DOI QR코드

DOI QR Code

Effect of endometrial cell-conditioned medium and platelet-rich plasma on the developmental competence of mouse preantral follicles: An in vitro study

  • Taghizabet, Neda (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Bahmanpour, Soghra (Department of Anatomical Sciences, School of Medicine, Shiraz University of Medical Sciences) ;
  • Zarei-fard, Nehleh (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences) ;
  • Mohseni, Gholamreza (Men's Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences) ;
  • Aliakbari, Fereshteh (Men's Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences) ;
  • Dehghani, Farzaneh (Histomorphometry and Stereology Research Center, Shiraz University of Medical Sciences)
  • Received : 2022.02.01
  • Accepted : 2022.07.04
  • Published : 2022.09.30

Abstract

Objective: The aim of this study was to evaluate the impacts of platelet-rich plasma (PRP) and conditioned medium (CM) derived from endometrial stromal cells on mouse preantral follicle culture in a two-dimensional system to produce competent mature oocytes for fertilization. Methods: In total, 240 preantral follicles were isolated from female mouse ovarian tissue and divided into four groups. The preantral follicles were isolated three times for each group and then cultured, respectively, in the presence of alpha minimum essential medium (control), PRP, CM, and PRP+CM. The in vitro growth, in vitro maturation, and cleavage percentage of the preantral follicles were investigated. Immunocytochemistry (IHC) was also conducted to monitor the meiotic progression of the oocytes. Additionally, the mRNA expression levels of the two folliculogenesis-related genes (Gdf9 and Bmp15) and two apoptosis-related genes (Bcl2 and Bax) were investigated using real-time polymerase chain reaction. Results: In the PRP, CM, and PRP+CM groups, the preantral follicle maturation (evaluated by identifying polar bodies) were greater than the control group. The cleavage rate in the CM, and PRP+CM groups were also greater than the control group. IHC analysis demonstrated that in each treatment group, meiotic spindle was normal. In the PRP+CM group, the gene expression levels of Bmp15, Gdf9, and Bcl2 were greater than in the other groups. The Bax gene was more strongly expressed in the PRP and control groups than in the other groups. Conclusion: Overall, the present study suggests that the combination of CM and PRP can effectively increase the growth and cleavage rate of mouse preantral follicles in vitro.

Keywords

Acknowledgement

This article was extracted from the PhD thesis written by Neda Taghizabet. The research was performed at the Men's Health and Reproductive Health Research Center at Shahid Beheshti University of Medical Sciences and the Experimental and Comparative Medical Center, Anatomy Department, Shiraz University of Medical Sciences in Shiraz, Iran.

