Skip to main content
SpringerLink
Log in

Selenium Deficiency Influences Nitric Oxide and Selenoproteins in Pancreas of Chickens

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

Abstract

Selenium (Se) deficiency induces pancreatic atrophy in chickens, but the molecular mechanism remains unclear. In this study, we investigated the effect of dietary Se deficiency on the expressions of 25 selenoproteins and the content of nitric oxide (NO) and examined the relationship between selenoproteins and NO. Chickens (180; 1 day old) were randomly divided into two groups, low (L) group (fed with Se deficient (Se 0.033 mg/kg) diet) and control (C) group (fed with normal (Se 0.2 mg/kg) diet). Then, pancreas was collected at 15, 25, 35, 45, and 55 days, and the content of NO, the activity of inducible NO synthase (iNOS), and the messenger RNA (mRNA) levels of 25 selenoproteins and iNOS were measured. The results showed that 25 selenoproteins were decreased (P < 0.05) by Se deficiency. Among them, thioredoxin reductase 1 (TXNRD1), selenoprotein S (SELS), selenoprotein U (SELU), selenoprotein X1 (SEPX1), and selenoprotein synthetase 2 (SPS2) were highly and extensively expressed than other types of selenoproteins in pancreas of chickens (P < 0.05). Thioredoxin reductase 2 (TXNRD2), glutathione peroxidase 1 (GPX1), glutathione peroxidase 3 (GPX3), selenoprotein I (SELI), iodothyronine deiodinase 1 (DIO1), selenoprotein P1 (SEPP1), selenoprotein W1 (SEPW1), selenoprotein O (SELO), selenoprotein T (SELT), selenoprotein M (SELM), selenoprotein X1 (SEPX1), and SPS2 were excessively decreased (P < 0.05). Meanwhile, NO content, iNOS activity, and mRNA level were increased strikingly compared with C group (P < 0.05). The correlation analysis suggested that NO had a strong negative correlation with GPX1, glutathione peroxidase 2 (GPX2), GPX3, DIO1, selenoprotein K (SELK), SELI, SEPX1, and SPS2. These results suggested that Se deficiency induced pancreatic injury by influencing NO and selenoproteins in pancreas of chickens. Thus, it offers some information on the mechanism of pancreatic injury induced by Se deficiency.

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

  1. Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Rederstorff M, Krol A, Lescure A (2006) Understanding the importance of selenium and selenoproteins in muscle function. Cell Mol Life Sci 63:52–59

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Thompson JN, Scott ML (1970) Impaired lipid and vitamin E absorption related to atrophy of the pancreas in selenium-deficient chicks. J Nutr 100:797–809

    CAS  PubMed  Google Scholar 

  5. Xu S-W, Yao H-D, Zhang J et al (2012) The oxidative damage and disbalance of calcium homeostasis in brain of chicken induced by selenium deficiency. Biol Trace Elem Res 151:225–233

    Article  PubMed  Google Scholar 

  6. Wu Q, Yao HD, Tan SR, et al. (2014) Possible correlation of selenoprotein W with inflammation factors in chicken skeletal muscles. Biol Trace Elem Res. doi:10.1007/s12011-014-0092-7

  7. Ghazi Harsini S, Habibiyan M, Moeini MM, Abdolmohammadi AR (2012) Effects of dietary selenium, vitamin E, and their combination on growth, serum metabolites, and antioxidant defense system in skeletal muscle of broilers under heat stress. Biol Trace Elem Res 148:322–330

    Article  CAS  PubMed  Google Scholar 

  8. Kryukov GV, Gladyshev VN (2002) Mammalian selenoprotein gene signature: identification and functional analysis of selenoprotein genes using bioinformatics methods. Methods Enzymol 347:84–100

    Article  CAS  PubMed  Google Scholar 

  9. 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 

  10. Pappas AC, Zoidis E, Surai PF, Zervas G (2008) Selenoproteins and maternal nutrition. Comp Biochem Phys B 151:361–372

    Article  CAS  Google Scholar 

  11. Lescure A, Rederstorff M, Krol A, Guicheney P, Allamand V (2009) Selenoprotein function and muscle disease. Biochim Biophys Acta 1790:1569–1574

