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The beneficial effects of polyethylene glycol-superoxide dismutase on ovarian tissue culture and transplantation

  • Fertility Preservation
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Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

Reducing the ischemic damage from free radicals that is inflicted on ovarian tissue is critical for successful ovarian tissue transplantation. Polyethylene glycol-superoxide dismutase (PEG-SOD) is mimetic of superoxide dismutase (SOD) and powerful free radical scavenger acts by reducing superoxide anions. The objective of study was to evaluate effects of PEG-SOD on mouse ovarian tissues in in vitro culture and in autotransplantation.

Methods

Ovaries were collected and randomly divided into four groups that received different doses of PEG-SOD. To assess effects of PEG-SOD on in vitro cultures, four different doses of PEG-SOD were applied to in vitro culture media during in vitro culturing following ovarian tissue vitrification and warming. To evaluate effects of PEG-SOD on ovarian tissue transplantation, four different doses of PEG-SOD were applied for 2, 7, and 21 days to mice following vitrified-warmed mouse ovarian tissue autotransplantation.

Results

The percentage of primordial follicles was maintained at the highest dose of PEG-SOD for 2 h in vitro, and there was a significant decrease in the percentage of apoptotic follicles at 2 h, but not at later time points. The highest dose of PEG-SOD also maintained primordial, primary, and secondary follicles 2 days post-transplantation, but only primordial follicles were maintained up to 21 days after transplantation.

Conclusions

PEG-SOD is protective mainly toward primordial follicles only for a short interval in vitro, presumably via antioxidant effects. PEG-SOD may be a promising additive for preserving ovarian tissue integrity, at least for primordial follicles, up to 21 days post-transplantation.

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References

  1. Donnez J, Dolmans M-M. Fertility preservation in women. Nat Rev Endocrinol. 2013;9(12):735–49. doi:10.1038/nrendo.2013.205.

    Article  CAS  PubMed  Google Scholar 

  2. Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM. Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update. 2006;12(5):519–35. doi:10.1093/humupd/dml032.

    Article  PubMed  Google Scholar 

  3. Kim SS, Yang HW, Kang HG, Lee HH, Lee HC, Ko DS, et al. Quantitative assessment of ischemic tissue damage in ovarian cortical tissue with or without antioxidant (ascorbic acid) treatment. Fertil Steril. 2004;82(3):679–85. doi:10.1016/j.fertnstert.2004.05.022.

    Article  CAS  PubMed  Google Scholar 

  4. Soleimani R, Heytens E, Oktay K. Enhancement of neoangiogenesis and follicle survival by sphingosine-1-phosphate in human ovarian tissue xenotransplants. PLoS One. 2011;6(4), e19475. doi:10.1371/journal.pone.0019475.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Hancke K, Walker E, Strauch O, Gobel H, Hanjalic-Beck A, Denschlag D. Ovarian transplantation for fertility preservation in a sheep model: can follicle loss be prevented by antiapoptotic sphingosine-1-phosphate administration? Gynecol Endocrinol Off J Int Soc Gynecol Endocrinol. 2009;25(12):839–43. doi:10.3109/09513590903159524.

    Article  CAS  Google Scholar 

  6. Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, et al. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93(5):1676–85. doi:10.1016/j.fertnstert.2009.04.048.

    Article  PubMed  Google Scholar 

  7. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update. 2009;15(6):649–65. doi:10.1093/humupd/dmp021.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Zhang HJ, Yan T, Oberley TD, Oberley LW. Comparison of effects of two polymorphic variants of manganese superoxide dismutase on human breast MCF-7 cancer cell phenotype. Cancer Res. 1999;59(24):6276–83.

    CAS  PubMed  Google Scholar 

  9. Dolgachev V, Oberley LW, Huang TT, Kraniak JM, Tainsky MA, Hanada K, et al. A role for manganese superoxide dismutase in apoptosis after photosensitization. Biochem Biophys Res Commun. 2005;332(2):411–7. doi:10.1016/j.bbrc.2005.04.141.

    Article  CAS  PubMed  Google Scholar 

  10. Chan PH. Role of oxidants in ischemic brain damage. Stroke J Cereb Circul. 1996;27(6):1124–9.

    Article  CAS  Google Scholar 

  11. Mossman BT, Marsh JP. Evidence supporting a role for active oxygen species in asbestos-induced toxicity and lung disease. Environ Health Perspect. 1989;81:91–4.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Galinanes M, Qiu Y, Ezrin A, Hearse DJ. PEG-SOD and myocardial protection. Studies in the blood- and crystalloid-perfused rabbit and rat hearts. Circulation. 1992;86(2):672–82.

    Article  CAS  PubMed  Google Scholar 

  13. Reddy MK, Labhasetwar V. Nanoparticle-mediated delivery of superoxide dismutase to the brain: an effective strategy to reduce ischemia-reperfusion injury. FASEB J Off Pub Fed Am Soc Experimen Biol. 2009;23(5):1384–95. doi:10.1096/fj.08-116947.

