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Selenium Deficiency Downregulates Selenoproteins and Suppresses Immune Function in Chicken Thymus

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Abstract

Selenoproteins and selenium (Se) play important roles in the immune system. Selenoprotein expression in the immune system of mammals is sensitive to dietary Se levels; however, little is known about the expression of selenoproteins and their immune functions in the chicken thymus. We assessed selenoprotein gene expression and cytokine content in the chicken thymus in this study. The animals were randomly assigned to two groups as follows: the Se-deficient group (L group) was fed a diet containing 0.033 mg Se/Kg, and the control group was fed the same basal diet supplemented with Se at 0.15 mg/kg (sodium selenite). Real-time qPCR was used to investigate the expression level of selenoproteins on days 15, 25, 35, 45, and 55, and ELISA was used to evaluate the cytokine content on days 15, 35, and 55. The messenger RNA (mRNA) levels of Txnrd1, Txnrd2, Txnrd3, Dio1, Dio2, Dio3, GPx1, GPx2, GPx3, Gpx4, Sepp1, Selo, Sep15, Sepx1, Sels, Seli, Selu, Selh, and SPS2 were all significantly decreased (P < 0.05) in the L group compared to the control group. A significant decrease in IL-2, IL-10, IL-17, IL-1β, IFN-α, and IFN-β was observed in the L group, and there was also a significant increase in IL-6, IL-8, IFN-γ, and TNF-α in the L group. In summary, Se deficiency results in significant changes in the expression of selenoproteins, which may cause oxidative stress in the chicken thymus tissue. Moreover, immunological changes and immune stress may occur because of Se deficiency in the chicken thymus.

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References

  1. Loflin J, Lopez N, Whanger PD et al (2006) Selenoprotein W during development and oxidative stress. J Inorg Biochem 100:1679–1684

    Article  CAS  PubMed  Google Scholar 

  2. Zhang ZW, Wang QH, Zhang JL et al (2012) Effects of oxidative stress on immunosuppression induced by selenium deficiency in chickens. Biol Trace Elem Res 149:352–361

    Article  CAS  PubMed  Google Scholar 

  3. Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16:705–743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. You L, Liu C, Yang ZJ et al (2014) Prediction of selenoprotein T structure and its response to selenium deficiency in chicken immune organs. Biol Trace Elem Res 160:222–231

    Article  CAS  PubMed  Google Scholar 

  5. Kryukov GV, Castellano S, Novoselov SV et al (2003) Characterization of mammalian selenoproteomes. Science 300:1439–1443

    Article  CAS  PubMed  Google Scholar 

  6. Mariotti M, Ridge PG, Zhang Y et al (2012) Composition and evolution of the vertebrate and mammalian selenoproteomes. PLoS One 7:e33066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Yao HD, Liu W, Zhao WC et al (2014) Different responses of selenoproteins to the altered expression of selenoprotein W in chicken myoblasts. Rsc Adv 4:64032–64042

    Article  CAS  Google Scholar 

  8. Yao HD, Wu Q, Zhang ZW et al (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of se-deficient chicks. J Nutr 143:613–619

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Yao HD, Wu Q, Zhang ZW et al (2013) Selenoprotein W serves as an antioxidant in chicken myoblasts. Biochim Biophys Acta 1830:3112–3120

    Article  CAS  PubMed  Google Scholar 

  10. Lin SL, Wang CW, Tan SR et al (2014) Selenium deficiency inhibits the conversion of thyroidal thyroxine (T4) to triiodothyronine (T3) in chicken thyroids. Biol Trace Elem Res 161:263–271

    Article  CAS  PubMed  Google Scholar 

  11. Zhao X, Yao H, Fan R et al (2014) Selenium deficiency influences nitric oxide and selenoproteins in pancreas of chickens. Biol Trace Elem Res 161:341–349

    Article  CAS  PubMed  Google Scholar 

  12. Liang Y, Lin SL, Wang CW et al (2014) Effect of selenium on selenoprotein expression in the adipose tissue of chickens. Biol Trace Elem Res 160:41–48

    Article  CAS  PubMed  Google Scholar 

  13. 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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  15. Sheng PF, Jiang Y, Zhang ZW et al (2014) The effect of Se-deficient diet on gene expression of inflammatory cytokines in chicken brain. Biometals 27:33–43

    Article  CAS  PubMed  Google Scholar 

  16. Pappas AC, Zoidis E, Surai PF et al (2008) Selenoproteins and maternal nutrition. Comp Biochem Physiol B Biochem Mol Biol 151:361–372

    Article  CAS  PubMed  Google Scholar 

  17. Lescure A, Rederstorff M, Krol A et al (2009) Selenoprotein function and muscle disease. Biochim Biophys Acta 1790:1569–1574

    Article  CAS  PubMed  Google Scholar 

  18. Hoffmann PR (2008) Selenium and asthma: a complex relationship. Allergy 63:854–856

    Article  CAS  PubMed  Google Scholar 

  19. Liu CP, Fu J, Lin SL et al (2014) Effects of dietary selenium deficiency on mRNA levels of twenty-one selenoprotein genes in the liver of layer chicken. Biol Trace Elem Res 159:192–198

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Kim KH, Gao Y, Walder K et al (2007) SEPS1 protects RAW264.7 cells from pharmacological ER stress agent-induced apoptosis. Biochem Biophys Res Commun 354:127–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Ye Y, Shibata Y, Yun C et al (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429:841–847

