Skip to main content
Log in

The Co-Induced Effects of Molybdenum and Cadmium on the Trace Elements and the mRNA Expression Levels of CP and MT in Duck Testicles

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

Abstract

To investigate the chronic toxicity of molybdenum (Mo) and cadmium (Cd) on the trace elements and the mRNA expression levels of ceruloplasmin (CP) and metallothionein (MT) in duck testicles, 120 healthy 11-day-old male ducks were randomly divided into six groups with 20 ducks in each group. Ducks were treated with the diet containing different dosages of Mo or Cd. The source of Mo and Cd was hexaammonium molybdate ([(NH4)6Mo7O24·4H2O]) and cadmium sulfate (3CdSO4·8H2O), respectively, in this study. After being treated for 60 and 120 days, ten male birds in each group were randomly selected and euthanized and then testicles were aseptically collected for determining the mRNA expression levels of MT and CP, antioxidant indexes, and contents of trace elements in the testicle. In addition, testicle tissues at 120 days were subjected to histopathological analysis with the optical microscope. The results showed that co-exposure to Mo and Cd resulted in an increase in malondialdehyde (MDA) level while decrease in xanthine oxidase (XOD) and catalase (CAT) activities. The mRNA expression level of MT gene was upregulated while CP was decreased in combination groups. Contents of Mo, copper (Cu), iron (Fe), and zinc (Zn) decreased in combined groups while Cd increased in Cd and combined groups at 120 days. Furthermore, severe congestion, low sperm count, and malformation were observed in low dietary of Mo combined with Cd group and high dietary of Mo combined with Cd group. Our results suggested that Mo and Cd might aggravate testicular degeneration synergistically through altering the mRNA expression levels of MT and CP, increasing lipid peroxidation through inhibiting related enzyme activities and disturbing homeostasis of trace elements in testicles. Interaction of Mo and Cd may have a synergistic effect on the testicular toxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–849

    Article  PubMed  CAS  Google Scholar 

  2. Donald G, Barceloux (1999) Molybdenum. Clin Toxicol 37:231–237

    Google Scholar 

  3. Hille R (2002) Molybdenum and tungsten in biology. Trends Biochem Sci 27:360–367

    Article  PubMed  CAS  Google Scholar 

  4. Davies TD, Pickard J, Hall KJ (2011) Acute molybdenum toxicity to rainbow trout and other fish. J Environ Eng Sci 4:481–485

    Article  Google Scholar 

  5. Swan DA, Creeper JH, White CL, Ridings M, Smith GM, Costa ND (1998) Molybdenum poisoning in feedlot cattle. Aust Vet J 76:345–349

    Article  PubMed  CAS  Google Scholar 

  6. Raisbeck MF, Siemion RS, Smith MA (2006) Modest copper supplementation blocks molybdenosis in cattle. J Vet Diagn Investig 18:566–572

    Article  Google Scholar 

  7. Bersényi A, Berta E, Kádár I, Glávits R, Szilágyi M, Fekete SG (2008) Effects of high dietary molybdenum in rabbits. Acta Vet Hung 56:41–55

    Article  PubMed  CAS  Google Scholar 

  8. Sharma AK, Parihar NS (1994) Pathology of experimental molybdenosis in goats. Ind J Anim Sci 64:114–119

    Google Scholar 

  9. Ostrom CA, Van Reen R, Miller CW (1961) Changes in the connective tissue of rats fed toxic diets containing molybdenum salts. J Dent Res 40:520–527

    Article  CAS  Google Scholar 

  10. Wang HW, Zhou BH, Zhang S, Guo HW, Zhang JL, Zhao J, Tian EJ (2015) Reproductive toxicity in male mice after exposure to high molybdenum and low copper concentrations. Toxicol Ind Health

  11. Cannino G, Ferruggia E, Luparello C, Rinaldi AM (2009) Cadmium and mitochondria. Mitochondrion 9:377–384

    Article  PubMed  CAS  Google Scholar 

  12. Manca D, Ricard AC, Trottier B, Chevalier G (1991) Studies on lipid peroxidation in rat tissues following administration of low and moderate doses of cadmium chloride. Toxicology 67:303–323

    Article  PubMed  CAS  Google Scholar 

  13. Satarug S, Nishijo M, Lasker JM, Edwards RJ, Moore MR (2006) Kidney dysfunction and hypertension: role for cadmium, P450 and heme oxygenases? Tohoku J Exp Med 208:179–202

    Article  PubMed  CAS  Google Scholar 

  14. Liu J, Cheng ML, Yang Q, Shan KR, Shen J, Zhou Y, Zhang X, Dill AL, Waalkes MP (2007) Blood metallothionein transcript as a biomarker for metal sensitivity: low blood metallothionein transcripts in arsenicosis patients from Guizhou, China. Environ Health Perspect 115:1101–1106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Yang S, Zhang Z, He J, Li J, Zhang J, Xing H, Xu S (2012) Ovarian toxicity induced by dietary cadmium in hen. Biol Trace Elem Res 148:53–60

