Advertisement

Biological Trace Element Research

, Volume 184, Issue 2, pp 463–473 | Cite as

Ameliorative Effects of Selenium on Cadmium-Induced Injury in the Chicken Ovary: Mechanisms of Oxidative Stress and Endoplasmic Reticulum Stress in Cadmium-Induced Apoptosis

  • Na Wan
  • Zhe Xu
  • Tianqi Liu
  • Yahong Min
  • Shu LiEmail author
Article

Abstract

Despite the well-established toxicity of cadmium (Cd) to animals and the ameliorative effects of selenium (Se), some specific mechanisms in the chicken ovary are not yet clarified. To explore the mechanism by which the toxicity effect of Cd is induced and explore the effect of supranutritional Se on Cd toxicity in female bird reproduction, forty-eight 50-day-old Isa Brown female chickens were divided randomly into four groups. Group I (control group) was fed the basic diet containing 0.2 mg/kg Se. Group II (Se-treated group) was fed the basic diet supplemented with sodium selenite (Na2SeO3), and the total Se content was 2 mg/kg. Group III (Se + Cd-treated group) was fed the basic diet supplemented with Na2SeO3; the total Se content was 2 mg/kg, and it was supplemented with 150 mg/kg cadmium chloride (CdCl2). Group IV (Cd-treated group) was with the basic diet supplemented with 150 mg/kg CdCl2. The Cd, estradiol (E2), and progestogen (P4) contents changed after subchronic Cd exposure in chicken ovarian tissue; subsequently, oxidative stress occurred and activated the endoplasmic reticulum (ER) pathway to induce apoptosis. Further, Se decreased the accumulation of Cd in ovarian tissue, increased the E2 and P4 contents, alleviated oxidative stress, and reduced apoptosis via the ER stress pathway. The present results demonstrated that Cd could induce apoptosis via the ER stress pathway in chicken ovarian tissue and that Se had a significant antagonistic effect. These results are potentially valuable for finding a strategy to prevent Cd poisoning.

Keywords

Cadmium Selenium Oxidative stress Endoplasmic reticulum stress Apoptosis Chicken ovary 

Abbreviations

Cd

cadmium

Se

selenium

E2

estradiol

P4

progestogen

Na2SeO3

sodium selenite

CdCl2

cadmium chloride

ER

endoplasmic reticulum

SOD

superoxide dismutase

GSH-Px

glutathione peroxidase

MDA

malondialdehyde

NO

nitric oxide

iNOS

inducible nitric oxide synthase

LPO

lipid peroxidation

ROS

reactive oxygen species

GRP78

glucose-regulated protein 78

PERK

PKR-like ER kinase

ATF6

activating transcription factor 6

ATF4

activating transcription factor 4

IRE1

inositol requiring enzyme 1

Caspase

cysteine-aspartic protease

CHOP

ATF6-CCAAT/enhancer-binding protein-homologous protein

XBP1

IRE1-X-box-binding protein 1

TRAF2

IRE1-TNF receptor associated factor 2

Notes

Acknowledgments

The authors thank the Key Laboratory of the Provincial Education Department of Heilongjiang for Common Animal Disease Prevention and Treatment.

Funding

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

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Humane Care of Animals

The experiments were approved by the Institutional Animal Care and Use Committee of the Northeast Agricultural University under the approved protocol number SRM-06.

