress. Comp Biochem Physiol B 137:35–42

    Article  Google Scholar 

  • Maurya VP, Naqvi SMK, Joshi A, Mittal JP (2007) Effect of high temperature stress on physiological responses of Malpura sheep. Indian J Anim Sci 77:1244–1247

    Google Scholar 

  • Mcdowell LR (1989) Vitamins in animal nutrition. In: Mcdowell LR (ed) Comparative aspects to human nutrition. Vitamin E. Academic, London, pp 93–131

    Google Scholar 

  • Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288

    Article  CAS  Google Scholar 

  • Misurova L, Pavlata L, Pechova A, Dvorak R (2009) Effect of a long-term peroral supplementation with sodium selenite and selenium lactate-protein complex on selenium status in goats and their kids. Vet Med 52(7):324–332

    Google Scholar 

  • Morange F (2006) HSFs in development. Handb Exp Pharmacol 172:153–169

    Article  CAS  Google Scholar 

  • Mujahid A, Akiba Y, Warden CH, Toyomizu M (2007) Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat-stressed chickens. FEBS Lett 581:3461–3467

    Article  CAS  Google Scholar 

  • Na WW, Yue W, Wang A (2006) Effect of supplemental L-ascorbyl-2-polyphosphate (APP) in enriched live food on the immune response of Peaus vannamie exposed to ammoni –N. Aquaculture 256:552–557

    Article  Google Scholar 

  • Oksala NKJ, Laaksonen DE, Lappalainen J, Khanna S, Nakao C, Hänninen O, Sen CK, Atalay M (2006) Heat shock protein 60 response to exercise in diabetes. Effects of α-lipoic acid supplementation. J Diabetes Complicat 20:257–261

    Article  Google Scholar 

  • Omar R, Pappolla M (1993) Oxygen free radicals as inducers of heat shock protein synthesis in cultured human neuroblastoma cells: relevance to neurodegenerative disease. Eur Arch Psychiatry Clin Neurosci 242:262–267

    Article  CAS  Google Scholar 

  • Pagliaro P, Gattullo D, Rastaldo R, Losano G (2001) Ischemic preconditioning: from the first to the second window of protection. Life Sci 69:1–15

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real time RT-PCR. Nucleic Acid Res 29:2002–2007

    Article  Google Scholar 

  • Pratt WB (1993) The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J Biol Chem 268:21455–21458

    CAS  Google Scholar 

  • Prodromou C, Panaretou B, Chohan S, Siligardi G, O'Brien R, Ladbury JE, Roe SM, Piper PW, Pearl LH (2000) The ATPase cycle of Hsp90 drives a molecular'clamp'via transient dimerization of the N-terminal domains. EMBO J 19(16):4383–4392

    Article  CAS  Google Scholar 

  • Rivera RE, Christensen VL, Edens FW, Wineland MJ (2005) Influence of selenium on heat shock protein 70 expression in heat stressed turkey embryos (Meleagris gallopavo). Comp Biochem Physiol A 142:427–432

    Article  Google Scholar 

  • Robine JM, Cheung SLK, Roy SL, Oyen HV, Griffiths C, Michel JP, Herrmann FR (2008) Death toll exceeded 70,000 in Europe during the summer of 2003. C R Biol 331:171–178

    Article  Google Scholar 

  • Rosenberg LJ, Blad BL, Verma SB (1983) Human and animal biometeorology. In: Rosenberg LJ, Blad BL, Verma SB (eds) Microclimatethe biological environment. Wiley, New York

    Google Scholar 

  • Sahin K, Kucuk O (2003) Heat stress and dietary vitamin supplementation of poultry diets. Nutrition Abstracts and Reviews. Ser B Livest Feeds Feed 73:41R–50R

    Google Scholar 

  • Sahin N, Tuzcu M, Orhan C, Onderci M, Eroksuz Y, Sahin K (2009) The effects of vitamin C and E supplementation on heat shock protein 70 response of ovary and brain in heat-stressed quail. Br Poult Sci 50(2):259–265