    Article  PubMed  CAS  Google Scholar 

  16. 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 23:695–705

    Article  PubMed  CAS  Google Scholar 

  17. Benoff SH, Millan C, Hurley IR, Napolitano B, Marmar JL (2004) Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele. Hum Reprod 19:616–627

    Article  PubMed  CAS  Google Scholar 

  18. Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res 533:107–120

    Article  PubMed  CAS  Google Scholar 

  19. Prozialeck WC, Edwards JR (2012) Mechanisms of cadmium-induced proximal tubule injury: new insights with implications for biomonitoring and therapeutic interventions. J Pharmacol Exp Ther 343:2–12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Telisman S, Cvitković P, Jurasović J, Pizent A, Gavella M, Rocić B (2000) Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 108:45–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Xu DX, Shen HM, Zhu QX, Chua L, Wang QN, Chia SE, Ong CN (2003) The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 534:155–163

    Article  PubMed  CAS  Google Scholar 

  22. Cantin A, Crystal RG (1985) Oxidants, antioxidants and the pathogenesis of emphysema. Eur J Respir Dis Suppl 139:7–17

    PubMed  CAS  Google Scholar 

  23. Rajeshkumar S, Mini J, Munuswamy N (2013) Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. Ecotoxicol Environ Saf 98:8–18

    Article  PubMed  CAS  Google Scholar 

  24. Yang F, Cui H, Xiao J, Peng X, Deng J, Zuo Z (2011) Increased apoptotic lymphocyte population in the spleen of young chickens fed on diets high in molybdenum. Biol Trace Elem Res 140:308–316

    Article  PubMed  CAS  Google Scholar 

  25. Lasfer M, Vadrot N, Aoudjehane L, Conti F, Bringuier AF, Feldmann G, Reyl-Desmars F (2008) Cadmium induces mitochondria-dependent apoptosis of normal human hepatocytes. Cell Biol Toxicol 24:55–62

    Article  PubMed  CAS  Google Scholar 

  26. Martelli A, Rousselet E, Dycke C, Bouron A, Moulis JM (2006) Cadmium toxicity in animal cells by interference with essential metals. Biochimie 88:1807–1814

    Article  PubMed  CAS  Google Scholar 

  27. Khandare AL, Suresh P, Kumar PU, Lakshmaiah N, Manjula N, Rao GS (2005) Beneficial effect of copper supplementation on deposition of fluoride in bone in fluoride- and molybdenum-fed rabbits. Calcif Tissue Int 77:233–238

    Article  PubMed  CAS  Google Scholar 

  28. Xia B, Cao H, Luo J, Liu P, Guo X, Hu G, Zhang C (2015) The co-induced effects of molybdenum and cadmium on antioxidants and heat shock proteins in duck kidneys. Biol Trace Elem Res. doi:10.1007/s12011-015-0348-x

    Google Scholar 

  29. Liu X, Zuo N, Guan H, Han C, Xu SW (2013) Manganese-induced effects on cerebral trace element and nitric oxide of Hyline cocks. Biol Trace Elem Res 154:202–209

    Article  PubMed  CAS  Google Scholar 

  30. Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443

    Article  PubMed  CAS  Google Scholar 

  31. Korchazhkina O, Exley C, Andrew Spencer S (2003) Measurement by reversed-phase high-performance liquid chromatography of malondialdehyde in normal human urine following derivatisation with 2,4-dinitrophenylhydrazine. J Chromatogr B Anal Technol Biomed Life Sci 794:353–362

    Article  CAS  Google Scholar 

  32. Ozguner F, Koyu A, Cesur G (2005) Active smoking causes oxidative stress and decreases blood melatonin levels. Toxicol Ind Health 21: 21-26.

  33. Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    Article  PubMed  CAS  Google Scholar 

  34. Zhang M, He Z, Wen L, Wu J, Yuan L, Lu Y, Guo C, Zhu L, Deng S, Yuan H (2010) Cadmium suppresses the proliferation of piglet Sertoli cells and causes their DNA damage, cell apoptosis and aberrant ultrastructure. Reprod Biol Endocrinol 8:97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Kim J, Soh J (2009) Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicol Lett 188:45–51

    Article  PubMed  CAS  Google Scholar 

  36. Kaisman-Elbaz T, Sekler I, Fishman D, Karol N, Forberg M, Kahn N, Hershfinkel M, Silverman WF (2009) Cell death induced by zinc and cadmium is mediated by clusterin in cultured mouse seminiferous tubules. J Cell Physiol 220:222–229

    Article  PubMed  CAS  Google Scholar 

  37. Acharya UR, Mishra M, Patro J, Panda MK (2008) Effect of vitamins C and E on spermatogenesis in mice exposed to cadmium. Reprod Toxicol 25:84–88

