Improvement of Mouse Preantral Follicle Survival and Development following Co-Culture with Ovarian Parenchyma Cell Suspension

Document Type : Original Article

Authors

1 Department of Basic Sciences and New Biological Technologies, Science and Culture University, Tehran, Iran

2 Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran

3 Reproductive Epidemiology Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran

4 Department of Genetics, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran

5 Department of Lab Sciences, School of Allied Medicine, Iran University of Medical Sciences, Tehran, Iran

Abstract

Background: The parallel and continued improvements in both infertility treatment and the management of malignancy
cases have brought to the forefront the potential for fertility preservation. Using ovarian follicular resources
can effectively improve reproductive capacity and prevent infertility. The primary aim of this research was to try to
generate an appropriate in vivo environment for the growth of the mouse follicles. Hence, the possible effects of the
ovarian parenchyma cell suspension were explored on the growth and maturation of preantral follicles in vitro.
Materials and Methods: In this experimental study, ovarian parenchymal cells were mechanically dissociated from
preantral follicles of 12-14 days-old NMRI mice and then divided into 5 experimental groups (G1: Control, G2: Fresh
follicle with fresh parenchyma cell suspension, G3: Vitrified-warmed follicle with fresh parenchyma cell suspension,
G4: Fresh follicle with frozen-thawed parenchyma cell suspension, and G5: Vitrified-warmed follicle with frozen-thawed
parenchyma cell suspension). The diameter of the follicles and immature oocytes, viability, antrum formation,
resumption of meiosis, in vitro fertilization (IVF), and Gdf9, Bmp6, and Bmp15 gene expression were examined on
different periods.
Results: The diameter of the follicles and the oocytes on days 4 and 8, as well as the survival rate of the follicles up
to day 12, were significantly higher in G2 and G4 compared to the Ctrl group (G1: 73.66%, G2:87.99%, G3: 82.70%,
G4: 94.37%, and G5: 78.59%). Expression of growth marker genes for G3, and G5 groups was significantly higher
than other groups, which indicated the protective effects of parenchyma cell suspension on follicles damaged by vitrification
solutions.
Conclusion: The growth, survival, and maturation of preantral follicles could be enhanced by co-culturing them with
ovarian parenchyma cells. Further studies are needed to optimize the conditions for a successful parenchyma cell
suspension-induced in vitro maturation (IVM) to occur in infertility clinics.

Keywords

Main Subjects


  1.  

