Abstract
To investigate the effects of molybdenum (Mo) combined with cadmium (Cd) on the antioxidant function and the mRNA expression levels of apoptosis-related genes in duck ovaries, 60 healthy 11-old-day female ducks were treated with hexaammonium molybdate ([(NH4)6Mo7O24·4H2O]) or/and cadmium sulfate (3CdSO4·8H2O) at different doses on a daily basis for 120 days. On the 120th day, ten female birds in each group were euthanized, and the ovaries and blood were collected to determine the antioxidant indexes and the mRNA expression levels of Bak-1, Bcl-2, and caspase-3 in ovaries. In addition, ovary tissues were subjected to histopathological analysis with optical microscope. The total antioxidant capacity (T-AOC) and superoxide dismutase (SOD) activity decreased significantly (P < 0.01) in treated groups comparing with control while the nitric oxide synthase (NOS) activity increased (P < 0.01) both in ovary tissue and serum. The Bak-1 and caspase-3 expressions were upregulated while the Bcl-2 was downgraded by Mo or/and Cd. Biomolecules were affected in all metal-treated groups, whereas combined-treated animals showed greater effects. What is more, pathological damage in Mo and Cd combination treated groups was more severe. The results from the present study indicated that Mo or/and Cd caused oxidative stress and apoptosis in duck ovaries. Combination of Mo and Cd showed additive or synergistic effect leading to apoptosis and oxidative stress, and the pathway might be the mitochondrial pathway.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12011-015-0514-1/MediaObjects/12011_2015_514_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12011-015-0514-1/MediaObjects/12011_2015_514_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12011-015-0514-1/MediaObjects/12011_2015_514_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12011-015-0514-1/MediaObjects/12011_2015_514_Fig4_HTML.gif)
Similar content being viewed by others
References
International Agency for Research on Cancer (1993) Beryllium, cadmium, mercury and exposures in the glass manufacturing industry. International Agency for Research on Cancer Monographs on the Evaluation of Carcinogenic Risks to Humans. IARC, Lion, vol. 58, pp. 119–237
Wang Y, Maud CO, Ferrari ZH, Yousafzai AM, Chivers DP, Niyogi S (2014) The effects of chronic exposure to environmentally relevant levels of waterborne cadmium on reproductive capacity and behaviour in fathead minnows. Arch Environ Contam Toxicol 67:181–191. doi:10.1007/s00244-014-0018-6
Laxmipriya P, Nampoothiri AA, Gupta S (2007) Effect of co-exposure to lead and cadmium on antioxidant status in rat ovarian granulose cells. Arch Toxicol 81:145–150. doi:10.1007/s00204-006-0133-x
Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940
Banfalvi G, Ujvarosi K, Trencsenyi G, Somogyi C, Nagy G, Basnakian A (2007) Cell culture density dependent toxicity and chromatin changes upon cadmium treatment in murine pre-B-cells. Apoptosis 12:1219–1228. doi:10.1007/s10495-006-0045-5
Liu LL, Zhang JL, Zhang ZW, Yao HD, Sun G, Xu SW (2015) Protective roles of selenium on nitric oxide-mediated apoptosis of immune organs induced by cadmium in chickens. Biol Trace Elem Res 159:199–209. doi:10.1007/s12011-014-0007-7
Yuan G, Dai S, Yin Z et al (2014) Sub-chronic lead and cadmium co-induce apoptosis protein expression in liver and kidney of rats. Int J Clin Exp Pathol 7:2905–2914
Amutha C, Subramanian P (2013) Cadmium alters the reproductive endocrine disruption and enhancement of growth in the early and adult stages of Oreochromis mossambicus. Fish Physiol Biochem 39:351–361. doi:10.1007/s10695-012-9704-3
Angenard G, Muczynski V, Coffigny H et al (2010) Cadmium increases human fetal germ cell apoptosis. Environ Health Perspect 118:331–337
Samuel JB, Stanley JA, Princess RA, Shanthi P, Sebastian MS (2011) Gestational cadmium exposure-induced ovotoxicity delays puberty through oxidative stress and impaired steroid hormone levels. J Med Toxicol 7:195–204. doi:10.1007/s13181-011-0143-9
Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847
Davies TD, Pickard J, Hall KJ (2011) Acute molybdenum toxicity to rainbow trout and other fish. J Environ Eng Sci 4:481–485
Swan DA, Creeper JH, White CL, Ridings M, Smith GM, Costa ND (1998) Molybdenum poisoning in feedlot cattle. Aust Vet J 76:345–349
Raisbeck MF, Siemion RS, Smith MA (2006) Modest copper supplementation blocks molybdenosis in cattle. J Vet Diagn Investig 18:566–572
