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Does the ovarian surface epithelium differentiate into primordial follicle and primary follicle precursor structures?

Year 2022, Volume: 47 Issue: 3, 1256 - 1262, 30.09.2022
https://doi.org/10.17826/cumj.1134852

Abstract

Purpose: The aim of this study is to investigate the differentiation capacity of ovarian surface epithelial cells both in cell culture conditions and in ovarian tissue sections.
Materials and Methods: The ovaries of two prepubertal (4 weeks old) female rats were divided into small pieces and explant cell culture was created. Ovarian surface epithelium proliferating together with ovarian stromal cells in mixed cell culture was isolated and reproduced. In addition, ovarian surface epithelium was examined in histological sections of ovarian tissue and images were taken under the microscope.
Results: The morphological appearance of the ovarian surface epithelium was found to be cobblestone. In the count performed under phase contrast microscopy, it was observed that 2x106 and 3x106 cells were grown in the culture dishes, respectively. Primordial follicle-like structures were observed in some areas of the petri dishes. On the histological sections, primordial and primary follicle precursor structures were observed on the basement membrane.
Conclusion: Showing oocyte markers (Gdf-9, C-Mos, Zpc, Stella) and germ cell markers (Dazl, Vasa, Blimp1, Fragilis) both in cell cultures and in histological sections can give us valuable information in terms of monitoring the differentiation capacity of these cells.