    Article  CAS  PubMed  Google Scholar 

  12. Bellinger FP, Raman AV, Reeves MA, Berry MJ (2009) Regulation and function of selenoproteins in human disease. Biochem J 422:11–22

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142

    CAS  PubMed  Google Scholar 

  14. Lowenstein CJ, Snyder SH (1992) Nitric oxide, a novel biologic messenger. Cell 70:705–707

    Article  CAS  PubMed  Google Scholar 

  15. Nathan C (1995) Natural resistance and nitric oxide. Cell 82:873–876

    Article  CAS  PubMed  Google Scholar 

  16. Dias RG, Negrao CE, Krieger MH (2011) Nitric oxide and the cardiovascular system: cell activation, vascular reactivity and genetic variant. Arq Bras Cardiol 96:68–75

    CAS  PubMed  Google Scholar 

  17. Kouti L, Noroozian M, Akhondzadeh S et al (2013) Nitric oxide and peroxynitrite serum levels in Parkinson's disease: correlation of oxidative stress and the severity of the disease. Eur Rev Med Pharm Sci 17:964–970

    CAS  Google Scholar 

  18. Nathan C, Xie QW (1994) Regulation of biosynthesis of nitric oxide. J Biol Chem 269:13725–13728

    CAS  PubMed  Google Scholar 

  19. Kroncke KD, Fehsel K, Kolb-Bachofen V (1997) Nitric oxide: cytotoxicity versus cytoprotection–how, why, when, and where? Nitric Oxide 1:107–120

    Article  CAS  PubMed  Google Scholar 

  20. Allan CB, Lacourciere GM, Stadtman TC (1999) Responsiveness of selenoproteins to dietary selenium. Annu Rev Nutr 19:1–16

    Article  CAS  PubMed  Google Scholar 

  21. Holben DH, Smith AM (1999) The diverse role of selenium within selenoproteins: a review. J Am Diet Assoc 99:836–843

    Article  CAS  PubMed  Google Scholar 

  22. Tinkel J, Hassanain H, Khouri SJ (2012) Cardiovascular antioxidant therapy: a review of supplements, pharmacotherapies, and mechanisms. Cardiol Rev 20:77–83

    PubMed  Google Scholar 

  23. 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 

  24. 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 

  25. Wang R, Sun B, Zhang Z, Li S, Xu S (2011) Dietary selenium influences pancreatic tissue levels of selenoprotein W in chickens. J Inorg Biochem 105:1156–1160

    Article  CAS  PubMed  Google Scholar 

  26. Sun B, Wang R, Li J, Jiang Z, Xu S (2011) Dietary selenium affects selenoprotein W gene expression in the liver of chicken. Biol Trace Elem Res 143:1516–1523

    Article  CAS  PubMed  Google Scholar 

  27. 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 

  28. Zhao FQ, Zhang ZW, Wang C et al (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  PubMed Central  PubMed  Google Scholar 

  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  30. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  31. 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 

  32. Zhang J, Li J, Zhang Z et al (2012) Ubiquitous expression of selenoprotein N transcripts in chicken tissues and early developmental expression pattern in skeletal muscles. Biol Trace Elem Res 146:187–191

    Article  CAS  PubMed  Google Scholar 

  33. Ruan H, Zhang Z, Wu Q et al (2012) Selenium regulates gene expression of selenoprotein W in chicken skeletal muscle system. Biol Trace Elem Res 145:59–65

    Article  CAS  PubMed  Google Scholar 

  34. Gao X, Xing H, Li S et al (2012) Selenium regulates gene expression of selenoprotein W in chicken gastrointestinal tract. Biol Trace Elem Res 145:181–188

    Article  CAS  PubMed  Google Scholar 

  35. Yu D, Li JL, Zhang JL, Gao XJ, Xu S (2011) Effects of dietary selenium on selenoprotein W gene expression in the chicken immune organs. Biol Trace Elem Res 144:678–687

    Article  CAS  PubMed  Google Scholar 

  36. Li JL, Li HX, Li S et al (2012) Effects of selenoprotein W gene expression by selenium involves regulation of mRNA stability in chicken embryos neurons. Biometals 25:459–468

    Article  CAS  PubMed  Google Scholar 

  37. Scheerer P, Borchert A, Krauss N et al (2007) Structural basis for catalytic activity and enzyme polymerization of phospholipid hydroperoxide glutathione peroxidase-4 (GPx4). Biochemistry 46:9041–9049