    Article  CAS  Google Scholar 

  • Sharma S, Ramesh K, Hyder I, Uniyal S, Yadav VP, Panda RP, Maurya VP, Singh G, Kumar P, Mitra A, 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 Rumin Res 112:216–223

    Article  Google Scholar 

  • Silanikove N, Maltz E, Halevi A, Shinder D (1997) Metabolism of water, sodium, potassium and chloride by high yielding dairy cows at the onset of lactation. J Dairy Sci 80:949–956

    Article  CAS  Google Scholar 

  • Sivakumar AVN, Singh G, Varshney VP (2010) Antioxidants supplementation on acid base balance during heat stress in goats. Asian Australas J Anim Sci 23(11):1462–1468

    Article  CAS  Google Scholar 

  • Stott GH (1981) What is animal stress and how is it measured. J Anim Sci 52:150–153

    CAS  Google Scholar 

  • Tan GY, Yang L, Fu YQ, Feng JH, Zhang MH (2010) Effects of different acute high ambient temperatures on function of hepatic mitochondrial respiration, antioxidative enzymes, and oxidative injury in broiler chickens. Poult Sci 89:115–122

    Article  CAS  Google Scholar 

  • Topbas OF, Jehle R, Sinha P, Rüstow B (2000) An electrophoretic study of vitamin E status and expression of heat shock proteins in alveolar type II and liver cells. Electrophoresis 21(17):3552–3557

    Article  CAS  Google Scholar 

  • Yamagishi N, Nishihori H, Ishihara K, Ohtsuka K, Hatayama T (2000) Modulation of the chaperone activities of Hsc70/Hsp40 by Hsp105alpha and Hsp105beta. Biochem Biophys Res Commun 272:850–855

    Article  CAS  Google Scholar 

  • Yamagishi N, Ishihara K, Saito Y, Hatayama T (2003) Hsp105 but not Hsp70 family proteins suppress the aggregation of heat-denatured protein in the presence of ADP. FEBS Lett 555:390–396

    Article  CAS  Google Scholar 

  • Yasuda K, Nakai A, Hatayama T, Nagata K (1995) Cloning and expression of murine high molecular mass heat shock proteins, HSP105. J Biol Chem 270:29718–29723

    Article  CAS  Google Scholar 

  • Yellon DM, Baxter GF (1995) A second window of protection or delayed preconditioning phenomenon: future horizons for myocardial protection? J Cell Cardiol 27(4):1023–1034

    Article  CAS  Google Scholar 

  • Young RA (1990) Stress and immunology. Annu Rev Immunol 8:401–420

    Article  CAS  Google Scholar 

  • Zaytsev V, Sinev AB, Ionov PS, Sharabrin IG (1971) Clinical diagnosis of internal diseases of farm animals. Kolos, Moscow (in Russian)

    Google Scholar 

Download references

Acknowledgments

National Initiative on Climate Resilient Agriculture (NICRA), Indian Council of Agricultural Research (ICAR), funded the study.

Conflict of interest

None declared.

Author information

Authors and Affiliations

  1. Physiology and Climatology, Indian Veterinary Research Institute, Izatnagar, Bareilly, Uttar Pradesh, 243122, India

    Satyaveer Singh Dangi, Mahesh Gupta, Vikrant Singh Chouhan, V. P. Maurya, Puneet Kumar, Gyanendra Singh & Mihir Sarkar

  2. Division of Bacteriology and Mycology, Indian Veterinary Research Institute, Izatnagar, Bareilly, Uttar Pradesh, 243122, India

    Saroj K. Dangi

Authors
  1. Satyaveer Singh Dangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahesh Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saroj K. Dangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vikrant Singh Chouhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. P. Maurya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Puneet Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gyanendra Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mihir Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mihir Sarkar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dangi, S.S., Gupta, M., Dangi, S.K. et al. Expression of HSPs: an adaptive mechanism during long-term heat stress in goats (Capra hircus). Int J Biometeorol 59, 1095–1106 (2015). https://doi.org/10.1007/s00484-014-0922-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-014-0922-5

Keywords

Search

Navigation