References

  • 1)Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology and pathology. Endocr Rev.2001;22:255-88.
  • 2)Xu J, Zheng T, Hong W, Ye H, Hu C, Zheng Y. Mechanism for the decision of ovarian surface epithelial stem cells to undergo neo-oogenesis or ovarian tumorigenesis. Cell Physiol Biochem. 2018;50:214-232.
  • 3)Kinnear HM, Tomaszewski CE, Chang FL, Moravek MB, Xu M, Padmanabhan V et al. The ovarian stroma as a new frontier. Reproduction 2020;160:25-39.
  • 4) Chichi CDC, Smith ER, Yang DH, Roland IH, Vanderveer L, Cohen C et al. Dynamic alterations of the extracellular environment of ovarian surface epithelial cells in premalignant transformation, tumorigenicity, and metastasis. Cancer 2002;15;95:1802-15
  • 5) Ross MH, Pawlina W. Histoloji Konu Anlatımı ve Atlas. (Çeviri Eds Baykal B, Ankara) Palme Yayıncılık, 2014.
  • 6) Seghinsara AM, Banimohammad M. New facts about ovarian stem cells: the origin and the fate. Int. J. Women's Health Reprod. Sci.2018;6:127-133.
  • 7) Kruk PA, Bandiera SLM, Auersperg N. A simplified method to culture human ovarian surface epithelium. Lab Invest.1990;63:132-6.
  • 8) Dunfield LD, Shepherd TG, Nachtigal MW. Primary culture and mRNA analysis of human ovarian cells. Biol Proced Online.2002;28:55-61.
  • 9) Okamoto S, Okamoto A, Nikaido T, Saito M, Takao M, Yanaihara N et al. Mesenchymal to epithelial transition in the human ovarian surface epithelium focusing on inclusion cysts. Oncol Rep.2009;21:1209-14.
  • 10) Edmondson RJ, Monaghan JM, Davies BR. The human ovarian surface epithelium is an androgen responsive tissue. Br J Cancer. 2002;18;86:879-85.
  • 11) Bhartiya D, Singh J. FSH–FSHR3–stem cells in ovary surface epithelium: basis for adult ovarian biology, failure, aging, and cancer. Reproduction.2015;149:35-48.
  • 12) Wong AST, Leung PCK. Role of endocrine and growth factors on the ovarian surface epithelium. J. Obstet. Gynaecol. Res.2007;33:3–16.
  • 13) Huang WL, Li Z, Lin TY, Wang SW, Wu FJ, Luo CW. Thyrostimulin-TSHR signaling promotes the proliferation of NIH:OVCAR-3 ovarian cancer cells via trans-regulation of the EGFR pathway. Sci Rep.2016;7:27471.
  • 14) Murdoch WJ, McDonnel AC. Roles of the ovarian surface epithelium in ovulation and carcinogenesis. Reproduction.2002;123:743-50.
  • 15) Gaytán M, Sánchez MS, Morales C, Bellido C, Millán Y, de Las Mulas JM. et al. Cyclic changes of the ovarian surface epithelium in the rat. Reproduction.2005;129:311-2.
  • 16) Mara JN, Zhou LT, Larmore M, Johnson B, Rebecca Ayiku R, Amargant F. et al. Ovulation and ovarian wound healing are impaired with advanced reproductive age. Aging. 2020;12:9686-9713.
  • 17) Bukovsky A. Ovarian stem cell niche and follicular renewal in mammals. Anat Rec. (Hoboken).2011;294:1284-306.
  • 18) Klun IV, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A. et al. Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed Res Int.2013;690415
  • 19) Klun IV, Skutella T, Stimpfel M, Sinkovec J. Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. J Biomed Biotechnol.2011;381928.
  • 20) Klun IV, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation.2008;76:843-56.
  • 21) Martin JJ, Woods DC, Tilly JL. Implications and current limitations of oogenesis from female germline or oogonial stem cells in adult mammalian ovaries. Cells.2019;8:93
  • 22) Galateanu AAG, Hinescu ME, Enciu AM. Ovarian adult stem cells: hope or pitfall? J Ovarian Res.2014;7:71.
  • 23) Bharti D, Jang SJ, Lee SY, Lee SL, Rho GJ. In vitro generation of oocyte like cells and their in vivo efficacy: how far we have been succeeded. Cells.2020;9:557.
  • 24) Hanna C, Hennebold J. Ovarian germline stem cells: an unlimited source of oocytes? Fertil Steril. 2014;101:20–30
  • 25) Clarkson YL, McLaughlin M, Waterfall M, Dunlop CE, Skehel PA, Anderson RA et al. Initial characterisation of adult human ovarian cell populations isolated by DDX4 expression and aldehyde dehydrogenase activity. Sci Rep.2018;8:6953.
  • 26) Özakpinar ÖB, Maurer AM, Özsavci D. Ovarian stem cells: from basic to clinical applications. World J Stem Cells.2015;7:757-68.
  • 27) Liu HC, He Z, Rosenwaks Z. In vitro culture and in vitro maturation of mouse preantral follicles with recombinant gonadotropins. Fertil Steril.2002;77:373-83.
  • 28) Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and non-human primates. Fertil Steril.2013;99:1523-33.
  • 29) Wang JJ, Ge W, Liu JC, Klinger FG, Dyce PW, Felici MD et al. Complete in vitro oogenesis: retrospects and prospects oogenesis in cultures derived from adult human ovaries. Cell Death and Differentiation. 2017;24;1845–185.
  • 30) 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.
  • 31) Jin SY, Lei L, Shikanov A, Shea LD, Woodruff TK. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril.2010;93:2633-9.
  • 32) Güzel Y, Oktem Ö. Understanding follicle growth in vitro: Are we getting closer to obtaining mature oocytes from in vitro-grown follicles in human? Mol Reprod Dev. 2017;84:544-559.
  • 33) Bertoldo MJ, Walters KA, Ledger WL, Gilchrist RB, Mermillod P, Locatelli Y. In-vitro regulation of primordial follicle activation: challenges for fertility preservation strategies. Reprod Biomed Online.2018;36:491-499.
  • 34) Yang L, Chen L, Lu X, Tan A, Chen Y, Li Y et al. Peri-ovarian adipose tissue contributes to intraovarian control during folliculogenesis in mice. Reproduction.2018;156:133-144.
  • 35) Zhu M,Shen Q, Li X, Kang J. Removal of peri-ovarian adipose tissue affects follicular development and lipid metabolism. Biol Reprod.2020;103:1199–1208.
  • 36) Zhang L, An G, Wu S, Wang J, Yang D, Zhang Y. et al. Long-term intermittent cold exposure affects peri-ovarian adipose tissue and ovarian microenvironment in rats. J Ovarian Res.2021;14:107.

Ovaryum yüzey epiteli primordial folikül ve primer folikül öncüsü yapılara farklılaşıyor mu?