References

  1. 1.
    Kim J, Koo TH (2008) Heavy metal distribution in chicks of two heron species from Korea. Arch Environ Contam Toxicol 54(4):740–747CrossRefPubMedGoogle Scholar
  2. 2.
    Bagchi D, Vuchetich PJ, Bagchi M, Hassoun EA, Tran MX, Tang L, Stohs SJ (1997) Induction of oxidative stress by chronic administration of sodium dichromate [chromium VI] and cadmium chloride [cadmium II] to rats. Free Radic Biol Med 22(3):471–478CrossRefPubMedGoogle Scholar
  3. 3.
    Ferramola ML, Pérez Díaz MF, Honoré SM, Sánchez SS, Antón RI, Anzulovich AC, Giménez MS (2012) Cadmium-induced oxidative stress and histological damage in the myocardium. Effects of a soy-based diet. Toxicol Appl Pharmacol 265(3):380–389CrossRefPubMedGoogle Scholar
  4. 4.
    Napolitano JR, Liu MJ, Bao S, Crawford M, Nana-Sinkam P, Cormet-Boyaka E, Knoell DL (2012) Cadmium-mediated toxicity of lung epithelia is enhanced through NF-κB-mediated transcriptional activation of the human zinc transporter ZIP8. Am J Physiol Lung Cell Mol Physiol 302(9):909–918CrossRefGoogle Scholar
  5. 5.
    Liu L, Yang B, Cheng Y, Lin H (2015) Ameliorative effects of selenium on cadmium-induced oxidative stress and endoplasmic reticulum stress in the chicken kidney. Biol Trace Elem Res 167(2):308–319CrossRefPubMedGoogle Scholar
  6. 6.
    Li JL, Jiang CY, Li S, Xu SW (2013) Cadmium induced hepatotoxicity in chickens ( Gallus domesticus ) and ameliorative effect by selenium. Ecotoxicol Environ Saf 96(8):103–109CrossRefPubMedGoogle Scholar
  7. 7.
    Liu S, Xu FP, Yang ZJ, Li M, Min YH, Li S (2014) Cadmium-induced injury and the ameliorative effects of selenium on chicken splenic lymphocytes: mechanisms of oxidative stress and apoptosis. Biol Trace Elem Res 160(3):340–351CrossRefPubMedGoogle Scholar
  8. 8.
    Li JL, Gao R, Li S, Wang JT, Tang ZX, Xu SW (2010) Testicular toxicity induced by dietary cadmium in cocks and ameliorative effect by selenium. Biometals 23(4):695–705CrossRefPubMedGoogle Scholar
  9. 9.
    Wenchang Z, Zhiren W, Huangyuan L, Ezaki T, Koji T (2002) Effects of cadmium as a possible endocrine disruptor upon the serum level of sex steroids and secretion of gonadotropins from pituitary in adult rats. Acta Med Nagasaki 47(1):53–56Google Scholar
  10. 10.
    Yang S, Zhang Z, He J, Li J, Zhang JL, Xing H, Xu S (2012) Ovarian toxicity induced by dietary cadmium in hen. Biol Trace Elem Res 148(1):53–60CrossRefPubMedGoogle Scholar
  11. 11.
    Zhang W, Pang F, Huang Y, Yan P, Lin W (2008) Cadmium exerts toxic effects on ovarian steroid hormone release in rats. Toxicol Lett 182(1):18–23CrossRefPubMedGoogle Scholar
  12. 12.
    Paksy K, Varga B, Lázár P (1992) Cadmium interferes with steroid biosynthesis in rat granulosa and luteal cells in vitro. Biometals Int J Role Metal Ions Biol Biochem Med 5(4):245CrossRefGoogle Scholar
  13. 13.
    Tribowo JA, Arizal MH, Nashrullah M, Aditama AR, Utama DG (2014) Oxidative stress of cadmium-induced ovarian rat toxicity. Int J Chem Eng Appl 5(3):389–391Google Scholar
  14. 14.
    Wang J, Zhu H, Liu X, Liu Z (2014) Oxidative stress and Ca2+ signals involved on cadmium-induced apoptosis in rat hepatocyte. Biol Trace Elem Res 161(2):180–189CrossRefPubMedGoogle Scholar
  15. 15.
    Kitamura M, Hiramatsu N (2010) The oxidative stress: endoplasmic reticulum stress axis in cadmium toxicity. Biometals Int J Role Metal Ions Biol Biochem Med 23(5):941–950CrossRefGoogle Scholar
  16. 16.
    Yokouchi M, Hiramatsu N, Hayakawa K, Okamura M, Du S, Kasai A, Takano Y, Shitamura A, Shimada T, Yao J (2008) Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem 283(7):42–52CrossRefGoogle Scholar
  17. 17.
    Jin Y, Zhang S, Tao R, Huang J, He X, Qu L, Fu Z (2016) Oral exposure of mice to cadmium (II), chromium (VI) and their mixture induce oxidative- and endoplasmic reticulum-stress mediated apoptosis in the livers. Environ Toxicol 31(6):693–705CrossRefPubMedGoogle Scholar
  18. 18.
    Jihen EH, Imed M, Fatima H, Abdelhamid K (2009) Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Saf 72(5):1559–1564CrossRefGoogle Scholar
