Skip to main content
SpringerLink
Log in

Cold stress induces antioxidants and Hsps in chicken immune organs

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

Abstract

The aim of this study was to investigate the effects of cold stress on oxidative indexes, immune function, and the expression levels of heat shock protein (Hsp90, Hsp70, Hsp60, Hsp40, and Hsp27) in immune organs of chickens. Two hundred forty 15-day-old male chickens were randomly divided into 12 groups and kept under the temperature of (12 ± 1) °C for acute and chronic cold stress. There were one control group and five treatment groups for acute cold stress and three control groups and three treatment groups for chronic cold stress. The results showed that cold stress influence the activities of antioxidant enzymes in the immune organs. The activities of SOD and GSH-Px were first increased then decreased, and activity of total antioxidation capacity (T-AOC) was significantly decreased (P < 0.05) at the acute cold stress in chicks; however, T-AOC activities were significantly increased (P < 0.05) at the chronic cold stress in these tissues. Cold stress induced higher level of malondialdehyde (MDA) in chicken immune organs. In addition, the cytokine contents were increased in cold stress groups. As one protective factor, the expression levels of Hsps were increased significantly (P < 0.05) in both cold stress groups. These results suggested that cold stress induced the oxidative stress in the three tissues and influenced immune function of chicks. Higher expression of Hsps (Hsp90, Hsp70, Hsp60, Hsp40, and Hsp27) may play a role in protecting immune organs against cold 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

  • Al-Aqil A, Zulkifli I (2009) Changes in heat shock protein 70 expression and blood characteristics in transported broiler chickens as affected by housing and early age feed restriction. Poult Sci 88(7):1358–1364

    Article  CAS  PubMed  Google Scholar 

  • Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88(1):287–332

    Article  CAS  PubMed  Google Scholar 

  • Ausiello CM, Palazzo R, Spensieri F, Fedele G, Lande R, Ciervo A, Fioroni G, Cassone A (2005) 60-kDa heat shock protein of Chlamydia pneumoniae is a target of T-cell immune response. J Biol Regul Homeost Agents 19(3–4):136–140

    CAS  PubMed  Google Scholar 

  • Bottje WG, Wang S, Beers KW, Cawthon D (1998) Lung lining fluid antioxidants in male broilers: age-related changes under thermoneutral and cold temperature conditions. Poult Sci 77(12):1905–1912

    Article  CAS  PubMed  Google Scholar 

  • Brenner IK, Castellani JW, Gabaree C, Young AJ, Zamecnik J, Shephard RJ, Shek PN (1999) Immune changes in humans during cold exposure: effects of prior heating and exercise. J Appl Physiol (1985) 87(2):699–710

    CAS  Google Scholar 

  • Chang CK, Huang HY, Tseng HF, Hsuuw YD, Tso TK (2007) Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. J Nutr Biochem 18(1):39–45

    Article  CAS  PubMed  Google Scholar 

  • Ellis RJ (1990) The molecular chaperone concept. Semin Cell Biol 1(1):1–9

    CAS  PubMed  Google Scholar 

  • Felten SY, Madden KS, Bellinger DL, Kruszewska B, Moynihan JA, Felten DL (1998) The role of the sympathetic nervous system in the modulation of immune responses. Adv Pharmacol 42:583–587

    Article  CAS  PubMed  Google Scholar 

  • Ferreccio C, Gonzalez Psych C, Milosavjlevic Stat V, Marshall Gredis G, Sancha AM (1998) Lung cancer and arsenic exposure in drinking water: a case–control study in northern Chile. Cad Saude Publica 14(Suppl 3):193–198

    Article  PubMed  Google Scholar 

  • Fleshner M, Nguyen KT, Cotter CS, Watkins LR, Maier SF (1998) Acute stressor exposure both suppresses acquired immunity and potentiates innate immunity. Am J Physiol 275(3 Pt 2):R870–R878

    CAS  PubMed  Google Scholar 

  • Gu XH, Hao Y, Wang XL (2012) Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poult Sci 91:790–799

