Advertisement

Biological Trace Element Research

, Volume 176, Issue 2, pp 407–415 | Cite as

Selenium Deficiency-Induced Apoptosis of Chick Embryonic Vascular Smooth Muscle Cells and Correlations with 25 Selenoproteins

  • Qingyu Wang
  • Jiaqiang Huang
  • Hao Zhang
  • Xingen Lei
  • Zhongyao Du
  • Chen Xiao
  • Silu Chen
  • Fazheng Ren
Article

Abstract

Selenium deficiency is the major cause of exudative diathesis in chicks. Subcutaneous hemorrhage is one of the typical symptoms of the disease. However, the reason for the occurrence of blood exudation remains unknown. In the present study, the vascular smooth muscle cells (VSMCs) were isolated from 17-day-old broiler chick embryos. Cell viability, cell apoptosis, and intracellular reactive oxygen species level under different concentrations of selenium (0–0.9 μM) were investigated. The mRNA expression levels of 25 selenoproteins and apoptosis-related genes (p53, CytC, Caspase-3, Caspase-8, Bcl-2, and Bax) were also measured. Selenium deficiency significantly decreased cell viability and increased cell apoptosis (p < 0.05). Supplementation with selenium could alleviate these changes. In general, at all levels of selenium addition, Gpx1, Gpx3, Gpx4, SepW1, and Sep15 mRNAs were all highly expressed in VSMCs, whereas Gpx2, Dio1, SepN1, SelO, and SelPb were at lower levels. There was a high correlation between Gpx2, Gpx3, Gpx4, Dio1, Txnrd1, Txnrd2, and Txnrd3 gene expression. Additionally, Gpx3, Gpx4, Dio1, Txnrd1, Txnrd2, Txnrd3, SelS, and SelPb showed a strong negative correlation with pro-apoptotic gene Caspase-3 as well as a strong positive correlation with anti-apoptotic gene Bcl-2, especially SelI (r = 0.913 and r = 0.929, p < 0.01). These results suggest that selenium deficiency could induce VSMC apoptosis, and several selenoproteins may be involved in the development of apoptosis. Our findings provide information on the molecular mechanism of vascular injury by selenium deficiency.

Keywords

Exudative diathesis Selenium deficiency Selenoproteins Vascular smooth muscle Cell apoptosis Chicks 

Notes

Acknowledgments

This study was funded by Chinese Natural Science Foundation: the Major International (Regional) Joint Research Program of China (No. 31320103920).

Compliance with Ethical Standards

Conflict of Interest

All authors declare that they have no conflict of interest.

Ethical Approval

The study followed all applicable international, national, and institutional guidelines for the care and use of animals. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice.

Supplementary material

12011_2016_823_MOESM1_ESM.doc (80 kb)
ESM 1 (DOC 79 kb)