    Article  CAS  PubMed  Google Scholar 

  38. Chen J, Berry MJ (2003) Selenium and selenoproteins in the brain and brain diseases. J Neurochem 86:1–12

    Article  CAS  PubMed  Google Scholar 

  39. Rederstorff M, Castets P, Arbogast S et al (2011) Increased muscle stress-sensitivity induced by selenoprotein N inactivation in mouse: a mammalian model for SEPN1-related myopathy. PLoS One 6:e23094

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Arbogast S, Beuvin M, Fraysse B et al (2009) Oxidative stress in SEPN1-related myopathy: from pathophysiology to treatment. Ann Neurol 65:677–686

    Article  CAS  PubMed  Google Scholar 

  41. Kryukov GV, Gladyshev VN (2000) Selenium metabolism in zebrafish: multiplicity of selenoprotein genes and expression of a protein containing 17 selenocysteine residues. Genes Cells 5:1049–1060

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  43. Reeves MA, Bellinger FP, Berry MJ (2010) The neuroprotective functions of selenoprotein M. Antioxid Redox Signal 12

  44. Liu CP, Fu J, Lin SL, Wang XS, Li S (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 

  45. Guimaraes MJ, Peterson D, Vicari A et al (1996) Identification of a novel selD homolog from eukaryotes, bacteria, and archaea: is there an autoregulatory mechanism in selenocysteine metabolism? Proc Natl Acad Sci U S A 93:15086–15091

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Hawkes WC, Alkan Z (2010) Regulation of redox signaling by selenoproteins. Biol Trace Elem Res 134:235–251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Huang JQ, Li DL, Zhao H et al (2011) The selenium deficiency disease exudative diathesis in chicks is associated with downregulation of seven common selenoprotein genes in liver and muscle. J Nutr 141:1605–1610

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Grisham MB, Pavlick KP, Laroux FS et al (2002) Nitric oxide and chronic gut inflammation: controversies in inflammatory bowel disease. J Investig Med 50:272–283

    Article  CAS  PubMed  Google Scholar 

  49. Bachmaier K, Neu N, Pummerer C et al (1997) iNOS expression and nitrotyrosine formation in the myocardium in response to inflammation is controlled by the interferon regulatory transcription factor 1. Circulation 96:585–591

    CAS  PubMed  Google Scholar 

  50. Boger RH, Bode-Boger SM, Thiele W et al (1997) Biochemical evidence for impaired nitric oxide synthesis in patients with peripheral arterial occlusive disease. Circulation 95:2068–2074

    Article  CAS  PubMed  Google Scholar 

  51. Hingorani AD, Liang CF, Fatibene J et al (1999) A common variant of the endothelial nitric oxide synthase (Glu298-->Asp) is a major risk factor for coronary artery disease in the UK. Circulation 100:1515–1520

    Article  CAS  PubMed  Google Scholar 

  52. Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G (2004) Nitric oxide in health and disease of the respiratory system. Physiol Rev 84:731–765

    Article  CAS  PubMed  Google Scholar 

  53. Prabhu KS, Zamamiri-Davis F, Stewart JB et al (2002) Selenium deficiency increases the expression of inducible nitric oxide synthase in RAW 264.7 macrophages: role of nuclear factor-kappaB in up-regulation. Biochem J 366:203–209

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (31272626), the Study Abroad Foundation of Heilongjiang Province (LC201031), the Doctoral Fund of the Ministry of Education of China (20122325110018), and the Heilongjiang Postdoctoral Fund (LBH-Z13028).

Conflict of Interest

The authors declare that there are no conflicts of interest.

Author information

Authors and Affiliations

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

    Xia Zhao, Haidong Yao, Ruifeng Fan, Ziwei Zhang & Shiwen Xu

Authors
  1. Xia Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haidong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruifeng Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ziwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shiwen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ziwei Zhang or Shiwen Xu.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, X., Yao, H., Fan, R. et al. Selenium Deficiency Influences Nitric Oxide and Selenoproteins in Pancreas of Chickens. Biol Trace Elem Res 161, 341–349 (2014). https://doi.org/10.1007/s12011-014-0139-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-014-0139-9

Keywords

Search

Navigation