    Article  CAS  PubMed  Google Scholar 

  • Guo S, Wharton W, Moseley P, Shi H (2007) Heat shock protein 70 regulates cellular redox status by modulating glutathione-related enzyme activities. Cell Stress Chaperones 12(3):245–254

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Habich C, Burkart V (2007) Heat shock protein 60: regulatory role on innate immune cells. Cell Mol Life Sci 64(6):742–751

    Article  CAS  PubMed  Google Scholar 

  • Hamdoun AM, Cheney DP, Cherr GN (2003) Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biol Bull 205(2):160–169

    Article  CAS  PubMed  Google Scholar 

  • Hangalapura BN, Nieuwland MG, de Vries RG, Heetkamp MJ, van den Brand H, Kemp B, Parmentier HK (2003) Effects of cold stress on immune responses and body weight of chicken lines divergently selected for antibody responses to sheep red blood cells. Poult Sci 82(11):1692–1700

    Article  CAS  PubMed  Google Scholar 

  • Hangalapura BN, Nieuwland MG, Buyse J, Kemp B, Parmentier HK (2004a) Effect of duration of cold stress on plasma adrenal and thyroid hormone levels and immune responses in chicken lines divergently selected for antibody responses. Poult Sci 83(10):1644–1649

    Article  CAS  PubMed  Google Scholar 

  • Hangalapura BN, Nieuwland MG, de Vries RG, van den Brand H, Kemp B, Parmentier HK (2004b) Durations of cold stress modulates overall immunity of chicken lines divergently selected for antibody responses. Poult Sci 83(5):765–775

    Article  CAS  PubMed  Google Scholar 

  • Hangalapura BN, Kaiser MG, Poel JJ, Parmentier HK, Lamont SJ (2006) Cold stress equally enhances in vivo pro-inflammatory cytokine gene expression in chicken lines divergently selected for antibody responses. Dev Comp Immunol 30(5):503–511

    Article  CAS  PubMed  Google Scholar 

  • Hao Y, Gu XH, Wang XL (2012) Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 1. Intestinal structure and digestive function. Poult Sci 91:781–789

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Martin J, Neupert W (1992) Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Biophys Biomol Struct 21:293–322

    Article  CAS  PubMed  Google Scholar 

  • Helmreich DL, Parfitt DB, Lu XY, Akil H, Watson SJ (2005) Relation between the hypothalamic-pituitary-thyroid (HPT) axis and the hypothalamic-pituitary-adrenal (HPA) axis during repeated stress. Neuroendocrinology 81(3):183–192

    Article  CAS  PubMed  Google Scholar 

  • Jaattela M (1999) Escaping cell death: survival proteins in cancer. Exp Cell Res 248(1):30–43

    Article  CAS  PubMed  Google Scholar 

  • Jansky L, Pospisilova D, Honzova S, Ulicny B, Sramek P, Zeman V, Kaminkova J (1996) Immune system of cold-exposed and cold-adapted humans. Eur J Appl Physiol Occup Physiol 72(5–6):445–450

    Article  CAS  PubMed  Google Scholar 

  • Jia HY, Li JM, Yu Q, Wang JJ, Li S (2009) The effect of cold stress on DNA oxidative damage of lung in chicken. Zhongguo Ying Yong Sheng Li Xue Za Zhi 25(3):373–376

    CAS  PubMed  Google Scholar 

  • Kadiiska MB, Gladen BC, Baird DD, Germolec D, Graham LB, Parker CE, Nyska A, Wachsman JT, Ames BN, Basu S, Brot N, Fitzgerald GA, Floyd RA, George M, Heinecke JW, Hatch GE, Hensley K, Lawson JA, Marnett LJ, Morrow JD, Murray DM, Plastaras J, Roberts LJ 2nd, Rokach J, Shigenaga MK, Sohal RS, Sun J, Tice RR, Van Thiel DH, Wellner D, Walter PB, Tomer KB, Mason RP, Barrett JC (2005) Biomarkers of oxidative stress study II: are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radic Biol Med 38(6):698–710

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Curetty L, Corry PM (1991) Differences in preferential synthesis and redistribution of HSP70 and HSP28 families by heat or sodium arsenite in Chinese hamster ovary cells. J Cell Physiol 149(1):77-87.