References

  1. 1.
    Wang X, Zhang W, Chen H, Liao N, Wang Z, Zhang X, Hai C (2014) High selenium impairs hepatic insulin sensitivity through opposite regulation of ROS. Toxicol Lett 224(1):16–23CrossRefPubMedGoogle Scholar
  2. 2.
    Wichtel J (1998) A review of selenium deficiency in grazing ruminants part 1: new roles for selenium in ruminant metabolism. Vet J 46(2):47–52Google Scholar
  3. 3.
    Yao H-D, Wu Q, Zhang Z-W, Zhang J-L, Li S, Huang J-Q, Ren F-Z, S-W X, Wang X-L, Lei XG (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of se-deficient chicks. J Nutr 143(5):613–619CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigó R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300(5624):1439–1443CrossRefPubMedGoogle Scholar
  5. 5.
    Wachi H, Seyama Y, Yamashita S, Tajima S (1995) Cell cycle-dependent regulation of elastin gene in cultured chick vascular smooth-muscle cells. Biochem J 309:575–579CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Zhao X, Yao H, Fan R, Zhang Z, Xu S (2014) Selenium deficiency influences nitric oxide and selenoproteins in pancreas of chickens. Biol Trace Elem Res 161(3):341–349CrossRefPubMedGoogle Scholar
  7. 7.
    Liang Y, Lin S-l, Wang C-w, H-d Y, Z-w Z, Xu S-w (2014) Effect of selenium on selenoprotein expression in the adipose tissue of chickens. Biol Trace Elem Res 160(1):41–48CrossRefPubMedGoogle Scholar
  8. 8.
    Huang J-Q, Li D-L, Zhao H, Sun L-H, Xia X-J, Wang K-N, Luo X, Lei XG (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(9):1605–1610CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Vunta H, Belda BJ, Arner RJ, Channa Reddy C, Vanden Heuvel JP, Sandeep Prabhu K (2008) Selenium attenuates pro-inflammatory gene expression in macrophages. Mol Nutr Food Res 52(11):1316–1323CrossRefPubMedGoogle Scholar
  10. 10.
    Halliwell B, Gutteridge J (1989) Protection against oxidants in biological systems: the superoxide theory of oxygen toxicity. Free radicals in biology and medicine. Claredon Press, OxfordGoogle Scholar
  11. 11.
    Zwolak I, Zaporowska H (2012) Selenium interactions and toxicity: a review. Biol Toxicol 28(1):31–46CrossRefGoogle Scholar
  12. 12.
    Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE (1999) Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscl Throm Vas 19(7):1589–1594CrossRefGoogle Scholar
  13. 13.
    Hungerford J, Little C (1999) Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J Vasc Res 36(1):2–27CrossRefPubMedGoogle Scholar
  14. 14.
    Palomino-Morales R, Alejandre MJ, Perales S, Torres C, Linares A (2014) Effect of PUFAs on extracellular matrix production and remodeling in vascular smooth muscle cell cultures in an atherosclerotic model. Eur J Lipid Sci Tech 116(11):1485–1495CrossRefGoogle Scholar
  15. 15.
    Safaralizadeh R, Nourizadeh M, Zare A, Kardar GA, Pourpak Z (2013) Influence of selenium on mast cell mediator release. Biol Trace Elem Res 154(2):299–303CrossRefPubMedGoogle Scholar
  16. 16.
    Gao J, Zhang D, Zhang K, Liu M, Han Z, Li J (2012) Effects of selenium supplementation on expression of endothelin-1 and its receptors in pulmonary microvascular endothelial cells from chick embryos. Biol Trace Elem Res 150(1–3):173–177CrossRefPubMedGoogle Scholar
  17. 17.
    Yu D, Z-w Z, H-d Y, Li S, Xu S-w (2014) Antioxidative role of selenoprotein W in oxidant-induced chicken splenic lymphocyte death. Biometals 27(2):277–291CrossRefPubMedGoogle Scholar
  18. 18.
    Fang B, Zhang M, Tian M, Ren F (2015) Self-assembled β-lactoglobulin–oleic acid and β-lactoglobulin–linoleic acid complexes with antitumor activities. J Dairy Sci 98(5):2898–2907CrossRefPubMedGoogle Scholar
  19. 19.
    Perales S, Alejandre MJ, Palomino-Morales R, Torres C, Linares A (2010) Influence of cholesterol and fish oil dietary intake on nitric oxide-induced apoptosis in vascular smooth muscle cells. Nitric Oxide 22(3):205–212CrossRefPubMedGoogle Scholar
  20. 20.
    Saito Y, Yoshida Y, Akazawa T, Takahashi K, Niki E (2003) Cell death caused by selenium deficiency and protective effect of antioxidants. J Biol Chem 278(41):39428–39434CrossRefPubMedGoogle Scholar
  21. 21.
    Hassan A, Ahn J, Suh Y, Choi YM, Chen P, Lee K (2014) Selenium promotes adipogenic determination and differentiation of chicken embryonic fibroblasts with regulation of genes involved in fatty acid uptake, triacylglycerol synthesis and lipolysis. J Nutr Biochem 25(8):858–867CrossRefPubMedGoogle Scholar
