Skip to main content

Advertisement

SpringerLink
Log in

Expression analysis of NOS family and HSP genes during thermal stress in goat (Capra hircus)

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

Abstract

Approximately 50 genes other than heat shock protein (HSP) expression changes during thermal stress. These genes like nitric oxide synthase (NOS) need proper attention and investigation to find out their possible role in the adaptation to thermal stress in animals. So, the present study was undertaken to demonstrate the expressions of inducible form type II NOS (iNOS), endothelial type III NOS (eNOS), constitutively expressed enzyme NOS (cNOS), HSP70, and HSP90 in peripheral blood mononuclear cells (PBMCs) during different seasons in Barbari goats. Real-time polymerase chain reaction, western blot, and immunocytochemistry were applied to investigate messenger RNA (mRNA) expression, protein expression, and immunolocalization of examined factors. The mRNA and protein expressions of iNOS, eNOS, cNOS, HSP70, and HSP90 were significantly higher (P < 0.05) during peak summer, and iNOS and eNOS expressions were also observed to be significantly higher (P < 0.05) during peak winter season as compared with moderate season. The iNOS, eNOS, cNOS, HSP70, and HSP90 were mainly localized in plasma membrane and cytoplasm of PBMCs. To conclude, data generated in the present study indicate the possible involvement of the NOS family genes in amelioration of thermal stress so as to maintain cellular integrity and homeostasis in goats.

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

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 

  • Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615

    Article  CAS  Google Scholar 

  • Ali EMM, Soha HM, Mohamed TM (2012) Nitric oxide synthase and oxidative stress: regulation of nitric oxide synthase. In: Volodymyr Lushchak (ed.) Oxidative stress—molecular mechanisms and biological effects. InTech, 61-72 ISBN: 978-953-51-0554-1

  • 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 

  • Bernabucci U, Biffani S, Buggiotti L, Vitali A, Lacetera N, Nardone A (2014) The effects of heat stress in Italian Holstein dairy cattle. J Dairy Sci 97(1):471–486

    Article  CAS  Google Scholar 

  • Bettaieb A, Averill-Bates DA (2008) Thermotolerance induced at a fever temperature of 40 degrees C protects cells against hyperthermia-induced apoptosis mediated by death receptor signalling. Biochem Cell Biol 86:521–538

    Article  CAS  Google Scholar 

  • Bogdan C (2001) Nitric oxide and the immune response. Nat Immunol 2:907–916

    Article  CAS  Google Scholar 

  • Coleman JW (2001) Nitric oxide in immunity and inflammation. Int Immunopharmacol 1:1397–1406

    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, Om S, Chouhan VS, Kumar P, Singh G, Sarkar M (2014a) Impact of short-term heat stress on physiological responses and expression profile of HSPs in Barbari goats. Int J Biometeorol 58(10):2085–2093

    Article  Google Scholar 

  • Dangi SS, Gupta M, Dangi SK, Chouhan VS, Maurya VP, Kumar P, Singh G, Sarkar M (2014b) Expression of HSPs: an adaptive mechanism during long-term heat stress in goats (Capra hircus). Int J Biometeorol. doi:10.1007/s00484-014-0922-5

    Google Scholar 

  • Drouin A, Thorin-Trescases N, Hamel E, Falck JR, Thorin E (2007) Endothelial nitric oxide synthase activation leads to dilatory H2O2 production in mouse cerebral arteries. Cardiovasc Res 73(1):73–81

    Article  CAS  Google Scholar 

  • Dubey PK, Tripathi V, Singh RP, Saikumar G, Nath A, Gade N, Sharma GT (2012) Expression of nitric oxide synthase isoforms in different stages of buffalo (Bubalus bubalis) ovarian follicles: effect of nitric oxide on in vitro development of preantral follicle. Theriogenology 77(2):280–291

    Article  CAS  Google Scholar 

  • Hauser GJ, Dayao EK, Wasserloose K, Pitt BR, Wong HR (1996) HSP induction inhibits iNOS RNA expression and attenuates hypotension in endotoxin-challenged rats. Am J Physiol 271:H2529–H2535

    CAS  Google Scholar 

  • Johnson JM, O’Leary DS, Taylor WF, Kosiba W (1986) Effect of local warming on forearm reactive hyperaemia. Clin Physiol 6:337–346

    Article  CAS  Google Scholar 

  • Kellogg D, Crandall C, Liu Y, Charkoudian N, Johnson J (1998) Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol 85:824–829

    CAS  Google Scholar 

  • Kellogg DL Jr, Liu Y, Kosiba IF, O’Donnell D (1999) Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol 86:1185–1190

    CAS  Google Scholar 

  • Kiang JG (2004) Inducible heat shock protein 70 kD and inducible nitric oxide synthase in hemorrhage/resuscitation-induced injury. Cell Res 14(6):450–459

    Article  CAS  Google Scholar 

  • Kiang JG, Bowman PD, Wu BW et al (2004) Geldanamycin treatment inhibits hemorrhage-induced increases in KLF6 and iNOS expression in un-resuscitated mouse organs: role of inducible HSP-70. J Appl Physiol 97:564–569