Year 2022, Volume: 47 Issue: 3, 1256 - 1262, 30.09.2022
https://doi.org/10.17826/cumj.1134852

Abstract

Amaç: Ovaryum yüzey epiteli hücrelerinin farklılaşma kapasitelerini hem hücre kültürü şartlarında hem de ovaryum doku kesitlerinde araştırmaktır.
Gereç ve Yöntem: İki tane puberte öncesi dönemdeki (4 haftalık) dişi sıçanların ovaryumları küçük parçalara ayrılarak eksplant hücre kültürü oluşturuldu. Miks hücre kültüründe overyan stromal hücrelerle birlikte çoğalan ovaryum yüzey epiteli izole edilerek çoğaltıldı. Bununla birlikte ovaryum dokusunun histolojik kesitlerinde ovaryum yüzey epiteli incelenerek mikroskop altında görüntüleri alındı.
Bulgular: Ovaryum yüzey epitelinin morfolojik görünümünün parke taşı (cobblestone) şeklinde olduğu görüldü. Faz kontrast mikroskobisi altında yapılan sayımda kültür kaplarında sırasıyla 2x106 ve 3x106 hücrenin ürediği izlendi. Petri kaplarının bazı alanlarında primordial folikül benzeri yapıların oluştuğu görüldü. Histolojik kesitlerde ise bazal membranın üzerinde primordial ve primer folikül öncüsü yapıların olduğu gözlemlendi.
Sonuç: Hem hücre kültürlerinde, hem de histolojik kesitlerde oosit belirteçlerini (Gdf-9, C-Mos, Zpc, Stella) ve germ hücre belirteçlerini (Dazl,Vasa,Blimp1,Fragilis) göstermek bu hücrelerin farklılaşma kapasitelerini izlememiz açısından bizlere değerli bilgiler verebilir.