  22. 22.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods 25(4):402–408. doi: 10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  23. 23.
    Liu H, Li X, Qin F, Huang K (2014) Selenium suppresses oxidative-stress-enhanced vascular smooth muscle cell calcification by inhibiting the activation of the PI3K/AKT and ERK signaling pathways and endoplasmic reticulum stress. J Biol Inorg Chem 19(3):375–388CrossRefPubMedGoogle Scholar
  24. 24.
    Lin S-l, Wang C-w, Tan S-r, Liang Y, H-d Y, Z-w Z, Xu S-w (2014) Selenium deficiency inhibits the conversion of thyroidal thyroxine (T4) to triiodothyronine (T3) in chicken thyroids. Biol Trace Elem Res 161(3):263–271CrossRefPubMedGoogle Scholar
  25. 25.
    Stadtman TC (2000) Selenium biochemistry: mammalian selenoenzymes. Ann N Y Acad Sci 899(1):399–402CrossRefPubMedGoogle Scholar
  26. 26.
    Monsen ER (2000) Dietary reference intakes for the antioxidant nutrients: vitamin C, vitamin E, selenium, and carotenoids. J Am Diet Assoc 100(6):637–640CrossRefPubMedGoogle Scholar
  27. 27.
    Wang J, Qiao J, Zhao L, Li K, Wang H, Xu T, Tian Y, Gao M, Wang X (2007) Proliferation of pulmonary artery smooth muscle cells in the development of ascites syndrome in broilers induced by low ambient temperature. J Vet Med A 54(10):564–570CrossRefGoogle Scholar
  28. 28.
    Nunes VA, Gozzo AJ, Cruz-Silva I, Juliano MA, Viel TA, Godinho RO, Meirelles FV, Sampaio MU, Sampaio CA, Araujo MS (2005) Vitamin E prevents cell death induced by mild oxidative stress in chicken skeletal muscle cells. Comp Biochem Phys C 141(3):225–240CrossRefGoogle Scholar
  29. 29.
    Scheerer P, Borchert A, Krauss N, Wessner H, Gerth C, Höhne W, Kuhn H (2007) Structural basis for catalytic activity and enzyme polymerization of phospholipid hydroperoxide glutathione peroxidase-4 (GPx4). Biochemistry-US 46(31):9041–9049CrossRefGoogle Scholar
  30. 30.
    Chen J, Berry MJ (2003) Selenium and selenoproteins in the brain and brain diseases. J Neurochem 86(1):1–12CrossRefPubMedGoogle Scholar
  31. 31.
    Loflin J, Lopez N, Whanger PD, Kioussi C (2006) Selenoprotein W during development and oxidative stress. J Inorg Biochem 100(10):1679–1684CrossRefPubMedGoogle Scholar
  32. 32.
    Reeves MA, Hoffmann PR (2009) The human selenoproteome: recent insights into functions and regulation. Cell Mol Life Sci 66(15):2457–2478CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Yao H, Liu W, Zhao W, Fan R, Zhao X, Khoso PA, Zhang Z, Xu S (2014) Different responses of selenoproteins to the altered expression of selenoprotein W in chicken myoblasts. RSC Adv 4(109):64032–64042CrossRefGoogle Scholar
  34. 34.
    Han Y-H, Zhang Z-W, Su J, Zhang B, Li S, S-W X (2012) Effects of chicken selenoprotein W on H2O2-induced apoptosis in CHO-K1 cells. Biol Trace Elem Res 147(1–3):395–402CrossRefPubMedGoogle Scholar
  35. 35.
    Skulachev VP (1998) Cytochrome c in the apoptotic and antioxidant cascades. FEBS Lett 423(3):275–280CrossRefPubMedGoogle Scholar
  36. 36.
    Parihar A, Parihar MS, Nazarewicz R, Ghafourifar P (2010) Importance of cytochrome c redox state for ceramide-induced apoptosis of human mammary adenocarcinoma cells. BBA-Biomembranes 1800(7):646–654PubMedGoogle Scholar
  37. 37.
    Horibata Y, Hirabayashi Y (2007) Identification and characterization of human ethanolaminephosphotransferase1. J Lipid Res 48(3):503–508CrossRefPubMedGoogle Scholar
  38. 38.
    Wright MM, McMaster CR (2002) PC and PE synthesis: mixed micellar analysis of the cholinephosphotransferase and ethanolaminephosphotransferase activities of human choline/ethanolamine phosphotransferase 1 (CEPT1. Lipids 37(7):663–672CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Qingyu Wang
    • 1
    • 2
  • Jiaqiang Huang
    • 1
    • 2
  • Hao Zhang
    • 1
    • 2
  • Xingen Lei
    • 1
    • 3
  • Zhongyao Du
    • 1
    • 2
  • Chen Xiao
    • 1
    • 2
  • Silu Chen
    • 1
    • 2
  • Fazheng Ren
    • 1
    • 2
  1. 1.Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Food Science & Nutritional EngineeringChina Agricultural UniversityBeijingChina
  2. 2.Beijing Laboratory for Food Quality and Safety, and Key Laboratory of Functional Dairy, College of Food Science and Nutritional EngineeringChina Agricultural UniversityBeijingChina
  3. 3.Department of Animal ScienceCornell UniversityIthacaUSA

Personalised recommendations