    1. Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O'Neill CL, Songsasen N, et al. Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice. Reproduction. 2016; 152(6): R201-R210.
    2. Fathi R, Rezazadeh Valojerdi M, Ebrahimi B, Eivazkhani F, Akbarpour M, Tahaei LS, et al. Fertility preservation in cancer patients: in vivo and in vitro options. Cell J. 2017; 19(2): 173-183.
    3. Guzel Y, Oktem O. Understanding follicle growth in vitro: are we getting closer to obtaining mature oocytes from in vitro-grown follicles in human? Mol Reprod Dev. 2017; 84(7): 544-559.
    4. Lai D, Wang F, Yao X, Zhang Q, Wu X, Xiang C. Human endometrial mesenchymal stem cells restore ovarian function through improving the renewal of germline stem cells in a mouse model of premature ovarian failure. J Transl Med. 2015; 13: 155.
    5. Pastore LM, Christianson MS, Stelling J, Kearns WG, Segars JH. Reproductive ovarian testing and the alphabet soup of diagnoses: DOR, POI, POF, POR, and FOR. J Assist Reprod Genet. 2018; 35(1): 17-23.
    6. Kim EJ, Yang C, Lee J, Youm HW, Lee JR, Suh CS, et al. The new biocompatible material for mouse ovarian follicle development in three-dimensional in vitro culture systems. Theriogenology. 2020; 144: 33-40.
    7. Martinez F, International Society for Fertility Preservation–ESHRE– ASRM Expert Working Group. Update on fertility preservation from the Barcelona International Society for Fertility Preservation- ESHRE-ASRM 2015 expert meeting: indications, results and future perspectives. Fertil Steril. 2017; 108(3): 407-415. e11.
    8. Xiao S, Zhang J, Romero MM, Smith KN, Shea LD, Woodruff TK. In vitro follicle growth supports human oocyte meiotic maturation. Sci Rep. 2015; 5: 17323.
    9. Araújo VR, Gastal MO, Figueiredo JR, Gastal EL. In vitro culture of bovine preantral follicles: a review. Reprod Biol Endocrinol. 2014; 12: 78.
    10. Simon LE, Kumar TR, Duncan FE. In vitro ovarian follicle growth: a comprehensive analysis of key protocol variables. Biol Reprod. 2020; 103(3): 455-470.
    11. Kim CH, Cheon YP, Lee YJ, Lee KH, Kim SH, Chae HD, et al. The effect of fibroblast co-culture on in vitro maturation of mouse preantral follicles. Dev Reprod. 2013; 17(3): 269-274.
    12. Karimpour Malekshah A, Heidari M, Parivar K, Azami NS. The effects of fibroblast co-culture and activin A on in vitro growth of mouse preantral follicles. Iran Biomed J. 2014; 18(1): 49-54.
    13. Jamalzaei P, Valojerdi MR, Ebrahimi B, Farrokhi A. Oocyte maturation and expression pattern of follicular genes during in-vitro culture of vitrified mouse pre-antral follicles. Gene Expr Patterns. 2016; 20(1): 63-70.
    14. Rajabi Z, Yazdekhasti H, Noori Mugahi SMH, Abbasi M, Kazemnejad S, Shirazi A, et al. Mouse preantral follicle growth in 3D co-culture system using human menstrual blood mesenchymal stem cell. Reprod Biol. 2018; 18(1): 122-131.
    15. Green LJ, Zhou H, Padmanabhan V, Shikanov A. Adipose-derived stem cells promote survival, growth, and maturation of early-stage murine follicles. Stem Cell Res Ther. 2019; 10(1): 102.
    16. Jamalzaei P, Valojerdi MR, Montazeri L, Baharvand H. Effects of alginate concentration and ovarian cells on in vitro development of mouse preantral follicles: a factorial study. Int J Fertil Steril. 2020; 13(4): 330-338.
    17. Mescher AL. Junqueira's basic histology text & atlas. 16th ed. Mescher, New York: McGraw-Hill Medical; 2013: 449-478.
    18. Schöler HR. The potential of stem cells: an inventory. Humanbiotechnology as social challenge. 1st ed. Routledge; 2016: 45-72.
    19. Chu YL, Xu YR, Yang WX, Sun Y. The role of FSH and TGF-β superfamily in follicle atresia. Aging (Albany NY). 2018; 10(3): 305-321.
    20. Patton BK, Madadi S, Pangas SA. Control of ovarian follicle development by TGFβ family signaling. Curr Opin Endocr Metab Res. 2021; 18: 102-110.
    21. Ganji R, Nabiuni M, Faraji R. Development of mouse preantral follicle after in vitro culture in a medium containing melatonin. Cell J. 2015; 16(4): 546-553.
    22. Freshney RI. Culture of cells for tissue engineering. In: Vunjak- Novakovic G, Freshney RI, editors. Basic principles of cell culture. 2006: 3-22.
    23. Sadr SZ, Ebrahimi B, Shahhoseini M, Fatehi R, Favaedi R. Mouse preantral follicle development in two-dimensional and three-dimensional culture systems after ovarian tissue vitrification. Eur J Obstet Gynecol Reprod Biol. 2015; 194: 206-211.
    24. Green LJ, Shikanov A. In vitro culture methods of preantral follicles. Theriogenology. 2016; 86(1): 229-238.
    25. Tavana S, Eimani H, Azarnia M, Shahverdi A, Eftekhari-Yazdi P. Effects of saffron (Crocus sativus L.) aqueous extract on in vitro maturation, fertilization and embryo development of mouse oocytes. Cell J. 2012; 13(4): 259-264.
    26. Liang X, Liang J, Zeng F, Lin Y, Li Y, Cai K, et al. Evaluation of oocyte maturity using artificial intelligence quantification of follicle volume biomarker by three-dimensional ultrasound. Reprod Biomed Online. 2022; 45(6): 1197-1206.
    27. Price CA. Mechanisms of fibroblast growth factor signaling in the ovarian follicle. J Endocrinol. 2016; 228(2): R31-R43.
    28. de Castro FC, Cruz MH, Leal CL. Role of growth differentiation factor 9 and bone morphogenetic protein 15 in ovarian function and their importance in mammalian female fertility - a review. Asian- Australas J Anim Sci. 2016; 29(8): 1065-1074.
    29. Chen Y, Zhao S, Qiao J, Liu P, Lian Y, Zheng X. Expression of bone morphogenetic protein-15 in human oocyte and cumulus granulosa cells primed with recombinant follicle-stimulating hormone followed by human chorionic gonadotropin. Fertil Steril. 2009; 92(6): 2045- 2046.
    30. Celestino JJ, Lima-Verde IB, Bruno JB, Matos MH, Chaves RN, Saraiva MV, et al. Steady-state level of bone morphogenetic protein-15 in goat ovaries and its influence on in vitro development and survival of preantral follicles. Mol Cell Endocrinol. 2011; 338(1- 2): 1-9.
    31. Lin ZL, Li YH, Xu YN, Wang QL, Namgoong S, Cui XS, et al. Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod Domest Anim. 2014; 49(2): 219-227.
    32. De Los Reyes M, Rojas C, Parraguez VH, Palomino J. Expression of growth differentiation factor 9 (GDF-9) during in vitro maturation in canine oocytes. Theriogenology. 2013; 80(6): 587-596
    33. Wang W, Rigueur D, Lyons KM. TGFβ as a gatekeeper of BMP action in the developing growth plate. Bone. 2020; 137: 115439.
    34. Lee SH, Oh HJ, Kim MJ, Kim GA, Choi YB, Jo YK, et al. Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes. J Assist Reprod Genet. 2017; 34(7): 929-938.
    35. Cook-Andersen H, Curnow KJ, Su HI, Chang RJ, Shimasaki S. Growth and differentiation factor 9 promotes oocyte growth at the primary but not the early secondary stage in three-dimensional follicle culture. J Assist Reprod Genet. 2016; 33(8): 1067-1077.
    36. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996; 383(6600): 531-535.
    37. Sanfins A, Rodrigues P, Albertini DF. GDF-9 and BMP-15 direct the follicle symphony. J Assist Reprod Genet. 2018; 35(10): 1741- 1750.
    38. Monte APO, Santos JM, Menezes VG, Gouveia BB, Lins TLBG, Barberino RS, et al. Growth differentiation factor-9 improves development, mitochondrial activity and meiotic resumption of sheep oocytes after in vitro culture of secondary follicles. Reprod Domest Anim. 2019; 54(9): 1169-1176.