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 148:53–60. doi:10.1007/s12011-012-9343-7
Su M, Mei Y, Sinha S (2013) Role of the crosstalk between autophagy and apoptosis in cancer. J Oncol. doi:10.1155/2013/102735
Ma W, Xu W, Xu H, Chen Y, He Z, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335
Xiaolong G, Ali T, Chen R, Yu GH, Zhuang JL, Cao H, Han B (2015) In vivo studies of molybdenum-induced apoptosis in kidney cells of caprine. Biol Trace Elem Res 165:51–58. doi:10.1007/s12011-015-0238-2
Zhang YL, Liu FJ, Chen XL, Zhang ZQ, Shu RZ, Yu XL, Zhai XW, Jin LJ, Ma XG, Qi Q, Liu ZJ (2013) Dual effects of molybdenum on mouse oocyte quality and ovarian oxidative stress. Syst Biol Reprod Med 59:312–318. doi:10.3109/19396368.2013.826296
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
Cao H, Zhang M, Xia B, Xiong J, Zong Y, Hu G, Zhang C (2015) Effects of molybdenum or/and cadmium on mRNA expression levels of inflammatory cytokines and HSPs in duck spleens. Biol Trace Elem Res. doi:10.1007/s12011-015-0442-0
Xia B, Chen H, Hu G, Wang L, Cao H, Zhang C (2015) 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. doi:10.1007/s12011-015-0410-8
Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular mechanisms of cadmium carcinogenesis. Toxicology 192:117–195
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 164:130–138. doi:10.1007/s12011-014-0187-1
Patra RC, Swarup D, Senapati SK (1999) Effects of cadmium on lipid peroxides and superoxide dismutase in hepatic, renal and testicular tissue in rats. Vet Human Toxicol 41:65–67
Han XY, Xu ZR, Wang YZ, Huang QC (2006) Effect of cadmium on lipid peroxidation and activities of antioxidant enzymes in growing pigs. Biol Trace Elem Res 110:251–263
Kumchai J, Huang J-Z, Lee C-Y, Chen F-C, Chin S-W (2013) Proline partially overcomes excess molybdenum toxicity in cabbage seedlings grown in vitro. Genet Mol Res 12:5589–5601
Li JL, Jiang CY, Li S, Xu SW (2013) Cadmium induced hepatotoxicity in chickens (Gallus domesticus) and ameliorative effect by selenium. Ecotoxicol Environ Saf 96:103–109. doi:10.1016/j.ecoenv
Bekheet SHM (2011) Comparative effects of repeated administration of cadmium chloride during pregnancy and lactation and selenium protection against cadmium toxicity on some organs in immature rats’ offsprings. Biol Trace Elem Res 144:1008–1023. doi:10.1007/s12011-011-9084-z
Wang C, Ma W, Yuhong S (2013) NF-κB pathway contributes to cadmium-induced apoptosis of porcine granulosa cells. Biol Trace Elem Res 153:403–410. doi:10.1007/s12011-013-9650-7
Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501
Sun YL, Zhang J, Ping ZG, Wang CQ, Sun YF, Chen L, Li XY, Li CJ, Zhu XL, Liu Z, Zhang W, Zhou X (2011) Relationship between apoptosis and proliferation in granulosa and theca cells of cystic follicles in sows. Reprod Dom Anim. doi:10.1111/j.1439-0531.2011. 01929
Xiao J, Cui H-M, Yang F (2011) Effect of dietary high molybdenum on the cell cycle and apoptosis of kidney in broilers. Biol Trace Elem Res 142:523–531
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 40:49–56. doi:10.1016/j.etap.2015.05.001
Eleawa SM, Alkhateeb MA, Alhashem FH, Bin-Jaliah I, Sakr HF, Elrefaey HM, Elkarib AO, Alessa RM, Haidara MA, Shatoor AS, Khalil MA (2014) Resveratrol reverses cadmium chloride-induced testicular damage and subfertility by downregulating p53 and Bax and upregulating gonadotropins and Bcl-2 gene expression. J Reprod Dev 60:115–127
Raisbeck MF, Siemion RS, Smith MA (2006) Modest copper supplementation blocks molybdenosis in cattle. J Vet Diagn Invest 18:566–572
Acknowledgments
This study was supported by the National Science Foundation of China (31260625), the Technology R&D Program of Jiangxi Province (20122BBF60078), and the Training Plan for Young Scientists of Jiangxi province (No. 2014BCB23040). 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.
Author information
Authors and Affiliations
Corresponding authors
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, Bing Xia and Mengmeng Zhang contributed equally to this work.
Rights and permissions
About this article
Cite this article
Cao, H., Xia, B., Zhang, M. et al. Changes of Antioxidant Function and the mRNA Expression Levels of Apoptosis Genes in Duck Ovaries Caused by Molybdenum or/and Cadmium. Biol Trace Elem Res 171, 410–418 (2016). https://doi.org/10.1007/s12011-015-0514-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-015-0514-1