Skip to main content
SpringerLink
Log in

Effect of Stress from Cadmium Combined with Different Levels of Molybdenum on Serum Free Radical and Expression of Related Apoptosis Genes in Goat Livers

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

Abstract

Molybdenum (Mo) is an essential element for human beings and animals; however, high dietary intake of Mo can lead to adverse reactions. Cadmium (Cd) is one of the major transitional metals which have toxic effects in animals. The toxicity of simple Cd or Mo has been researched frequently. However, the toxicity of Mo combined with Cd was rarely studied. To investigate the toxicity of Mo combined with Cd in liver of goats, 36 Boer goats were randomly divided into four groups and assigned with one of the three oral treatments of CdCl2 (0.5 mg kg−1 Cd) and [(NH4)6Mo7O24·4H2O] (15 mg kg−1 Mo, group I; 30 mg kg−1 Mo, group II; 45 mg kg−1 Mo, group III), while the control group received deionized water. Blood samples were collected on days 0, 10, 20, 30, 40, and 50 to determine antioxidant indices in serum. In addition, liver tissues were collected on days 0, 25, and 50 for detecting the messenger RNA (mRNA) expression levels of Bcl-2 and Bax. Moreover, liver tissues at 50 days were subjected to histopathological analysis with the optical microscope. The results revealed a significant increase (P < 0.05 or P < 0.01) in the levels of nitric oxide (NO), malonaldehyde (MDA), and the activity of nitrix oxide synthase (NOS) and a significant decline (P < 0.05) in the activities of total superoxide dismutase (T-SOD) and total antioxidative capacity (T-AOC). The mRNA expression level of Bcl-2 was suppressed (P < 0.05), while the expression of Bax was increased (P < 0.05) in liver. The histopathological changes were observed in the liver of goats including a small amount of erythrocyte, the unclear structure of hepatic cord and hepatic sinusoid, granular degeneration, vacuolar degeneration, and steatosis. In conclusion, combined chronic toxicity of Cd with different levels of Mo might induce goat liver cell apoptosis and cause oxidative stress in serum, and it showed a possible synergistic relationship between the two elements.

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. Gu X, Chen R, Hu G, Zhuang Y, Luo J, Zhang C, Guo X, Huang A, Cao H (2015) Cell apoptosis of caprine spleen induced by toxicity of cadmium with different levels of molybdenum. Environ Toxicol Pharmacol 40(1):49–56. doi:10.1016/j.etap.2015.05.001

    Article  CAS  PubMed  Google Scholar 

  2. Turnlund JR (2002) Molybdenum metabolism and requirements in humans. Metal Ions Biological Syst 39:727–739

    CAS  Google Scholar 

  3. Gu X, Ali T, Chen R, Hu G, Zhuang Y, Luo J, Cao H, Han B (2015) In vivo studies of molybdenum-induced apoptosis in kidney cells of caprine. Biol Trace Elem Res 165(1):51–58. doi:10.1007/s12011-015-0238-2

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  5. Sharma AK, Parihar NS (1994) Clinicopathology of induced molybdenum toxicity in young goats. J Anim Sci 64:120–125

    CAS  Google Scholar 

  6. Markesbery WR, Kryscio RJ, Lovell MA, Morrow JD (2005) Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment. Ann Neurol 58(5):730–735

    Article  CAS  PubMed  Google Scholar 

  7. Marettová E, Maretta M, Legáth J, Legath (2015) Toxic effects of cadmium on testis of birds and mammals: a review. Anim Reprod Sci 155:1–10

  8. Shih CM, Ko WC, Wu JS, Wei YH, Wang LF, Chang EE, Lo TY, Cheng HH, Chen CT (2004) Mediating of caspase-independent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 fibroblasts. J Cell Biochem 91(2):384–397

    Article  CAS  PubMed  Google Scholar 

  9. Park SJ, Lee JR, Jo MJ, Park SM, Ku SK, Kim SC (2013) Protective effects of Korean red ginseng extract on cadmium-induced hepatic toxicity in rats. J Ginseng Res 37(1):37–44. doi:10.5142/jgr.2013.37.37

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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 168(1):261–268. doi:10.1007/s12011-015-0348-x

    Article  CAS  PubMed  Google Scholar 

  11. Rautio A, Kunnasranta M, Valtonen A, Ikonen M, Hyvärinen H, Holopainen IJ, Kukkonen JV (2010) Sex, age, and tissue specific accumulation of eight metals, arsenic, and selenium in the European hedgehog (Erinaceus europaeus). Arch Environ Contam Toxicol 59(4):642–651. doi:10.1007/s00244-010-9503-8