    Article  CAS  PubMed  Google Scholar 

  23. Yao H, Zhao W, Zhao X et al (2014) Selenium deficiency mainly influences the gene expressions of antioxidative selenoproteins in chicken muscles. Biol Trace Elem Res 161:318–327

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  25. Hoffmann PR (2007) Mechanisms by which selenium influences immune responses. Arch Immunol Ther Exp (Warsz) 55:289–297

    Article  CAS  Google Scholar 

  26. Kiremidjian-Schumacher L, Roy M, Wishe HI et al (1992) Regulation of cellular immune responses by selenium. Biol Trace Elem Res 33:23–35

    Article  CAS  PubMed  Google Scholar 

  27. Liu LL, Zhang JL, Zhang ZW et al (2014) Protective roles of selenium on nitric oxide-mediated apoptosis of immune organs induced by cadmium in chickens. Biol Trace Elem Res 159:199–209

    Article  CAS  PubMed  Google Scholar 

  28. Zhang ZW, Zhang JL, Gao YH et al (2013) Effect of oxygen free radicals and nitric oxide on apoptosis of immune organ induced by selenium deficiency in chickens. Biometals 26:355–365

    Article  CAS  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

  30. 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  CAS  PubMed  Google Scholar 

  31. Netea MG, Joosten LA, Lewis E et al (2006) Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nat Med 12:650–656

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  33. Crhanova M, Hradecka H, Faldynova M et al (2011) Immune response of chicken gut to natural colonization by gut microflora and to Salmonella enterica serovar enteritidis infection. Infect Immun 79:2755–2763

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Ye P, Rodriguez FH, Kanaly S et al (2001) Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194:519–527

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Zhao FQ, Zhang ZW, Yao HD et al (2013) Effects of cold stress on mRNA expression of immunoglobulin and cytokine in the small intestine of broilers. Res Vet Sci 95:146–155

    Article  CAS  PubMed  Google Scholar 

  36. Sheridan PA, Zhong N, Carlson BA et al (2007) Decreased selenoprotein expression alters the immune response during influenza virus infection in mice. J Nutr 137:1466–1471

    CAS  PubMed  Google Scholar 

  37. de Andres C, Aristimuno C, De Las Heras V et al (2007) Interferon beta-1a therapy enhances CD4+ regulatory T-cell function: an ex vivo and in vitro longitudinal study in relapsing-remitting multiple sclerosis. J Neuroimmunol 182:204–211

    Article  PubMed  Google Scholar 

  38. Wang CX, Shuaib A (2002) Involvement of inflammatory cytokines in central nervous system injury. Prog Neurobiol 67:161–172

    Article  CAS  PubMed  Google Scholar 

  39. Olson TS, Reuter BK, Scott KG et al (2006) The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med 203:541–552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Yeh HY, Winslow BJ, Junker DE et al (1999) In vitro effects of recombinant chicken interferon-gamma on immune cells. J Interferon Cytokine Res 19:687–691

    Article  CAS  PubMed  Google Scholar 

  41. Rabinovitch A (1994) Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM. Therapeutic intervention by immunostimulation? Diabetes 43:613–621

    Article  CAS  PubMed  Google Scholar 

  42. Liu C, Li M, Cao Y et al (2014) Effects of avermectin on immune function and oxidative stress in the pigeon spleen. Chem Biol Interact 210:43–50

    Article  CAS  PubMed  Google Scholar 

  43. Zeng J, Zhou J, Huang K (2009) Effect of selenium on pancreatic proinflammatory cytokines in streptozotocin-induced diabetic mice. J Nutr Biochem 20:530–536

    Article  CAS  PubMed  Google Scholar 

  44. Simpson RJ, Hammacher A, Smith DK et al (1997) Interleukin-6: structure-function relationships. Protein Sci 6:929–955

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Hinton DM, Myers MJ, Raybourne RA et al (2003) Immunotoxicity of aflatoxin B1 in rats: effects on lymphocytes and the inflammatory response in a chronic intermittent dosing study. Toxicol Sci 73:362–377

    Article  CAS  PubMed  Google Scholar 

  46. Li Y, Ma QG, Zhao LH et al (2014) Effects of lipoic acid on immune function, the antioxidant defense system, and inflammation-related genes expression of broiler chickens fed aflatoxin contaminated diets. Int J Mol Sci 15:5649–5662

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Lee CC, Kim BS, Wu CC et al (2014) Bursal transcriptome of chickens protected by DNA vaccination versus those challenged with infectious bursal disease virus. Arch Virol 160:69–80

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the members of the Veterinary Internal Medicine Laboratory, College of Veterinary Medicine, and Northeast Agriculture University for their help with sample collection.

Funding

This study was supported by the National Natural Science Foundation of China (Grant No.31472161).

Conflict of Interest

The authors declare that they have no conflicts of interest.

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Authors and Affiliations

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

    Pervez Ahmed Khoso, Zijiang Yang, Chunpeng Liu & Shu Li

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  1. Pervez Ahmed Khoso
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  2. Zijiang Yang
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  3. Chunpeng Liu
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  4. Shu Li
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Correspondence to Shu Li.

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Khoso, P.A., Yang, Z., Liu, C. et al. Selenium Deficiency Downregulates Selenoproteins and Suppresses Immune Function in Chicken Thymus. Biol Trace Elem Res 167, 48–55 (2015). https://doi.org/10.1007/s12011-015-0282-y

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