Advertisement

Biological Trace Element Research

, Volume 189, Issue 1, pp 186–193 | Cite as

Sodium Arsenite Injection Induces Ovarian Oxidative Stress and Affects Steroidogenesis in Rats

  • Hao Yu
  • Meiqian Kuang
  • Yalei Wang
  • Saif Rodeni
  • Quanwei Wei
  • Wei Wang
  • Dagan MaoEmail author
Article
  • 99 Downloads

Abstract

Oxidative stress is involved in the regulation of mammalian reproduction. The present study was conducted to detect the sodium arsenite-induced oxidative stress and alterations in the structure and steroidogenesis in rat ovary. Twenty female adult rats were injected i.p. with sodium arsenite (8 mg/kg BW, T) or 0.9% saline (C) for 16 days. The oxidative stress indexes and morphology of the liver, kidney, and ovary were detected using commercial kits and HE staining, respectively. The serum progesterone and estradiol were detected by RIA, and the ovarian steroidogenic gene expressions were detected by real-time PCR. Results showed that the ovarian activities of SOD and GSH-PX decreased (P < 0.05), while the ROS activity and MDA level increased (P < 0.05) in the T group. HE staining results showed that treatment with sodium arsenite damaged the ovarian morphology, resulting in reduced large and medium follicles and increased atretic follicles. Nonetheless, neither the liver nor kidney showed evident changes in the oxidative stress indexes or morphology after sodium arsenite treatment. The serum progesterone and estradiol levels decreased (P < 0.05) with the reduced expressions in the ovarian steroidogenic genes (StAR, P450scc, and 3β-HSD) (P < 0.05). In conclusion, sodium arsenite injection can induce ovarian oxidative stress in rats which set up an appropriate model for future studies of ovarian diseases as well as the toxic mechanism of arsenic in the reproduction.

Keywords

Ovary Oxidative stress Sodium arsenite Steroidogenesis 

Notes

Acknowledgments

We express our gratitude to Miss. Ngekure M.X Kavita from University of Namibia for reading/editing the manuscripts

Funding

This work was supported by the National Nature Science Foundation of China (No. 31501956) and the Fundamental Research Funds for the Central Universities (KJQN201608 and Y0201500204).

Compliance with Ethical Standards

All surgical procedures were approved by the Institutional Animal Care and Use Committee of Nanjing Agricultural University.