    Article  CAS  PubMed  Google Scholar 

  12. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36

    Article  PubMed  PubMed Central  Google Scholar 

  13. Horiguchi H, Oguma E, Kayama F (2011) Cadmium induces anemia through interdependent progress of hemolysis, body iron accumulation, and insufficient erythropoietin production in rats. Toxicol Sci 122:198–210. doi:10.1093/toxsci/kfr100

    Article  CAS  PubMed  Google Scholar 

  14. Sahin E, Gümüşlü S (2004) Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 48(4):165–171

    Article  CAS  PubMed  Google Scholar 

  15. Bae DS, Gennings C, Carter Jr WH, Yang RS, Campain JA (2001) Toxicological interactions among arsenic, cadmium, chromium, and lead in human keratinocytes. Toxicol Sci 63(1):132–142

    Article  CAS  PubMed  Google Scholar 

  16. Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88(11):1549–1559

    Article  CAS  PubMed  Google Scholar 

  17. Boveri M, Pazos P, Gennari A, Casado J, Hartung T, Prieto P (2004) Comparison of the sensitivity of different toxicological endpoints in caco-2 cells after cadmium chloride treatment. Arch Toxicol 78(4):201–206

    Article  CAS  PubMed  Google Scholar 

  18. Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238(3):209–214. doi:10.1016/j.taap.2009.01.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Prozialeck WC (2000) Evidence that E-cadherin may be a target for cadmium toxicity in epithelial cells. Toxicol Appl Pharmacol 164(3):231–249

    Article  CAS  PubMed  Google Scholar 

  20. Simmons SO, Fan CY, Yeoman K, Wakefield J, Ramabhadran R (2011) NRF2 oxidative stress induced by heavy metals is cell type dependent. Current Chem Genomics 5:1–12. doi:10.2174/1875397301105010001

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. Smith GM, White CL (1997) A molybdenum–sulfur–cadmium interaction in sheep. Aust Vet J 48:147–154

    CAS  Google Scholar 

  23. Deosthale YG, Gopalan C (1974) The effect of molybdenum levels in sorghum (Sorghum vulgare pers.) on uric acid and copper excretion in man. Br J Nutr 31(3):351–355

    Article  CAS  PubMed  Google Scholar 

  24. Işlekel S, Işlekel H, Güner G, Ozdamar N (1999) Alterations in superoxide dismutase, glutathione peroxidase and catalase activities in experimental cerebral ischemia-reperfusion. Res Exp Med 199(3):167–176

    Article  Google Scholar 

  25. Shen WY, Fu LL, Li WF, Zhu YR (2010) Effect of dietary supplementation with Bacillus subtilis on the growth, performance, immune response and antioxidant activities of the shrimp (Litopenaeus vannamei). Aquac Res 41(11):1691–1698

    Article  CAS  Google Scholar 

  26. Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol 100(1–2):173–176

    CAS  Google Scholar 

  27. Zhong L, Wang L, Xu L, Liu Q, Jiang L, Zhi Y, Lu W, Zhou P (2015) The role of nitric oxide synthase in an early phase Cd-induced acute cytotoxicity in MCF-7 cells. Biol Trace Elem Res 164(1):130–138. doi:10.1007/s12011-014-0187-1

    Article  CAS  PubMed  Google Scholar 

  28. Bekheet SH, Awadalla EA, Salman MM, Hassan MK (2013) Prevention of hepatic and renal toxicity with bradykinin potentiating factor (BPF) isolated from Egyptian scorpion venom (buthus occitanus) in gentamicin treated rats. Tissue Cell 45:89–94. doi:10.1016/j.tice.2012.09.006

    Article  CAS  PubMed  Google Scholar 

  29. 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. Toxicology and Industrial hEalth [Epub Ahead of Print]

  30. Jia Y, Lin J, Mi Y, Zhang C (2011) Quercetin attenuates cadmium-induced oxidative damage and apoptosis in granulosa cells from chicken ovarian follicles. Reprod Toxicol 31(4):477–485

    Article  CAS  PubMed  Google Scholar 

  31. Amara S, Douki T, Garrel C, Favier A, Ben Rhouma K, Sakly M, Abdelmelek H (2011) Effects of static magnetic field and cadmium on oxidative stress and DNA damage in rat cortex brain and hippocampus. Toxicol Ind Health 27(2):99–106. doi:10.1177/0748233710381887

