Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
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Survival of isolated human preantral follicles after vitrification: Analyses of morphology and Fas ligand and caspase-3 mRNA expression

  • Wiweko, Budi (Department of Obstetrics and Gynecology, Dr. Cipto Mangunkusumo General Hospital, Faculty of Medicine Universitas Indonesia) ;
  • Soebijanto, Soegiharto (Department of Obstetrics and Gynecology, Dr. Cipto Mangunkusumo General Hospital, Faculty of Medicine Universitas Indonesia) ;
  • Boediono, Arief (Department of Anatomy, IPB University) ;
  • Mansyur, Muchtaruddin (Department of Public Health, Faculty of Medicine Universitas Indonesia) ;
  • Siregar, Nuryati C (Department of Pathology Anatomy, Faculty of Medicine Universitas Indonesia) ;
  • Suryandari, Dwi Anita (Department of Biology, Faculty of Medicine Universitas Indonesia) ;
  • Aulia, Ahmad (Department of Histology, Faculty of Medicine Universitas Indonesia) ;
  • Djuwantono, Tono (Department of Obstetrics and Gynecology, Dr. Hasan Sadikin Hospital, Faculty of Medicine Universitas Padjajaran) ;
  • Affandi, Biran (Department of Obstetrics and Gynecology, Dr. Cipto Mangunkusumo General Hospital, Faculty of Medicine Universitas Indonesia)
  • Received : 2019.03.22
  • Accepted : 2019.07.15
  • Published : 2019.12.31
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Abstract

Objective: This study aimed to examine the effect of vitrification on apoptosis and survival in human preantral follicles after thawing. Methods: This experimental study was conducted at an acute tertiary care hospital from March 2012 to April 2013. Ovaries were sliced into 5 × 5 × 1-mm pieces and divided into the following three groups: preantral follicle isolation, ovarian tissue vitrification-warming followed by follicle isolation, and immunohistochemistry of fresh ovarian tissue. For statistical analyses, the Student t-test, chi-square test, Kruskal-Wallis test, and Kaplan-Meier survival analysis were used. Results: A total of 161 preantral follicles (70% secondary) were collected from ovarian cortex tissue of six women between 30 and 37 years of age who underwent oophorectomy due to cervical cancer or breast cancer. There were no significant differences in the follicular morphology of fresh preantral follicles and vitrified follicles after thawing. The mean Fas ligand (FasL) mRNA expression level was 0.43 ± 0.20 (relative to β-actin) in fresh preantral follicles versus 0.51 ± 0.20 in vitrified follicles (p= 0.22). The mean caspase-3 mRNA expression level in fresh preantral follicles was 0.56 ± 0.49 vs. 0.27 ± 0.21 in vitrified follicles (p= 0.233). One vitrified-thawed secondary follicle grew and developed to an antral follicle within 6 days of culture. Conclusion: Vitrification did not affect preantral follicle morphology or mRNA expression of the apoptosis markers FasL and caspase-3. Further studies are required to establish whether vitrification affects the outcomes of in vitro culture and the maturation of preantral follicles.