References

  1. Rodrigues P, Marques M, Pimentel S, Rato M, Carvalho P, Correia SC, et al. Oncofertility case report: live birth 10 years after oocyte in vitro maturation and zygote cryopreservation. J Assist Reprod Genet 2020;37:3089-94. https://doi.org/10.1007/s10815-020-01984-3
  2. Fathi R, Rezazadeh Valojerdi M, Ebrahimi B, Eivazkhani F, Akbarpour M, et al. Fertility preservation in cancer patients: in vivo and in vitro options. Cell J 2017;19:173-83.
  3. Pais AS, Reis S, Laranjo M, Caramelo F, Silva F, Botelho MF, et al. The challenge of ovarian tissue culture: 2D versus 3D culture. J Ovarian Res 2021;14:147. https://doi.org/10.1186/s13048-021-00892-z
  4. Motamed M, Sadr Z, Valojerdi MR, Moini A, Oryan S, Totonchi M, et al. Tissue engineered human amniotic membrane application in mouse ovarian follicular culture. Ann Biomed Eng 2017;45:1664-75. https://doi.org/10.1007/s10439-017-1836-2
  5. Yang Q, Zhu L, Jin L. Human follicle in vitro culture including activation, growth, and maturation: a review of research progress. Front Endocrinol (Lausanne) 2020;11:548. https://doi.org/10.3389/fendo.2020.00548
  6. De Roo C, Tilleman K. In vitro maturation of oocytes retrieved from ovarian tissue: outcomes from current approaches and future perspectives. J Clin Med 2021;10:4680. https://doi.org/10.3390/jcm10204680
  7. 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. https://doi.org/10.1038/srep17323
  8. O'Brien MJ, Pendola JK, Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 2003;68:1682-6. https://doi.org/10.1095/biolreprod.102.013029
  9. Yoshino T, Suzuki T, Nagamatsu G, Yabukami H, Ikegaya M, Kishima M, et al. Generation of ovarian follicles from mouse pluripotent stem cells. Science 2021;373:eabe0237. https://doi.org/10.1126/science.abe0237
  10. De Clercq K, Hennes A, Vriens J. Isolation of mouse endometrial epithelial and stromal cells for in vitro decidualization. J Vis Exp 2017;(121):55168.
  11. McLaughlin M, Albertini DF, Wallace WH, Anderson RA, Telfer EE. Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Mol Hum Reprod 2018;24:135-42. https://doi.org/10.1093/molehr/gay002
  12. Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 1996;54:197-207. https://doi.org/10.1095/biolreprod54.1.197
  13. Cakiroglu Y, Saltik A, Yuceturk A, Karaosmanoglu O, Kopuk SY, Scott RT, et al. Effects of intraovarian injection of autologous platelet rich plasma on ovarian reserve and IVF outcome parameters in women with primary ovarian insufficiency. Aging (Albany NY) 2020;12:10211-22.
  14. Lee HJ, Quaas AM, Wright DL, Toth TL, Teixeira JM. In vitro maturation (IVM) of murine and human germinal vesicle (GV)-stage oocytes by coculture with immortalized human fallopian tube epithelial cells. Fertil Steril 2011;95:1344-8. https://doi.org/10.1016/j.fertnstert.2010.08.034
  15. Malekshah AK, Moghaddam AE, Daraka SM. Comparison of conditioned medium and direct co-culture of human granulosa cells on mouse embryo development. Indian J Exp Biol 2006;44:189-92.
  16. Tork S, Sharifi ZN, Movassaghi S, Molaeeghaleh N, Abdi S. Evaluation of the effects of human bone marrow mesenchymal stem cells conditioned medium on growth and maturation of mouse ovarian follicle after vitrification. Cells Tissues Organs 2021 Jul 13 [Epub]. https://doi.org/10.1159/000518402.
  17. Xu S, Chan RW, Li T, Ng EH, Yeung WS. Understanding the regulatory mechanisms of endometrial cells on activities of endometrial mesenchymal stem-like cells during menstruation. Stem Cell Res Ther 2020;11:239. https://doi.org/10.1186/s13287-020-01750-3
  18. Desai NN, Goldfarb JM. Growth factor/cytokine secretion by a permanent human endometrial cell line with embryotrophic properties. J Assist Reprod Genet 1996;13:546-50. https://doi.org/10.1007/BF02066606
  19. Sun C, Hao J, Qin H, Zhu Y, Li X, Zhang B, et al. Endometrial regenerative cell-derived conditioned medium alleviates experimental colitis. Stem Cells Int 2022;2022:7842296.
  20. Kawasaki F, Kawano Y, Kosay Hasan Z, Narahara H, Miyakawa I. The clinical role of interleukin-6 and interleukin-6 soluble receptor in human follicular fluids. Clin Exp Med 2003;3:27-31. https://doi.org/10.1007/s102380300012
  21. Wyse BA, Fuchs Weizman N, Defer M, Montbriand J, Szaraz P, Librach C. The follicular fluid adipocytokine milieu could serve as a prediction tool for fertility treatment outcomes. Reprod Biomed Online 2021;43:738-46. https://doi.org/10.1016/j.rbmo.2021.07.001
  22. Nilsson EE, Detzel C, Skinner MK. Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 2006;131:1007-15. https://doi.org/10.1530/rep.1.00978
  23. Hemeda H, Giebel B, Wagner W. Evaluation of human platelet lysate versus fetal bovine serum for culture of mesenchymal stromal cells. Cytotherapy 2014;16:170-80. https://doi.org/10.1016/j.jcyt.2013.11.004
  24. Rauch C, Feifel E, Amann EM, Spotl HP, Schennach H, Pfaller W, et al. Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media. ALTEX 2011;28:305-16. https://doi.org/10.14573/altex.2011.4.305