    Article  CAS  PubMed  Google Scholar 

  32. Tsujimoto Y, Shimizu S (2000) Bcl-2 family: life-or-death switch. FEBS Lett 466(1):6–10

    Article  CAS  PubMed  Google Scholar 

  33. Matsumoto A, Isomoto H, Nakayama M, Hisatsune J, Nishi Y (2011) Helicobacter pylori VacA reduces the cellular expression of STAT3 and prosurvival Bcl-2 family proteins, Bcl-2 and Bcl-XL, leading to apoptosis in gastric epithelial cells. Digest Dis Sci 56(4):999–1006. doi:10.1007/s10620-010-1420-1

    Article  CAS  PubMed  Google Scholar 

  34. Mertens HJ, Heineman MJ, Evers JL (2002) The expression of apoptosis-related proteins Bcl-2 and Ki67 in endometrium of ovulatory menstrual cycles. Gynecol Obstet Investig 53(4):224–230

    Article  CAS  Google Scholar 

  35. Cory S, Huang DC, Adams JM (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22(53):8590–8607

    Article  CAS  PubMed  Google Scholar 

  36. Li M, Xia T, Jiang CS, Li LJ, Fu JL, Zhou ZC (2003) Cadmium directly induced the opening of membrane permeability pore of mitochondria which possibly involved in cadmium-triggered apoptosis. Toxicology 194(1–2):19–33

    Article  CAS  PubMed  Google Scholar 

  37. Xiao, J, Cui, H. M, Yang, F, Peng, X, Cui, Y (2011) Effect of dietaryhigh molybdenum on the cell cycle and apoptosis of kidney in broilers. Biol Trace Elem Res 142:523–531

  38. Liu S, Xu FP, Yang ZJ, Li M, Min YH, Li S (2014) Cadmium-induced injury and the ameliorative effects ofselenium on chicken spleen lymphocytes: mechanisms of oxidative stress and apoptosis. Biol Trace Elem Res 160(3):340–351. doi:10.1007/s12011-014-0070-0

    Article  CAS  PubMed  Google Scholar 

  39. Zhou Z, Wang C, Liu H, Huang Q, Wang M, Lei Y (2013) Cadmium induced cell apoptosis, DNA damage, decreased DNA repair capacity, and genomic instability during malignant transformation of human bronchial epithelial cells. Inter J Med Sci 10(11):1485–1496. doi:10.7150/ijms.6308

    Article  Google Scholar 

  40. Pulido MD, Parrish AR (2003) Metal-induced apoptosis: mechanisms. Mutat Res 533(1–2):227–241

    Article  CAS  PubMed  Google Scholar 

  41. Salińska A, Włostowski T, Zambrzycka E (2012) Effect of dietary cadmium and/or lead on histopathological changes in the kidneys and liver of bank voles myodes glareolus kept in different group densities. Ecotoxicology 21(8):2235–2243. doi:10.1007/s10646-012-0979-z

    Article  PubMed  PubMed Central  Google Scholar 

  42. Milton Prabu S, Muthumani M, Shagirtha K (2012) Protective effect of Piper betle leaf extract against cadmium-induced oxidative stress and hepatic dysfunction in rats. Saudi J Biological Sci 19(2):229–239. doi:10.1016/j.sjbs.2012.01.005

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the Program of the National Natural Science Foundation (No. 31101863, Beijing, People’s Republic of China), Training Plan for Young Scientists of Jiangxi Province (No. 2014BCB23040, Nanchang, People’s Republic of China), and Educational Departmental Science Foundation of Jiangxi Province (No. GJJ14294, Nanchang, People’s Republic of China) to Huabin Cao.

Author information

Authors and Affiliations

  1. Institute of Animal Population Health, College of Animal Science and Technology, Jiangxi Agriculture University, No. 1101 Zhimin Avenue, Economic and Technological Development District, Nanchang, 330045, Jiangxi, People’s Republic of China

    Huabin Cao, Chenghong Xing, Yu Zhuang, Xiaolong Gu, Junrong Luo, Xiaoquan Guo, Ping Liu, Caiying Zhang & Guoliang Hu

Authors
  1. Huabin Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chenghong Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaolong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junrong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoquan Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ping Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Caiying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guoliang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Caiying Zhang or Guoliang Hu.

Additional information

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

Huabin Cao, Chenghong Xing and Yu Zhuang are the equal first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, H., Xing, C., Zhuang, Y. et al. Effect of Stress from Cadmium Combined with Different Levels of Molybdenum on Serum Free Radical and Expression of Related Apoptosis Genes in Goat Livers. Biol Trace Elem Res 172, 346–353 (2016). https://doi.org/10.1007/s12011-015-0610-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-015-0610-2

Keywords

Search

Navigation