Keywords

References

  1. Maltaris T, Boehm D, Dittrich R, Seufert R, Koelbl H. Reproduction beyond cancer: a message of hope for young women. Gynecol Oncol 2006;103:1109-21. https://doi.org/10.1016/j.ygyno.2006.08.003
  2. Meirow D. Reproduction post-chemotherapy in young cancer patients. Mol Cell Endocrinol 2000;169:123-31. https://doi.org/10.1016/S0303-7207(00)00365-8
  3. Nottola SA, Camboni A, Van Langendonckt A, Demylle D, Macchiarelli G, Dolmans MM, et al. Cryopreservation and xenotransplantation of human ovarian tissue: an ultrastructural study. Fertil Steril 2008;90:23-32. https://doi.org/10.1016/j.fertnstert.2007.05.069
  4. 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;12:519-35. https://doi.org/10.1093/humupd/dml032
  5. Martinez-Madrid B, Camboni A, Dolmans MM, Nottola S, Van Langendonckt A, Donnez J. Apoptosis and ultrastructural assessment after cryopreservation of whole human ovaries with their vascular pedicle. Fertil Steril 2007;87:1153-65. https://doi.org/10.1016/j.fertnstert.2006.11.019
  6. Revel A, Revel-Vilk S, Aizenman E, Porat-Katz A, Safran A, Ben-Meir A, et al. At what age can human oocytes be obtained? Fertil Steril 2009;92:458-63. https://doi.org/10.1016/j.fertnstert.2008.07.013
  7. Diedrich K, Fauser BC, Devroey P; Evian Annual Reproduction (EVAR) Workshop Group 2009. Cancer and fertility: strategies to preserve fertility. Reprod Biomed Online 2011;22:232-48. https://doi.org/10.1016/j.rbmo.2010.11.001
  8. Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O. Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Hum Reprod 2011;26:594-603. https://doi.org/10.1093/humrep/deq357
  9. von Wolff M, Donnez J, Hovatta O, Keros V, Maltaris T, Montag M, et al. Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy: a technique in its infancy but already successful in fertility preservation. Eur J Cancer 2009;45:1547-53. https://doi.org/10.1016/j.ejca.2009.01.029
  10. Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG, et al. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod Biomed Online 2011;22:162-71. https://doi.org/10.1016/j.rbmo.2010.10.015
  11. Gosden RG, Baird DT, Wade JC, Webb R. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196 degrees C. Hum Reprod 1994;9:597-603. https://doi.org/10.1093/oxfordjournals.humrep.a138556
  12. Santos RR, Amorim C, Cecconi S, Fassbender M, Imhof M, Lornage J, et al. Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds. Anim Reprod Sci 2010;122:151-63. https://doi.org/10.1016/j.anireprosci.2010.08.010
  13. Hussein MR, Bedaiwy MA, Falcone T. Analysis of apoptotic cell death, Bcl-2, and p53 protein expression in freshly fixed and cryopreserved ovarian tissue after exposure to warm ischemia. Fertil Steril 2006;85 Suppl 1:1082-92. https://doi.org/10.1016/j.fertnstert.2005.10.020
  14. Buyuk E, Oktem O, Sonmezer M, Oktay KH. Ovarian tissue cryopreservation and other fertility preservation strategies. In: Gardner DK, Weissman A, Howles CM, Shoham Z, editors. Textbook of assisted reproductive technologies: laboratory and clinical perspectives. 3rd ed. London: Informa; 2009. p. 327-41.
  15. Gosden RG, Mullan J, Picton HM, Yin H, Tan SL. Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. Hum Reprod Update 2002;8:105-10. https://doi.org/10.1093/humupd/8.2.105
  16. Hovatta O, Silye R, Krausz T, Abir R, Margara R, Trew G, et al. Cryopreservation of human ovarian tissue using dimethylsulphoxide and propanediol-sucrose as cryoprotectants. Hum Reprod 1996;11:1268-72. https://doi.org/10.1093/oxfordjournals.humrep.a019370
  17. Hovatta O. Methods for cryopreservation of human ovarian tissue. Reprod Biomed Online 2005;10:729-34. https://doi.org/10.1016/S1472-6483(10)61116-9
  18. Vajta G, Nagy ZP. Are programmable freezers still needed in the embryo laboratory? Review on vitrification. Reprod Biomed Online 2006;12:779-96. https://doi.org/10.1016/S1472-6483(10)61091-7