    Article  CAS  Google Scholar 

  • Malyshev IY, Bayda LA, Trifonov AI, Larionov NP, Kubrina LD, Mikoyan VD, Vanin AF, Manukhina EB (2000) Cross-talk between nitric oxide and HSP70 in the antihypotensive effect of adaptation to heat. Physiol Res 49:99–105

    CAS  Google Scholar 

  • Mangiafico RA, Malatino LS, Santonocito M, Spada RS, Tamburino G (1996) Plasma endothelin-1concentrations during cold exposure in essential acrocyanosis. Angiology 47:1033–1038

    Article  CAS  Google Scholar 

  • Marai IFM, Habeeb AAM (2010) Buffalo biological functions as affected by heat stress—a review. Livest Sci 127:89–109

    Article  Google Scholar 

  • Maurya D, Gupta M, Dangi SS, Yadav VP, Mahapatra RK, Sarkar M (2013) Expression of genes associated with thermal stress in goats during different seasons. Indian J Anim Sci 83(6):604–608

    Google Scholar 

  • Mc Ewen BS (2000) The neurobiology of stress from serendipity to clinical relevance. Brain Res 86:172–189

    Article  Google Scholar 

  • Meerson FZ, Malyshev IY (1993) Phenomenon of adaptive stabilization of structure and protection of heart. Nauka, Moscow (in Russian)

    Google Scholar 

  • Mehla K, Magotra A, Choudhary J, Singh AK, Mohanty AK, Upadhyay RC, Srinivasan S, Gupta P, Choudhary N, Antony B, Khan F (2013) Genome-wide analysis of the heat stress response in Zebu (Sahiwal) cattle. Gene. doi:10.1016/j.gene.2013.09.051

    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 

  • Mishra A, Hooda OK, Singh G, Meur SK (2010) Influence of induced heat stress on HSP70 in buffalo lymphocytes. J Anim Physiol Anim Nutr 95:540–544

    Article  Google Scholar 

  • Misra RP, Puneet K (2009) Improved shelter management, feeding and watering devices for goats. In: Kumar S, Sharma MC, Goel AK (eds) Goat enterprises. CIRG, Mathura, p 132

    Google Scholar 

  • Nathan C (1997) Inducible nitric oxide synthase: what difference does it make? J Clin Invest 100:2417–2423

    Article  CAS  Google Scholar 

  • Pergola PE, Kellogg DL Jr, Johnson JM, Kosiba WA (1993) Role of sympathetic nerves in the vascular effects of local temperature in human forearm skin. Am J Physiol 265:H785–H792, Heart Circ Physiol 34

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sharma HS, Drieu K, Alm P, Westman J (2000) Role of nitric oxide in blood–brain barrier permeability, brain edema and cell damage following hyperthermic brain injury. An experimental study using EGB-761 and Gingkolide B pretreatment in the rat. In: Brain edema XI. Springer, Vienna pp. 81–86

  • Sonna LA, Fujita J, Gaffin SL, Lilly CM (2002) Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742

    Article  CAS  Google Scholar 

  • Surh YJ, Chun KS, Cha HH, Han SS, Keum YS, Park KK, Lee SS (2001) Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-kappa B activation. Mutat Res 480–481:243–268

    Article  Google Scholar 

  • Taylor WF, Johnson JM, O’Leary D, Park MK (1984) Effect of high local temperature on reflex cutaneous vasodilation. J Appl Physiol 57:191–196

    CAS  Google Scholar 

  • Teshfam M, Brujeni GN, Hassanpour H (2006) Evaluation of endothelial and inducible nitric oxide synthase mRNA expression in the lung of broiler chickens with developmental pulmonary hypertension due to cold stress. Br Poult Sci 47:223–229

    Article  CAS  Google Scholar 

  • Wen JK, Han M (2000) Comparative study of induction of iNOS mRNA expression in vascular cells of different species. Biochem Mosc 65(12):1376–1379

    Article  CAS  Google Scholar 

  • Xu H, Yang S, Jingli W, Deron J, Dorothee W, Rong Y, Basam W, Kirkwood AP (2007) A heat shock protein 90 binding domain in endothelial nitric-oxide synthase influences enzyme function. J Biol Chem 282(52):37567–37574

    Article  CAS  Google Scholar 

  • Zhao FQ, Zhang ZW, Wang C, Zhang B, Yao HD, Li S, Xu SW (2013) The role of heat shock proteins in inflammatory injury induced by cold stress in chicken hearts. Cell Stress Chaperones 18:773–783

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledged funds received from NAIP, Indian Council of Agricultural Research and Director, IVRI.

Conflict of interest

None.

Author information

Authors and Affiliations

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

    Vijay Pratap Yadav, Satyaveer Singh Dangi, Vikrant Singh Chouhan, Mahesh Gupta, Gyanendra Singh, Vijay Prakash Maurya, Puneet Kumar & Mihir Sarkar

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

    Saroj K. Dangi

Authors
  1. Vijay Pratap Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Satyaveer Singh Dangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vikrant Singh Chouhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mahesh Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saroj K. Dangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gyanendra Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vijay Prakash Maurya
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Puneet Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. 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

Yadav, V.P., Dangi, S.S., Chouhan, V.S. et al. Expression analysis of NOS family and HSP genes during thermal stress in goat (Capra hircus). Int J Biometeorol 60, 381–389 (2016). https://doi.org/10.1007/s00484-015-1035-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-015-1035-5

Keywords

Search

Navigation