Skip to main content
SpringerLink
Log in

Effects of Oxidative Stress on Immunosuppression Induced by Selenium Deficiency in Chickens

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Selenium (Se) is an important nutritional trace element possessing immune-stimulatory properties. The aim of this 75-day study was to investigate effect of oxidative stress on immunosuppression induced by selenium deficiency by determining antioxidative function, morphological changes, DNA damage, and immune function in immune organ of chickens. One hundred sixty 1-day-old chickens (egg-type birds) were randomly assigned to two groups of 80 each and were fed on a low-Se diet (0.032 mg/kg Se) or a control diet (0.282 mg/kg Se, sodium selenite), respectively. Se contents in blood and immune organ (thymus, spleen, bursa of Fabricius) were determined on days 30, 45, 60, and 75, respectively. Antioxidative function was examined by total antioxidant capacity (T-AOC), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px), and xanthine oxidase (XOD), and oxidative damage was examined by malondialdehyde (MDA) detection. DNA damage was measured by comet assay, and immune function was examined by determining serum interleukin-1β (IL-1β), interleukin-2 (IL-2), and tumor necrosis factor (TNF) contents. The results showed that Se concentrations in the low-Se group were significantly lower (P < 0.05) than in the control group. Low-Se diet caused a decrease in the activities of T-AOC, SOD, GSH-Px, and an increase in XOD activity and MDA content. Pathological lesions and DNA damage of immune tissues were observed in low-Se group, while the serum IL-1β and IL-2 contents decreased, and TNF content increased. The present study demonstrated that chickens fed deficient in Se diets exhibited lesions in immune organs, decreased serum IL-1β, IL-2 content, and serum TNF content, indicating that oxidative stress inhibited the development of immune organs and finally impaired the immune function of chickens.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Carlson BA, Yoo MH, Shrimali RK et al (2010) Role of selenium-containing proteins in T-cell and macrophage function. Proc Nutr Soc 69:300–310

    Article  PubMed  CAS  Google Scholar 

  2. Li JL, Li HX, Li S et al (2011) Selenoprotein W gene expression in the gastrointestinal tract of chicken is affected by dietary selenium. Biometals 24:291–299

    Article  PubMed  CAS  Google Scholar 

  3. Diplock AT (1987) Dietary supplementation with antioxidants. Is there a case for exceeding the recommended dietary allowance. Free Radic Biol Med 3:199–201

    Article  PubMed  CAS  Google Scholar 

  4. Rayman MP (2000) The importance of selenium to human health. Lancet 356:233–241

    Article  PubMed  CAS  Google Scholar 

  5. Jayaprakash V, Marshall JR (2011) Selenium and other antioxidants for chemoprevention of gastrointestinal cancers. Best Pract Res Clin Gastroenterol 25:507–518

    Article  PubMed  CAS  Google Scholar 

  6. Kaushal N, Bansal MP (2007) Dietary selenium variation-induced oxidative stress modulates CDC2/cyclin B1 expression and apoptosis of germ cells in mice testis. J Nutr Biochem 18:553–564

    Article  PubMed  CAS  Google Scholar 

  7. Hadley KB, Sunde RA (2001) Selenium regulation of thioredoxin reductase activity and mRNA levels in rat liver. J Nutr Biochem 12:693–702

    Article  PubMed  CAS  Google Scholar 

  8. Singh K, Ahluwalia P (2012) Effect of monosodium glutamate on lipid peroxidation and certain antioxidantenzymes in cardiac tissue of alcoholic adult male mice. J Cardiovasc Dis Res 3:12–18

    Article  PubMed  CAS  Google Scholar 

  9. Bhaskaram P (2002) Micronutrient malnutrition, infection, and immunity: an overview. Nutr Rev 60:S40–S45

    Article  PubMed  Google Scholar 

  10. Brown KM, Arthur JR (2001) Selenium, selenoproteins and human health: a review. Public Health Nutr 4:593–599

    Article  PubMed  CAS  Google Scholar 

  11. Gromer S, Eubel JK, Lee BL et al (2005) Human selenoproteins at a glance. Cell Mol Life Sci 62:2414–2437

    Article  PubMed  CAS  Google Scholar 

  12. McKenzie RC, Rafferty TS, Beckett GJ (1998) Selenium: an essential element for immune function. Immunol Today 19:342–345