    Article  PubMed  CAS  Google Scholar 

  38. Hamer DH (1986) Metallothionein. Annu Rev Biochem 55:913–951

    Article  PubMed  CAS  Google Scholar 

  39. Karin M (1985) Metallothionein: protein in search of function. Cell 41:9–10

    Article  PubMed  CAS  Google Scholar 

  40. Adachi K, Dote T, Dote E, Mitsui G, Kono K (2007) Strong acute toxicity, severe hepatic damage, renal injury and abnormal serum electrolytes after intravenous administration of cadmium fluoride in rats. J Occup Health 49:235–241

    Article  PubMed  CAS  Google Scholar 

  41. Wlostowski T, Krasowska A, Bonda E (2008) Joint effects of dietary cadmium and polychlorinated biphenyls on metallothionein induction, lipid peroxidation and histopathology in the kidneys and liver of bank voles. Ecotoxicol Environ Saf 69:403–410

    Article  PubMed  CAS  Google Scholar 

  42. Wolff NA, Lee WK, Thévenod F (2011) Role of Arf1 in endosomal trafficking of protein-metal complexes and cadmium-metallothionein-1 toxicity in kidney proximal tubule cells. Toxicol Lett 203:210–218

    Article  PubMed  CAS  Google Scholar 

  43. Masters BA, Kelly EJ, Quaife CL, Brinster RL, Palmiter RD (1994) Target disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc Natl Acad Sci U S A 91:584–588

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Klaassen CD, Liu J, Diwan BA (2009) Metallothionein protection of cadmium toxicity. Toxicol Appl Pharmacol 238:215–220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39:267–294

    Article  PubMed  CAS  Google Scholar 

  46. Kadrabová J, Madaric A, Ginter E (1993) Zinc and copper in the tissues and serum of cadmium intoxicated guinea-pigs: influence of vitamin C. Physiol Res 42:261–266

    PubMed  Google Scholar 

  47. Torres MA, Barros MP, Campos SC, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15

    Article  PubMed  CAS  Google Scholar 

  48. Nemmiche S, Chabane-Sari D, Kadri M, Guiraud P (2011) Cadmium chloride-induced oxidative stress and DNA damage in the human Jurkat T cell line is not linked to intracellular trace elements depletion. Toxicol in Vitro 25:191–198

    Article  PubMed  CAS  Google Scholar 

  49. Satarug S, Haswell-Elkins MR, Moore MR (2000) Safe levels of cadmium intake to prevent renal toxicity in human subjects. Br J Nutr 84:791–802

    PubMed  CAS  Google Scholar 

  50. Yao HD, Wu Q, Zhang ZW, Zhang JL, Li S, Huang JQ, Ren FZ, Xu SW, Wang XL, Lei XG (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of Se-deficient chicks. J Nutr 143:613–619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Cardin CJ, Mason J (1976) Molybdate and tungstate transfer by rat ileum. Competitive inhibition by sulphate. Biochim Biophys Acta 455:937–946

    Article  PubMed  CAS  Google Scholar 

  52. Chen X, Zhu YH, Cheng XY, Zhang ZW, Xu SW (2012) The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules 17:14565–14572

    Article  PubMed  CAS  Google Scholar 

  53. Ellingsen DG, Thomassen Y, Aaseth J, Alexander J (1997) Cadmium and selenium in blood and urine related to smoking habits and previous exposure to mercury vapour. J Appl Toxicol 17:337–343

    Article  PubMed  CAS  Google Scholar 

  54. Wasowicz W, Gromadzińska J, Rydzyński K (2001) Blood concentration of essential trace elements and heavy metals in workers exposed to lead and cadmium. Int J Occup Med Environ Health 14:23–229

    Google Scholar 

  55. White CL, Caldwalader TK, Hoekstra WG, Pope AL (1989) Effects of copper and molybdenum supplements on the copper and selenium status of pregnant ewes and lambs. J Anim Sci 67:803–809

    PubMed  CAS  Google Scholar 

  56. Abdel Rahim AG, Arthur JR, Mills CF (1986) Effects of dietary copper, cadmium, iron, molybdenum and manganese on selenium utilization by the rat. J Nutr 116:403–411

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Science Foundation of China (31260625) and the training Plan for Young Scientists of Jiangxi province (No. 2014BCB23040, Nanchang, P. R. China). All authors thank all members of the team for their help in the experimental process in clinical veterinary medicine laboratory in the College of Animal Science and Technology, Jiangxi Agricultural University. The authors thank Ziwei Zhang for correcting common errors in this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Huabin Cao or Caiying Zhang.

Additional information

Bing Xia and Hua Chen are equally the first authors.

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

Xia, B., Chen, H., Hu, G. et al. The Co-Induced Effects of Molybdenum and Cadmium on the Trace Elements and the mRNA Expression Levels of CP and MT in Duck Testicles. Biol Trace Elem Res 169, 331–340 (2016). https://doi.org/10.1007/s12011-015-0410-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-015-0410-8

Keywords

Navigation