  19. Kagawa N, Silber S, Kuwayama M. Successful vitrification of bovine and human ovarian tissue. Reprod Biomed Online 2009;18:568-77. https://doi.org/10.1016/S1472-6483(10)60136-8
  20. Bian J, Li T, Ding C, Xin W, Zhu B, Zhou C. Vitreous cryopreservation of human preantral follicles encapsulated in alginate beads with mini mesh cups. J Reprod Dev 2013;59:288-95. https://doi.org/10.1262/jrd.2012-157
  21. Khosravi F, Reid RL, Moini A, Abolhassani F, Valojerdi MR, Kan FW. In vitro development of human primordial follicles to preantral stage after vitrification. J Assist Reprod Genet 2013;30:1397-406. https://doi.org/10.1007/s10815-013-0105-z
  22. Markstrom E, Svensson EC, Shao R, Svanberg B, Billig H. Survival factors regulating ovarian apoptosis: dependence on follicle differentiation. Reproduction 2002;123:23-30. https://doi.org/10.1530/rep.0.1230023
  23. Johnson AL, Bridgham JT. Caspase-mediated apoptosis in the vertebrate ovary. Reproduction 2002;124:19-27. https://doi.org/10.1530/rep.0.1240019
  24. Hussein MR. Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 2005;11:162-77. https://doi.org/10.1093/humupd/dmi001
  25. Dolmans MM, Michaux N, Camboni A, Martinez-Madrid B, Van Langendonckt A, Nottola SA, et al. Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Hum Reprod 2006;21:413-20. https://doi.org/10.1093/humrep/dei320
  26. Peduto Eberl L, Guillou L, Saraga E, Schroter M, French LE, Tschopp J, et al. Fas and Fas ligand expression in tumor cells and in vascular smooth-muscle cells of colonic and renal carcinomas. Int J Cancer 1999;81:772-8. https://doi.org/10.1002/(SICI)1097-0215(19990531)81:5<772::AID-IJC18>3.0.CO;2-S
  27. Sobenin IA, Bobryshev YV, Korobov GA, Borodachev EN, Postnov AY, Orekhov AN. Quantitative analysis of the expression of caspase 3 and caspase 9 in different types of atherosclerotic lesions in the human aorta. Exp Mol Pathol 2015;99:1-6. https://doi.org/10.1016/j.yexmp.2015.05.004
  28. Sheikhi M, Hultenby K, Niklasson B, Lundqvist M, Hovatta O. Preservation of human ovarian follicles within tissue frozen by vitrification in a xeno-free closed system using only ethylene glycol as a permeating cryoprotectant. Fertil Steril 2013;100:170-7. https://doi.org/10.1016/j.fertnstert.2013.03.018
  29. Keros V, Xella S, Hultenby K, Pettersson K, Sheikhi M, Volpe A, et al. Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum Reprod 2009;24:1670-83. https://doi.org/10.1093/humrep/dep079
  30. Amorim CA, Goncalves PB, Figueiredo JR. Cryopreservation of oocytes from pre-antral follicles. Hum Reprod Update 2003;9:119-29. https://doi.org/10.1093/humupd/dmg014
  31. Hovatta O, Wright C, Krausz T, Hardy K, Winston RM. Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum Reprod 1999;14:2519-24. https://doi.org/10.1093/humrep/14.10.2519
  32. Wiweko B, Prawesti DM, Hestiantoro A, Sumapraja K, Natadisastra M, Baziad A. Chronological age vs biological age: an age-related normogram for antral follicle count, FSH and anti-Mullerian hormone. J Assist Reprod Genet 2013;30:1563-7. https://doi.org/10.1007/s10815-013-0083-1
  33. Wiweko B, Mutia K, Mansyur E. Follicle isolation from ovarian tissue before and after cryopreservation. Fertil Steril 2013;100:S185-6. https://doi.org/10.1016/j.fertnstert.2013.07.1441
  34. Schroder CP, Timmer-Bosscha H, Wijchman JG, de Leij LF, Hollema H, Heineman MJ, et al. An in vitro model for purging of tumour cells from ovarian tissue. Hum Reprod 2004;19:1069-75. https://doi.org/10.1093/humrep/deh244
  35. Vanacker J, Camboni A, Dath C, Van Langendonckt A, Dolmans MM, Donnez J, et al. Enzymatic isolation of human primordial and primary ovarian follicles with Liberase DH: protocol for application in a clinical setting. Fertil Steril 2011;96:379-83. https://doi.org/10.1016/j.fertnstert.2011.05.075
  36. Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil Steril 2013;99:1523-33. https://doi.org/10.1016/j.fertnstert.2013.03.043

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