References

  1. 1.
    Al-Gubory KH, Fowler PA, Garrel C (2010) The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol 42(10):1634–1650.  https://doi.org/10.1016/j.biocel.2010.06.001 CrossRefGoogle Scholar
  2. 2.
    Das S, Chattopadhyay R, Ghosh S, Ghosh S, Goswami SK, Chakravarty BN, Chaudhury K (2006) Reactive oxygen species level in follicular fluid-embryo quality marker in IVF? Hum Reprod 21(9):2403–2407.  https://doi.org/10.1093/humrep/del156 CrossRefGoogle Scholar
  3. 3.
    Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM (2008) Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med 44(7):1295–1304.  https://doi.org/10.1016/j.freeradbiomed.2007.11.014 CrossRefGoogle Scholar
  4. 4.
    Gupta S, Agarwal A, Banerjee J, Alvarez JG (2007) The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstet Gynecol Surv 62(5):335–347.  https://doi.org/10.1097/01.ogx.0000261644.89300.df CrossRefGoogle Scholar
  5. 5.
    Kumar M, Pathak D, Venkatesh S, Kriplani A, Ammini AC, Dada R (2012) Chromosomal abnormalities & oxidative stress in women with premature ovarian failure (POF). Indian J Med Res 135(1):92–97CrossRefGoogle Scholar
  6. 6.
    Liu J, Zhang D (2012) The role of oxidative stress in the pathogenesis of polycystic ovary syndrome. Sichuan Da Xue Xue Bao Yi Xue Ban 43(2):187–190Google Scholar
  7. 7.
    Moti M, Amini L, Mirhoseini Ardakani SS, Kamalzadeh S, Masoomikarimi M, Jafarisani M (2015) Oxidative stress and anti-oxidant defense system in Iranian women with polycystic ovary syndrome. Iran J Reprod Med 13(6):373–378Google Scholar
  8. 8.
    Agarwal A, Gupta S, Sekhon L, Shah R (2008) Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal 10(8):1375–1403.  https://doi.org/10.1089/ars.2007.1964 CrossRefGoogle Scholar
  9. 9.
    Jeon SY, Hwang KA, Choi KC (2016) Effect of steroid hormones, estrogen and progesterone, on epithelial mesenchymal transition in ovarian cancer development. J Steroid Biochem Mol Biol 158:1–8.  https://doi.org/10.1016/j.jsbmb.2016.02.005 CrossRefGoogle Scholar
  10. 10.
    Ratnaike RN (2003) Acute and chronic arsenic toxicity. Postgrad Med J 79(933):391–396CrossRefGoogle Scholar
  11. 11.
    Ruiz-Ramos R, Lopez-Carrillo L, Rios-Perez AD, De Vizcaya-Ruiz A, Cebrian ME (2009) Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res 674(1–2):109–115.  https://doi.org/10.1016/j.mrgentox.2008.09.021 CrossRefGoogle Scholar
  12. 12.
    Zhang JQ, Shen M, Zhu CC, Yu FX, Liu ZQ, Ally N, Sun SC, Li K, Liu HL (2014) 3-Nitropropionic acid induces ovarian oxidative stress and impairs follicle in mouse. PLoS One 9(2):e86589.  https://doi.org/10.1371/journal.pone.0086589 CrossRefGoogle Scholar
  13. 13.
    Chattopadhyay S, Ghosh S, Chaki S, Debnath J, Ghosh D (1999) Effect of sodium arsenite on plasma levels of gonadotrophins and ovarian steroidogenesis in mature albino rats: duration-dependent response. J Toxicol Sci 24(5):425–431CrossRefGoogle Scholar
  14. 14.
    Chattopadhyay S, Ghosh S, Debnath J, Ghosh D (2001) Protection of sodium arsenite-induced ovarian toxicity by coadministration of L-ascorbate (vitamin C) in mature wistar strain rat. Arch Environ Contam Toxicol 41(1):83–89.  https://doi.org/10.1007/s002440010223 CrossRefGoogle Scholar
  15. 15.
    Chattopadhyay S, Pal Ghosh S, Ghosh D, Debnath J (2003) Effect of dietary co-administration of sodium selenite on sodium arsenite-induced ovarian and uterine disorders in mature albino rats. Toxicol Sci 75(2):412–422.  https://doi.org/10.1093/toxsci/kfg194 CrossRefGoogle Scholar
  16. 16.
    Manna P, Sinha M, Sil PC (2008) Protection of arsenic-induced testicular oxidative stress by arjunolic acid. Redox Rep 13(2):67–77.  https://doi.org/10.1179/135100008x259169 CrossRefGoogle Scholar
  17. 17.
    Wang A, Holladay SD, Wolf DC, Ahmed SA, Robertson JL (2006) Reproductive and developmental toxicity of arsenic in rodents: a review. Int J Toxicol 25(5):319–331.  https://doi.org/10.1080/10915810600840776 CrossRefGoogle Scholar
  18. 18.
    Nakareangrit W, Thiantanawat A, Visitnonthachai D, Watcharasit P, Satayavivad J (2016) Sodium arsenite inhibited genomic estrogen signaling but induced pER (Ser118) via MAPK pathway in breast cancer cells. Environ Toxicol 31(9):1133–1146.  https://doi.org/10.1002/tox.22122 CrossRefGoogle Scholar
  19. 19.
    Zhang C, Liu C, Li D, Yao N, Yuan X, Yu A, Lu C, Ma X (2010) Intracellular redox imbalance and extracellular amino acid metabolic abnormality contribute to arsenic-induced developmental retardation in mouse preimplantation embryos. J Cell Physiol 222(2):444–455.  https://doi.org/10.1002/jcp.21966 CrossRefGoogle Scholar
  20. 20.
    Deveci HS, Deveci I, Habesoglu M, Surmeli M, Kinis V, Eriman M, Gunes P, Yekrek M, Egeli E (2012) Histological evaluation of rat larynx in experimental polycystic ovary syndrome model. Eur Arch Otorhinolaryngol 269(8):1945–1950.  https://doi.org/10.1007/s00405-012-1978-7 CrossRefGoogle Scholar