    Google Scholar 

  • Li J, Qian X, Sha B (2009) Heat shock protein 40: structural studies and their functional implications. Protein Pept Lett 16(6):606–612

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Q, Zhang M, Chen YJ, Wang YJ, Huang F, Liu J (2011) Oxidative damage and HSP70 expression in masseter muscle induced by psychological stress in rats. Physiol Behav 104(3):365–372

    Article  CAS  PubMed  Google Scholar 

  • Liao F, Andalibi A, Qiao JH, Allayee H, Fogelman AM, Lusis AJ (1994) Genetic evidence for a common pathway mediating oxidative stress, inflammatory gene induction, and aortic fatty streak formation in mice. J Clin Invest 94(2):877–884

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin H, Decuypere E, Buyse J (2004) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol B: Biochem Mol Biol 139(4):745–751

    Article  CAS  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  • Lucca G, Comim CM, Valvassori SS, Reus GZ, Vuolo F, Petronilho F, Dal-Pizzol F, Gavioli EC, Quevedo J (2009) Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 54(5–6):358–362

    Article  CAS  PubMed  Google Scholar 

  • Moller P, Wallin H, Knudsen LE (1996) Oxidative stress associated with exercise, psychological stress and life-style factors. Chem Biol Interact 102(1):17–36

    Article  CAS  PubMed  Google Scholar 

  • Monari M, Foschi J, Rosmini R, Marin MG, Serrazanetti GP (2011) Heat shock protein 70 response to physical and chemical stress in Chamelea gallina. J Exp Mar Biol Ecol 397(2):71–78

    Article  CAS  Google Scholar 

  • Monroy FP, Banerjee SK, Duong T, Aviles H (1999) Cold stress-induced modulation of inflammatory responses and intracerebral cytokine mRNA expression in acute murine toxoplasmosis. J Parasitol 85(5):878–886

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259(5100):1409–1410

    Article  CAS  PubMed  Google Scholar 

  • Mujahid A (2010) Acute cold-induced thermogenesis in neonatal chicks (Gallus gallus). Comp Biochem Physiol A Mol Integr Physiol 156(1):34–41

    Article  PubMed  Google Scholar 

  • Mujahid A, Furuse M (2009) Oxidative damage in different tissues of neonatal chicks exposed to low environmental temperature. Comp Biochem Physiol A Mol Integr Physiol 152(4):604–608

    Article  PubMed  Google Scholar 

  • Onderci M, Sahin N, Sahin K, Kilic N (2003) Antioxidant properties of chromium and zinc: in vivo effects on digestibility, lipid peroxidation, antioxidant vitamins, and some minerals under a low ambient temperature. Biol Trace Elem Res 92(2):139–150

    Article  CAS  PubMed  Google Scholar 

  • Opara EC, Abdel-Rahman E, Soliman S, Kamel WA, Souka S, Lowe JE, Abdel-Aleem S (1999) Depletion of total antioxidant capacity in type 2 diabetes. Metabolism 48(11):1414–1417

    Article  CAS  PubMed  Google Scholar 

  • Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31(14):e73

    Article  PubMed Central  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Regnier JA, Kelley KW (1981) Heat- and cold-stress suppresses in vivo and in vitro cellular immune responses of chickens. Am J Vet Res 42(2):294–299

    CAS  PubMed  Google Scholar 

  • Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179(4073):588–590

    Article  CAS  PubMed  Google Scholar 

  • Rybakina EG, Shanin SN, Kozinets IA, Fomicheva EE, Korneva EA (1997) Cellular mechanisms of cold stress-related immunosuppression and the action of interleukin 1. Int J Tissue React 19(3–4):135–140