    Article  PubMed  CAS  Google Scholar 

  13. Kiremidjian-Schumacher L, Roy M (1998) Selenium and immune function. Z Ernährungswiss 37(Suppl 1):50–56

    PubMed  CAS  Google Scholar 

  14. Chan S, Gerson B, Subramaniam S (1998) The role of copper, molybdenum, selenium, and zinc in nutrition and health. Clin Lab Med 18:673–685

    PubMed  CAS  Google Scholar 

  15. Winnefeld K (1997) Selenium, antioxidant status and radical/reactive oxygen species in medicine. Med Klin (Munich) 92(Suppl 3):8–10

    Article  CAS  Google Scholar 

  16. Pighetti GM, Eskew ML, Reddy CC et al (1998) Selenium and vitamin E deficiency impair transferrin receptor internalization but not IL-2, IL-2 receptor, or transferrin receptor expression. J Leukoc Biol 63:131–137

    PubMed  CAS  Google Scholar 

  17. Hasunuma R, Ogawa T, Kawanishi Y (1982) Fluorometric determination of selenium in nanogram amounts in biological materials using 2,3-diaminonaphthalene. Anal Biochem 126:242–245

    Article  PubMed  CAS  Google Scholar 

  18. Opara EC, Abdel-Rahman E, Soliman S et al (1999) Depletion of total antioxidant capacity in type 2 diabetes. Metabolism 48:1414–1417

    Article  PubMed  CAS  Google Scholar 

  19. Rotruck JT, Pope AL, Ganther HE et al (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590

    Article  PubMed  CAS  Google Scholar 

  20. Zhang ZW, Lv ZH, Li JL et al (2011) Effects of cold stress on nitric oxide in duodenum of chicks. Poult Sci 90:1555–1561

    Article  PubMed  CAS  Google Scholar 

  21. Montufar-Solis D, Klein JR (2006) An improved method for isolating intraepithelial lymphocytes (IELs) from the murine small intestine with consistently high purity. J Immunol Methods 308:251–254

    Article  PubMed  CAS  Google Scholar 

  22. Singh NP, McCoy MT, Tice RR et al (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  PubMed  CAS  Google Scholar 

  23. Zhang XY, Zhou DF, Cao LY et al (2002) Decreased production of interleukin-2 (IL-2), IL-2 secreting cells and CD4+ cells in medication-free patients with schizophrenia. J Psychiatr Res 36:331–336

    Article  PubMed  Google Scholar 

  24. Hsieh HS, Ganther HE (1975) Acid-volatile selenium formation catalyzed by glutathione reductase. Biochemistry 14:1632–1636

    Article  PubMed  CAS  Google Scholar 

  25. Bjornstedt M, Kumar S, Holmgren A (1992) Selenodiglutathione is a highly efficient oxidant of reduced thioredoxin and a substrate for mammalian thioredoxin reductase. J Biol Chem 267:8030–8034

    PubMed  CAS  Google Scholar 

  26. Veres Z, Kim IY, Scholz TD et al (1994) Selenophosphate synthetase. Enzyme properties and catalytic reaction. J Biol Chem 269:10597–10603

    PubMed  CAS  Google Scholar 

  27. Ferreccio C, Gonzalez PC, Milosavjlevic SV et al (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 

  28. Papp LV, Lu J, Holmgren A et al (2007) From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 9:775–806

    Article  PubMed  CAS  Google Scholar 

  29. Sunde RA, Hadley KB (2010) Phospholipid hydroperoxide glutathione peroxidase (Gpx4) is highly regulated inmale turkey poults and can be used to determine dietary selenium requirements. Exp Biol Med (Maywood) 235:23–31

    Article  CAS  Google Scholar 

  30. Bozkaya LA, Ozturk-Urek R, Aydemir T et al (2001) Effects of Se, Cu and Se + vitamin E deficiency on the activities of CuZnSOD, GSH-Px, CAT and LPO levels in chicken erythrocytes. Cell Biochem Funct 19:153–157

    Article  PubMed  CAS  Google Scholar 

  31. Jun EJ, Ye JS, Hwang IS et al (2011) Selenium deficiency contributes to the chronic myocarditis in coxsackievirus-infected mice. Acta Virol 55:23–29

    Article  PubMed  CAS  Google Scholar 

  32. Zuberbuehler CA, Messikommer RE, Arnold MM et al (2006) Effects of selenium depletion and selenium repletion by choice feeding on selenium status of young and old laying hens. Physiol Behav 87:430–440

    Article  PubMed  CAS  Google Scholar 

  33. Xu JX, Wang J, Wang T (2007) Effects of vitamin E and selenium on the metabolism of free radicals in broilers. Ying Yong Sheng Tai Xue Bao 18:1789–1793