  19. 19.
    Newairy AA, Elsharaky AS, Badreldeen MM, Eweda SM, Sheweita SA (2007) The hepatoprotective effects of selenium against cadmium toxicity in rats. Toxicology 242(3):23–30CrossRefPubMedGoogle Scholar
  20. 20.
    Liu LL, Li CM, Zhang ZW, Zhang JL, Yao HD, Xu SW (2014) Protective effects of selenium on cadmium-induced brain damage in chickens. Biol Trace Elem Res 158(2):176–185CrossRefPubMedGoogle Scholar
  21. 21.
    Han G (1998) Exposure level of cadmium in poultry in cadmium polluted areas. J Environ Health 199(2):111–114Google Scholar
  22. 22.
    Shuvaeva OV, Belchenko LA, Romanova TE (2013) Studies on cadmium accumulation by some selected floating macrophytes. Int J Phytoremediation 15(10):979–990CrossRefPubMedGoogle Scholar
  23. 23.
    Tan S, Chi Q, Liu T, Sun Z, Min Y, Zhang Z, Li S (2017) Alleviation mechanisms of selenium on cadmium-spiked neutrophil injury to chicken. Biol Trace Elem Res 178(2):301–309Google Scholar
  24. 24.
    Zhang R, Xing L, Bao J, Sun H, Bi Y, Liu H, Li J (2017) Selenium supplementation can protect from enhanced risk of keel bone damage in laying hens exposed to cadmium. RSC Adv 7(12):7170–7178CrossRefGoogle Scholar
  25. 25.
    Uluozlu OD, Tuzen M, Mendil D, Soylak M (2009) Assessment of trace element contents of chicken products from Turkey. J Hazard Mater 163(2):982–987CrossRefPubMedGoogle Scholar
  26. 26.
    Xu T, Gao X, Liu G (2016) The antagonistic effect of selenium on lead toxicity is related to the ion profile in chicken liver. Biol Trace Elem Res 169(2):365–373CrossRefPubMedGoogle Scholar
  27. 27.
    Yang Z, Liu C, Liu C, Teng X, Li S (2016) Selenium deficiency mainly influences antioxidant selenoproteins expression in broiler immune organs. Biol Trace Elem Res 172(1):209–221CrossRefPubMedGoogle Scholar
  28. 28.
    Bradford MM (1976) A rapid and sensitive methods for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72(1–2):248–254CrossRefPubMedGoogle Scholar
  29. 29.
    Xu J, Lian LJ, Wu C, Wang XF, Fu WY, Xu LH (2008) Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem Toxicol 46(5):1488–1494CrossRefPubMedGoogle Scholar
  30. 30.
    Huff MOM, Todd SL, Bleser AS, Riggs KA, Dougherty SM, Klinge CM (2007) Cadmium chloride and sodium arsenate, environmental estrogens in cigarette smoke, activate estrogen signaling pathways to induce proliferation in a human lung adenocarcinoma cell line. FASEB J 21(2):A255–A259Google Scholar
  31. 31.
    Vrsanská S, Nagyová E, Mlynarcíková A, Ficková M, Kolena J (2002) Components of cigarette smoke inhibit expansion of oocyte-cumulus complexes from porcine follicles. Physiol Res 52(3):383–387Google Scholar
  32. 32.
    Paksy K, Varga B, Horváth E, Tátrai E, Ungváry G (1989) Acute effects of cadmium on preovulatory serum FSH, LH, and prolactin levels and on ovulation and ovarian hormone secretion in estrous rats. Reprod Toxicol 3(4):241–247CrossRefPubMedGoogle Scholar
  33. 33.
    Li JL, Sunde RA (2016) Selenoprotein transcript level and enzyme activity as biomarkers for selenium status and selenium requirements of chickens (Gallus gallus). PLoS One 11(4):e0152392CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lei W, Wang L, Liu D, Xu T, Luo J (2011) Histopathological and biochemical alternations of the heart induced by acute cadmium exposure in the freshwater crab Sinopotamon yangtsekiense. Chemosphere 84(5):689–694CrossRefPubMedGoogle Scholar
  35. 35.
    Pi J, Horiguchi S, Sun Y, Nikaido M, Shimojo N, Hayashi T, Yamauchi H, Itoh K, Yamamoto M, Sun G (2003) A potential mechanism for the impairment of nitric oxide formation caused by prolonged oral exposure to arsenate in rabbits. Free Radic Biol Med 35(1):102–113CrossRefPubMedGoogle Scholar
  36. 36.
    Wang M, Zhou Q (2006) Effects of herbicide chlorimuron-ethyl on physiological mechanisms in wheat (Triticum aestivum). Ecotoxicol Environ Saf 64(2):190–197CrossRefPubMedGoogle Scholar
  37. 37.