  25. Talebi M, Vatanmakanian M, Mirzaei A, Barfar Y, Hemmatzadeh M, Nahayati MA, et al. Platelet-rich and platelet-poor plasma might play supportive roles in cancer cell culture: a replacement for fetal bovine serum? Anticancer Agents Med Chem 2021;21:2236-42. https://doi.org/10.2174/1871520621999210101225912
  26. Garbin LC, Olver CS. Platelet-rich products and their application to osteoarthritis. J Equine Vet Sci 2020;86:102820. https://doi.org/10.1016/j.jevs.2019.102820
  27. Dehghani F, Aboutalebi H, Esmaeilpour T, Panjehshahin MR, Bordbar H. Effect of platelet-rich plasma (PRP) on ovarian structures in cyclophosphamide-induced ovarian failure in female rats: a stereological study. Toxicol Mech Methods 2018;28:653-9. https://doi.org/10.1080/15376516.2018.1491662
  28. Tan Q, Balofsky A, Weisz K, Peng C. Role of activin, transforming growth factor-beta and bone morphogenetic protein 15 in regulating zebrafish oocyte maturation. Comp Biochem Physiol A Mol Integr Physiol 2009;153:18-23. https://doi.org/10.1016/j.cbpa.2008.09.016
  29. Hosseini L, Shirazi A, Naderi MM, Shams-Esfandabadi N, Borjian Boroujeni S, Sarvari A, et al. Platelet-rich plasma promotes the development of isolated human primordial and primary follicles to the preantral stage. Reprod Biomed Online 2017;35:343-50. https://doi.org/10.1016/j.rbmo.2017.04.007
  30. Demeestere I, Centner J, Gervy C, Englert Y, Delbaere A. Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents. Reproduction 2005;130:147-56. https://doi.org/10.1530/rep.1.00648
  31. Ghosh D, Sengupta J. Morphological characteristics of human endometrial epithelial cells cultured on rat-tail collagen matrix. Hum Reprod 1995;10:785-90. https://doi.org/10.1093/oxfordjournals.humrep.a136038
  32. Srivastava A, Sengupta J, Kriplani A, Roy KK, Ghosh D. Profiles of cytokines secreted by isolated human endometrial cells under the influence of chorionic gonadotropin during the window of embryo implantation. Reprod Biol Endocrinol 2013;11:116. https://doi.org/10.1186/1477-7827-11-116
  33. Sengupta J, Given RL, Carey JB, Weitlauf HM. Primary culture of mouse endometrium on floating collagen gels: a potential in vitro model for implantation. Ann N Y Acad Sci 1986;476:75-94. https://doi.org/10.1111/j.1749-6632.1986.tb20924.x
  34. Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the MTT assay. Cold Spring Harb Protoc 2018;2018:pdb.prot095505.
  35. Adib M, Seifati SM, Ashkezari MD, Khoradmehr A, Rezaee-Ranjbar-Sardari R, Tahajjodi SS, et al. The effect of the human cumulus cells-conditioned medium on in vitro maturation of mouse oocyte: an experimental study. Int J Reprod Biomed 2020;18:1019-28.
  36. Tang J, Hu W, Di R, Liu Q, Wang X, Zhang X, et al. Expression analysis of the prolific candidate genes, BMPR1B, BMP15, and GDF9 in Small Tail Han Ewes with three fecundity (FecB gene) genotypes. Animals (Basel) 2018;8:166.
  37. Max MC, Bizarro-Silva C, Bufalo I, Gonzalez SM, Lindquist AG, Gomes RG, et al. In vitro culture supplementation of EGF for improving the survival of equine preantral follicles. In Vitro Cell Dev Biol Anim 2018;54:687-91. https://doi.org/10.1007/s11626-018-0296-9
  38. Liang CG, Su YQ, Fan HY, Schatten H, Sun QY. Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol Endocrinol 2007;21:2037-55. https://doi.org/10.1210/me.2006-0408
  39. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009;8:2741-7. https://doi.org/10.4161/cc.8.17.9471
  40. Alhaider AK, Watson PF. The effects of hCG and growth factors on in vitro nuclear maturation of dog oocytes obtained during anoestrus. Reprod Fertil Dev 2009;21:538-48. https://doi.org/10.1071/RD08167
  41. McNally FJ. Mechanisms of spindle positioning. J Cell Biol 2013;200:131-40. https://doi.org/10.1083/jcb.201210007
  42. Basu A, Haldar S. The relationship between BcI2, Bax and p53: consequences for cell cycle progression and cell death. Mol Hum Reprod 1998;4:1099-109. https://doi.org/10.1093/molehr/4.12.1099
  43. Hudgens JL, Sugg KB, Grekin JA, Gumucio JP, Bedi A, Mendias CL. Platelet-rich plasma activates proinflammatory signaling pathways and induces oxidative stress in tendon fibroblasts. Am J Sports Med 2016;44:1931-40. https://doi.org/10.1177/0363546516637176
  44. Buccellato LJ, Tso M, Akinci OI, Chandel NS, Budinger GR. Reactive oxygen species are required for hyperoxia-induced Bax activation and cell death in alveolar epithelial cells. J Biol Chem 2004;279:6753-60. https://doi.org/10.1074/jbc.M310145200
  45. Fenwick MA, Mora JM, Mansour YT, Baithun C, Franks S, Hardy K. Investigations of TGF-β signaling in preantral follicles of female mice reveal differential roles for bone morphogenetic protein 15. Endocrinology 2013;154:3423-36. https://doi.org/10.1210/en.2012-2251
  46. 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;80:587-96. https://doi.org/10.1016/j.theriogenology.2013.06.001