    PubMed  CAS  Google Scholar 

  34. Thomson CD, Chisholm A, McLachlan SK et al (2008) Brazil nuts: an effective way to improve selenium status. Am J Clin Nutr 87:379–384

    PubMed  CAS  Google Scholar 

  35. Rayman MP (2000) The importance of selenium to human health. Lancet 356:233–241

    Article  PubMed  CAS  Google Scholar 

  36. Cooke MS, Olinski R, Evans MD (2006) Does measurement of oxidative damage to DNA have clinical significance. Clin Chim Acta 365:30–49

    Article  PubMed  CAS  Google Scholar 

  37. Avanzo JL, de Mendonca CX, Jr PSM et al (2001) Effect of vitamin E and selenium on resistance to oxidative stress in chicken superficial pectoralis muscle. Comp Biochem Physiol C Toxicol Pharmacol 129:163–173

    Article  PubMed  CAS  Google Scholar 

  38. Collins AR (2004) The comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26:249–261

    Article  PubMed  CAS  Google Scholar 

  39. Peng X, Cui Y, Cui W et al (2011) The cell cycle arrest and apoptosis of bursa of Fabricius induced by low selenium in chickens. Biol Trace Elem Res 139:32–40

    Article  PubMed  CAS  Google Scholar 

  40. Harbige LS (1996) Nutrition and immunity with emphasis on infection and autoimmune disease. Nutr Health 10:285–312

    Article  PubMed  CAS  Google Scholar 

  41. Kiremidjian-Schumacher L, Roy M, Wishe HI et al (1994) Supplementation with selenium and human immune cell functions II. Effect on cytotoxic lymphocytes and natural killer cells. Biol Trace Elem Res 41:115–127

    Article  PubMed  CAS  Google Scholar 

  42. Sobolev SM, Nikolaeva TN, Pronin AV (2011) “Non-immune” interactions of gamma-globulin in regulation of immune reactions. Vestn Ross Akad Med Nauk 10:60–62

    PubMed  Google Scholar 

  43. Brigelius-Flohe R, Banning A, Kny M et al (2004) Redox events in interleukin-1 signaling. Arch Biochem Biophys 423:66–73

    Article  PubMed  CAS  Google Scholar 

  44. Bonham M, O'Connor JM, Hannigan BM et al (2002) The immune system as a physiological indicator of marginal copper status. Br J Nutr 87:393–403

    Article  PubMed  CAS  Google Scholar 

  45. Sethi G, Sung B, Aggarwal BB (2008) TNF: a master switch for inflammation to cancer. Front Biosci 13:5094–5107

    Article  PubMed  CAS  Google Scholar 

  46. Johnson VJ, Tsunoda M, Sharma RP (2000) Increased production of proinflammatory cytokines by murine macrophages following oral exposure to sodium selenite but not to seleno-l-methionine. Arch Environ Contam Toxicol 39:243–250

    Article  PubMed  CAS  Google Scholar 

  47. Maddox JF, Aherne KM, Reddy CC et al (1999) Increased neutrophil adherence and adhesion molecule mRNA expression in endothelial cells during selenium deficiency. J Leukoc Biol 65:658–664

    PubMed  CAS  Google Scholar 

  48. Peng X, Cui H, Yuan J et al (2011) Low-selenium diet induces cell cycle arrest of thymocytes and alters serum IL-2 content in chickens. Biol Trace Elem Res 144:688–694

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (30871902) and the Science Foundation of the Education Department of Heilongjiang Province (11551030). The authors thank the members of the veterinary internal medicine laboratory, especially the members of the cold stress group, in College of Veterinary Medicine, Northeast Agricultural University for 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

    Zi-wei Zhang, Qiao-hong Wang, Shu Li & Shi-wen Xu

  2. Heilongjiang Vocational Institute of Science and Technology, Shuangcheng, 150100, People’s Republic of China

    Jiu-li Zhang

  3. Wildlife Resource College, Northeast Forestry University, 26 Hexing Road, Xiangfang District, Harbin, 150040, People’s Republic of China

    Xiao-Long Wang

Authors
  1. Zi-wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiao-hong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiu-li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiao-Long Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shi-wen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiao-Long Wang 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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Zw., Wang, Qh., Zhang, Jl. et al. Effects of Oxidative Stress on Immunosuppression Induced by Selenium Deficiency in Chickens. Biol Trace Elem Res 149, 352–361 (2012). https://doi.org/10.1007/s12011-012-9439-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-012-9439-0

Keywords

Search

Navigation