    Bloom JA, Cox IJ, Miller ML, Min WU, Lin CY, Lui YM (2001) Rotation, scale and translation resilient public watermarking for images. IEEE Trans Image Process 10(5):767–782Google Scholar
  38. 38.
    Wittman R, Hu H (2002) Cadmium exposure and nephropathy in a 28-year-old female metals worker. Environ Health Perspect 110(12):1261–1266CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Bernard A (2008) Cadmium & its adverse effects on human health. Indian J Med Res 128(4):557–564PubMedGoogle Scholar
  40. 40.
    Fouad AA, Qureshi HA, Al-Sultan AI, Yacoubi MT, Ali AA (2009) Protective effect of hemin against cadmium-induced testicular damage in rats. Toxicology 257(3):153–160CrossRefPubMedGoogle Scholar
  41. 41.
    Pathak N, Khandelwal S (2006) Oxidative stress and apoptotic changes in murine splenocytes exposed to cadmium. Toxicology 220(1):26–36CrossRefPubMedGoogle Scholar
  42. 42.
    Ferramola ML, Antón RI, Anzulovich AC, Giménez MS (2011) Myocardial oxidative stress following sub-chronic and chronic oral cadmium exposure in rats. Environ Toxicol Pharmacol 32(1):17–26CrossRefPubMedGoogle Scholar
  43. 43.
    Hagar H, Malki WA (2014) Betaine supplementation protects against renal injury induced by cadmium intoxication in rats: role of oxidative stress and caspase-3. Environ Toxicol Pharmacol 37(2):803–811CrossRefPubMedGoogle Scholar
  44. 44.
    Hammadi M, Oulidi A, Gackière F, Katsogiannou M, Slomianny C, Roudbaraki M, Dewailly E, Delcourt P, Lepage G, Lotteau S (2013) Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEB J 27(4):1600–1609CrossRefPubMedGoogle Scholar
  45. 45.
    Yokouchi M, Hiramatsu N, Hayakawa K, Kasai A, Takano Y, Yao J, Kitamura M (2007) Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ 14(8):1467–1474CrossRefPubMedGoogle Scholar
  46. 46.
    Szabó C, Ohshima H (1997) DNA damage induced by peroxynitrite: subsequent biological effects. Nitric Oxide 1(5):373–385CrossRefPubMedGoogle Scholar
  47. 47.
    Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238(3):209–214CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M (2001) Nitric oxide-induced apoptosis in pancreatic cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 98:10845–10850CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Jia W, Loria RM, Park MA, Yacoub A, Dent P, Graf MR (2010) The neuro-steroid, 5-androstene 3β,17α diol; induces endoplasmic reticulum stress and autophagy through PERK/eIF2α signaling in malignant glioma cells and transformed fibroblasts. Int J Biochem Cell Biol 42(12):2019CrossRefPubMedGoogle Scholar
  50. 50.
    Talas ZS, Orun I, Ozdemir I, Erdogan K, Alkan A, Yılmaz I (2008) Antioxidative role of selenium against the toxic effect of heavy metals (Cd +2, Cr +3 ) on liver of rainbow trout ( Oncorhynchus mykiss Walbaum 1792). Fish Physiol Biochem 34(3):217–222CrossRefPubMedGoogle Scholar
  51. 51.
    Fischer JL, Lancia JK, Mathur A, Smith ML (2006) Selenium protection from DNA damage involves a Ref1/p53/Brca1 protein complex. Anticancer Res 26(2A):899–904PubMedGoogle Scholar
  52. 52.
    Bansal MP, Kaur P (2005) Selenium, a versatile trace element: current research implications. Indian J Exp Biol 43(12):1119–1129PubMedGoogle Scholar
  53. 53.
    Zhang ZW, Wang QH, Zhang JL, Li S, Wang XL, Xu SW (2012) Effects of oxidative stress on immunosuppression induced by selenium deficiency in chickens. Biol Trace Elem Res 149(3):352–361CrossRefPubMedGoogle Scholar
  54. 54.
    Liu LL, Zhang JL, Zhang ZW, Yao HD, Sun G, Xu SW (2014) Protective roles of selenium on nitric oxide-mediated apoptosis of immune organs induced by cadmium in chickens. Biol Trace Elem Res 159(1–3):199CrossRefPubMedGoogle Scholar
  55. 55.
    Yao L, Du Q, Yao H, Chen X, Zhang Z, Xu S (2015) Roles of oxidative stress and endoplasmic reticulum stress in selenium deficiency-induced apoptosis in chicken liver. Biometals 28(2):255–265CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.College of Veterinary MedicineNortheast Agricultural UniversityHarbinPeople’s Republic of China

Personalised recommendations