  21. 21.
    Ettema AM, Amadio PC, Zhao C, Wold LE, An KN (2004) A histological and immunohistochemical study of the subsynovial connective tissue in idiopathic carpal tunnel syndrome. J Bone Joint Surg Am 86-A(7):1458–1466CrossRefGoogle Scholar
  22. 22.
    Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM (2010) Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. Plos One 5(12):e15558.  https://doi.org/10.1371/journal.pone.0015558 CrossRefGoogle Scholar
  23. 23.
    Wang XN, Roy SK, Greenwald GS (1991) In vitro DNA synthesis by isolated preantral to preovulatory follicles from the cyclic mouse. Biol Reprod 44(5):857–863CrossRefGoogle Scholar
  24. 24.
    Han XM, Tang R, Chen XJ, Xu B, Qin YF, Wu W, Hu YH, Xu B, Song L, Xia YK, Wang XR (2012) 2,2 ',4,4 '-Tetrabromodiphenyl ether (BDE-47) decreases progesterone synthesis through cAMP-PKA pathway and P450scc downregulation in mouse Leydig tumor cells. Toxicology 302(1):44–50.  https://doi.org/10.1016/j.tox.2012.07.010 CrossRefGoogle Scholar
  25. 25.
    Giustarini D, Dalle-Donne I, Tsikas D, Rossi R (2009) Oxidative stress and human diseases: origin, link, measurement, mechanisms, and biomarkers. Crit Rev Clin Lab Sci 46(5–6):241–281.  https://doi.org/10.3109/10408360903142326 CrossRefGoogle Scholar
  26. 26.
    Jhala DD, Chinoy NJ, Rao MV (2008) Mitigating effects of some antidotes on fluoride and arsenic induced free radical toxicity in mice ovary. Food Chem Toxicol 46(3):1138–1142.  https://doi.org/10.1016/j.fct.2007.11.009 CrossRefGoogle Scholar
  27. 27.
    Zhu J, Guo JJ, Lin JH, Hai-Zhi BU (2012) Research advances in models of hepatic and intestinal first-pass drug metabolism. Chin J Clin Pharmacol Ther 17(8):944–949Google Scholar
  28. 28.
    DeSesso JM, Jacobson CF, Scialli AR, Farr CH, Holson JF (1998) An assessment of the developmental toxicity of inorganic arsenic. Reprod Toxicol 12(4):385–433CrossRefGoogle Scholar
  29. 29.
    Ingec M, Isaoglu U, Yilmaz M, Calik M, Polat B, Alp HH, Kurt A, Gundogdu C, Suleyman H (2011) Prevention of ischemia-reperfusion injury in rat ovarian tissue with the on-off method. J Physiol Pharmacol 62(5):575–582Google Scholar
  30. 30.
    Tamura H, Takasaki A, Miwa I, Tanoguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K, Morioka H, Ishikawa H, Reiter RJ, Sugino N (2008) Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 44(3):280–287.  https://doi.org/10.1111/j.1600-079X.2007.00524.X CrossRefGoogle Scholar
  31. 31.
    Qin Y, Pan X, Tang TT, Zhou L, Gong XG (2011) Anti-proliferative effects of the novel squamosamide derivative (FLZ) on HepG2 human hepatoma cells by regulating the cell cycle-related proteins are associated with decreased ca(2+)/ROS levels. Chem Biol Interact 193(3):246–253.  https://doi.org/10.1016/j.cbi.2011.07.004 CrossRefGoogle Scholar
  32. 32.
    Xu Z, Garverick HA, Smith GW, Smith MF, Hamilton SA, Youngquist RS (1995) Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Biol Reprod 53(4):951–957CrossRefGoogle Scholar
  33. 33.
    Matsuda F, Inoue N, Manabe N, Ohkura S (2012) Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev 58(1):44–50CrossRefGoogle Scholar
  34. 34.
    Jiang X, Chen C, Zhao W, Zhang Z (2013) Sodium arsenite and arsenic trioxide differently affect the oxidative stress, genotoxicity and apoptosis in A549 cells: an implication for the paradoxical mechanism. Environ Toxicol Pharmacol 36(3):891–902.  https://doi.org/10.1016/j.etap.2013.08.002 CrossRefGoogle Scholar
  35. 35.
    Yao XF, Zheng BL, Bai J, Jiang LP, Zheng Y, Qi BX, Geng CY, Zhong LF, Yang G, Chen M, Liu XF, Sun XC (2015) Low-level sodium arsenite induces apoptosis through inhibiting TrxR activity in pancreatic beta-cells. Environ Toxicol Pharmacol 40(2):486–491.  https://doi.org/10.1016/j.etap.2015.08.003 CrossRefGoogle Scholar
  36. 36.
    Ghosh D, Chattopadhyay S, Debnath J (1999) Effect of sodium arsenite on adrenocortical activity in immature female rats: evidence of dose dependent response. J Environ Sci (China) 11(4):419–422Google Scholar
  37. 37.
    Tsai SC, Lu CC, Lin CS, Wang PS (2003) Antisteroidogenic actions of hydrogen peroxide on rat Leydig cells. J Cell Biochem 90(6):1276–1286.  https://doi.org/10.1002/jcb.10738 CrossRefGoogle Scholar
  38. 38.
    Scolastici C, Alves de Lima RO, Barbisan LF, Ferreira AL, Ribeiro DA, Salvadori DMF (2007) Lycopene activity against chemically induced DNA damage in Chinese hamster ovary cells. Toxicol In Vitro 21(5):840–845.  https://doi.org/10.1016/j.tiv.2007.01.020 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Hao Yu
    • 1
  • Meiqian Kuang
    • 1
  • Yalei Wang
    • 1
  • Saif Rodeni
    • 1
  • Quanwei Wei
    • 1
  • Wei Wang
    • 1
  • Dagan Mao
    • 1
    Email author
  1. 1.College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China

Personalised recommendations