    CAS  Google Scholar 

  14. Werns SW, Lucchesi BR. Free radicals and ischemic tissue injury. Trends Pharmacol Sci. 1990;11(4):161–6. doi:10.1016/0165-6147(90)90068-j.

    Article  CAS  PubMed  Google Scholar 

  15. Youm HW, Lee JR, Lee J, Jee BC, Suh CS, Kim SH. Optimal vitrification protocol for mouse ovarian tissue cryopreservation: effect of cryoprotective agents and in vitro culture on vitrified-warmed ovarian tissue survival. Human Rep (Oxford, England). 2014;29(4):720–30. doi:10.1093/humrep/det449.

    Article  CAS  Google Scholar 

  16. Lundy T, Smith P, O'Connell A, Hudson NL, McNatty KP. Populations of granulosa cells in small follicles of the sheep ovary. J Reprod Fertil. 1999;115(2):251–62.

    Article  CAS  PubMed  Google Scholar 

  17. Gandolfi F, Paffoni A, Papasso Brambilla E, Bonetti S, Brevini TA, Ragni G. Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil Steril. 2006;85 Suppl 1:1150–6. doi:10.1016/j.fertnstert.2005.08.062.

    Article  PubMed  Google Scholar 

  18. Kim SS, Battaglia DE, Soules MR. The future of human ovarian cryopreservation and transplantation: fertility and beyond. Fertil Steril. 2001;75(6):1049–56.

    Article  CAS  PubMed  Google Scholar 

  19. Martinez-Madrid B, Donnez J, Van Eyck AS, Veiga-Lopez A, Dolmans MM, Van Langendonckt A. Chick embryo chorioallantoic membrane (CAM) model: a useful tool to study short-term transplantation of cryopreserved human ovarian tissue. Fertil Steril. 2009;91(1):285–92. doi:10.1016/j.fertnstert.2007.11.026.

    Article  PubMed  Google Scholar 

  20. Bigaud M, Gfeller P, Deveze S, Vogt G, Evenou JP, Bruns C, et al. Transplantation-induced ischemia/reperfusion injury in the rat heart. Transplant Proc. 1998;30(5):2311–3.

    Article  CAS  PubMed  Google Scholar 

  21. Guarrera JV, Polyak MM, Arrington B, Boykin J, Brown T, Jean-Jacques MA, et al. Pushing the envelope in renal preservation; improved results with novel perfusate modifications for pulsatile machine perfusion of cadaver kidneys. Transplant Proc. 2004;36(5):1257–60. doi:10.1016/j.transproceed.2004.04.083.

    Article  CAS  PubMed  Google Scholar 

  22. Cha SK, Shin DH, Kim BY, Yoon SY, Yoon TK, Lee WS, et al. Effect of human endothelial progenitor cell (EPC)- or mouse vascular endothelial growth factor-derived vessel formation on the survival of vitrified/warmed mouse ovarian grafts. Reprod Sci (Thousand Oaks, Calif). 2014. doi:10.1177/1933719113518983.

    Google Scholar 

  23. Carillon J, Rouanet JM, Cristol JP, Brion R. Superoxide dismutase administration, a potential therapy against oxidative stress related diseases: several routes of supplementation and proposal of an original mechanism of action. Pharm Res. 2013;30(11):2718–28. doi:10.1007/s11095-013-1113-5.

    Article  CAS  PubMed  Google Scholar 

  24. Morse H, Elfving M, Lindgren A, Wolner-Hanssen P, Andersen CY, Ora I. Acute onset of ovarian dysfunction in young females after start of cancer treatment. Pediatr Blood Cancer. 2013;60(4):676–81. doi:10.1002/pbc.24327.

    Article  PubMed  Google Scholar 

  25. Pizzo A, Lagana AS, Barbaro L. Comparison between effects of myo-inositol and D-chiro-inositol on ovarian function and metabolic factors in women with PCOS. Gynecol Endocrinol Off J Int Soc Gynecol Endocrinol. 2013. doi:10.3109/09513590.2013.860120.

    Google Scholar 

  26. Shikanov A, Zhang Z, Xu M, Smith RM, Rajan A, Woodruff TK, et al. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng A. 2011;17(23-24):3095–104. doi:10.1089/ten.TEA.2011.0204.

    Article  CAS  Google Scholar 

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Acknowledgement

This study was supported by a grant of the Korea Healthcare Technology R&D Project, Ministry of Health & Welfare, Republic of Korea (HI12C0055).

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Correspondence to Jung Ryeol Lee.

Additional information

Capsule In an animal model system, PEG-SOD is shown to be a promising free-radical scavenging additive for preserving ovarian tissue integrity destined for transplantation.

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Kim, E.J., Lee, H.J., Lee, J. et al. The beneficial effects of polyethylene glycol-superoxide dismutase on ovarian tissue culture and transplantation. J Assist Reprod Genet 32, 1561–1569 (2015). https://doi.org/10.1007/s10815-015-0537-8

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  • DOI: https://doi.org/10.1007/s10815-015-0537-8

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