    CAS  PubMed  Google Scholar 

  • Sahin E, Gumuslu S (2004) Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 48(4):165–171

    Article  CAS  PubMed  Google Scholar 

  • Sesti-Costa R, Ignacchiti MD, Chedraoui-Silva S, Marchi LF, Mantovani B (2012) Chronic cold stress in mice induces a regulatory phenotype in macrophages: correlation with increased 11beta-hydroxysteroid dehydrogenase expression. Brain Behav Immun 26(1):50–60

    Article  CAS  PubMed  Google Scholar 

  • Sima P, Cervinkova M, Funda DP, Holub M (1998) Enhancement by mild cold stress of the antibody forming capacity in euthymic and athymic hairless mice. Folia Microbiol (Praha) 43(5):521–523

    Article  CAS  Google Scholar 

  • Sreedhar AS, Csermely P (2004) Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy: a comprehensive review. Pharmacol Ther 101(3):227–257

    Article  CAS  PubMed  Google Scholar 

  • Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85(6):905–910

    Article  CAS  PubMed  Google Scholar 

  • Tu ZZ, Wang KK, Zou J, Liu K, Deng GH, Xiao XZ (2005) Oxidative stress-induced accumulation of heat shock protein 70 within nucleolus. Zhong Nan Da Xue Xue Bao Yi Xue Ban 30:384–389

    CAS  PubMed  Google Scholar 

  • Tupling AR, Bombardier E, Vigna C, Quadrilatero J, Fu M (2008) Interaction between Hsp70 and the SR Ca2+ pump: a potential mechanism for cytoprotection in heart and skeletal muscle. Appl Physiol Nutr Metab 33(5):1023–1032

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Xu SW (2008) Effects of Cold Stress on the Messenger Ribonucleic Acid Levels of Corticotrophin-Releasing Hormone and Thyrotropin-Releasing Hormone in Hypothalami of Broilers. Poult Sci 87(5):973–978

    Article  CAS  PubMed  Google Scholar 

  • Wang JT, Li S, Li JL, Zhang JW, Xu SW (2009) Effects of cold stress on the messenger ribonucleic acid levels of peroxisome proliferator-activated receptor- in spleen, thymus, and bursa of Fabricius of chickens. Poult Sci 88(12):2549–2554

    Article  CAS  PubMed  Google Scholar 

  • Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZW, Lv ZH, Li JL, Li S, Xu SW, Wang XL (2011) Effects of cold stress on nitric oxide in duodenum of chicks. Poult Sci 90(7):1555–1561

    Article  CAS  PubMed  Google Scholar 

  • Zhao FQ, Zhang ZW, Yao HD, Wang LL, Liu T, Yu XY, Li S, Xu SW (2013a) Effects of cold stress on mRNA expression of immunoglobulin and cytokine in the small intestine of broilers. Res Vet Sci 95(1):146–155

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by technological innovation projects special funds of Harbin, China (no. 2010RFXXN041). The authors thank the members in the veterinary internal medicine laboratory, especially the members of the cold stress group, at College of Veterinary Medicine, Northeast Agricultural University (Harbin, China) for the help in feeding the chicks and analyzing the data.

Author information

Authors and Affiliations

  1. Department of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Fu Qing Zhao, Zi Wei Zhang, Jian Ping Qu, Hai Dong Yao, Ming Li, Shu Li & Shi Wen Xu

  2. College of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Shu Li & Shi Wen Xu

Authors
  1. Fu Qing Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zi Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian Ping Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hai Dong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ming Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shi Wen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shu Li or Shi Wen Xu.

Additional information

All authors have read the manuscript and have agreed to submit it in its current form for consideration for publication in the Journal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, F.Q., Zhang, Z.W., Qu, J.P. et al. Cold stress induces antioxidants and Hsps in chicken immune organs. Cell Stress and Chaperones 19, 635–648 (2014). https://doi.org/10.1007/s12192-013-0489-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-013-0489-9

Keywords

Search

Navigation