References

  • 1)Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology and pathology. Endocr Rev.2001;22:255-88.
  • 2)Xu J, Zheng T, Hong W, Ye H, Hu C, Zheng Y. Mechanism for the decision of ovarian surface epithelial stem cells to undergo neo-oogenesis or ovarian tumorigenesis. Cell Physiol Biochem. 2018;50:214-232.
  • 3)Kinnear HM, Tomaszewski CE, Chang FL, Moravek MB, Xu M, Padmanabhan V et al. The ovarian stroma as a new frontier. Reproduction 2020;160:25-39.
  • 4) Chichi CDC, Smith ER, Yang DH, Roland IH, Vanderveer L, Cohen C et al. Dynamic alterations of the extracellular environment of ovarian surface epithelial cells in premalignant transformation, tumorigenicity, and metastasis. Cancer 2002;15;95:1802-15
  • 5) Ross MH, Pawlina W. Histoloji Konu Anlatımı ve Atlas. (Çeviri Eds Baykal B, Ankara) Palme Yayıncılık, 2014.
  • 6) Seghinsara AM, Banimohammad M. New facts about ovarian stem cells: the origin and the fate. Int. J. Women's Health Reprod. Sci.2018;6:127-133.
  • 7) Kruk PA, Bandiera SLM, Auersperg N. A simplified method to culture human ovarian surface epithelium. Lab Invest.1990;63:132-6.
  • 8) Dunfield LD, Shepherd TG, Nachtigal MW. Primary culture and mRNA analysis of human ovarian cells. Biol Proced Online.2002;28:55-61.
  • 9) Okamoto S, Okamoto A, Nikaido T, Saito M, Takao M, Yanaihara N et al. Mesenchymal to epithelial transition in the human ovarian surface epithelium focusing on inclusion cysts. Oncol Rep.2009;21:1209-14.
  • 10) Edmondson RJ, Monaghan JM, Davies BR. The human ovarian surface epithelium is an androgen responsive tissue. Br J Cancer. 2002;18;86:879-85.
  • 11) Bhartiya D, Singh J. FSH–FSHR3–stem cells in ovary surface epithelium: basis for adult ovarian biology, failure, aging, and cancer. Reproduction.2015;149:35-48.
  • 12) Wong AST, Leung PCK. Role of endocrine and growth factors on the ovarian surface epithelium. J. Obstet. Gynaecol. Res.2007;33:3–16.
  • 13) Huang WL, Li Z, Lin TY, Wang SW, Wu FJ, Luo CW. Thyrostimulin-TSHR signaling promotes the proliferation of NIH:OVCAR-3 ovarian cancer cells via trans-regulation of the EGFR pathway. Sci Rep.2016;7:27471.
  • 14) Murdoch WJ, McDonnel AC. Roles of the ovarian surface epithelium in ovulation and carcinogenesis. Reproduction.2002;123:743-50.
  • 15) Gaytán M, Sánchez MS, Morales C, Bellido C, Millán Y, de Las Mulas JM. et al. Cyclic changes of the ovarian surface epithelium in the rat. Reproduction.2005;129:311-2.
  • 16) Mara JN, Zhou LT, Larmore M, Johnson B, Rebecca Ayiku R, Amargant F. et al. Ovulation and ovarian wound healing are impaired with advanced reproductive age. Aging. 2020;12:9686-9713.
  • 17) Bukovsky A. Ovarian stem cell niche and follicular renewal in mammals. Anat Rec. (Hoboken).2011;294:1284-306.
  • 18) Klun IV, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A. et al. Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed Res Int.2013;690415
  • 19) Klun IV, Skutella T, Stimpfel M, Sinkovec J. Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. J Biomed Biotechnol.2011;381928.
  • 20) Klun IV, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation.2008;76:843-56.
  • 21) Martin JJ, Woods DC, Tilly JL. Implications and current limitations of oogenesis from female germline or oogonial stem cells in adult mammalian ovaries. Cells.2019;8:93
  • 22) Galateanu AAG, Hinescu ME, Enciu AM. Ovarian adult stem cells: hope or pitfall? J Ovarian Res.2014;7:71.
  • 23) Bharti D, Jang SJ, Lee SY, Lee SL, Rho GJ. In vitro generation of oocyte like cells and their in vivo efficacy: how far we have been succeeded. Cells.2020;9:557.
  • 24) Hanna C, Hennebold J. Ovarian germline stem cells: an unlimited source of oocytes? Fertil Steril. 2014;101:20–30
  • 25) Clarkson YL, McLaughlin M, Waterfall M, Dunlop CE, Skehel PA, Anderson RA et al. Initial characterisation of adult human ovarian cell populations isolated by DDX4 expression and aldehyde dehydrogenase activity. Sci Rep.2018;8:6953.
  • 26) Özakpinar ÖB, Maurer AM, Özsavci D. Ovarian stem cells: from basic to clinical applications. World J Stem Cells.2015;7:757-68.
  • 27) Liu HC, He Z, Rosenwaks Z. In vitro culture and in vitro maturation of mouse preantral follicles with recombinant gonadotropins. Fertil Steril.2002;77:373-83.
  • 28) Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and non-human primates. Fertil Steril.2013;99:1523-33.
  • 29) Wang JJ, Ge W, Liu JC, Klinger FG, Dyce PW, Felici MD et al. Complete in vitro oogenesis: retrospects and prospects oogenesis in cultures derived from adult human ovaries. Cell Death and Differentiation. 2017;24;1845–185.
  • 30) 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.
  • 31) Jin SY, Lei L, Shikanov A, Shea LD, Woodruff TK. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril.2010;93:2633-9.
  • 32) Güzel Y, Oktem Ö. Understanding follicle growth in vitro: Are we getting closer to obtaining mature oocytes from in vitro-grown follicles in human? Mol Reprod Dev. 2017;84:544-559.
  • 33) Bertoldo MJ, Walters KA, Ledger WL, Gilchrist RB, Mermillod P, Locatelli Y. In-vitro regulation of primordial follicle activation: challenges for fertility preservation strategies. Reprod Biomed Online.2018;36:491-499.
  • 34) Yang L, Chen L, Lu X, Tan A, Chen Y, Li Y et al. Peri-ovarian adipose tissue contributes to intraovarian control during folliculogenesis in mice. Reproduction.2018;156:133-144.
  • 35) Zhu M,Shen Q, Li X, Kang J. Removal of peri-ovarian adipose tissue affects follicular development and lipid metabolism. Biol Reprod.2020;103:1199–1208.
  • 36) Zhang L, An G, Wu S, Wang J, Yang D, Zhang Y. et al. Long-term intermittent cold exposure affects peri-ovarian adipose tissue and ovarian microenvironment in rats. J Ovarian Res.2021;14:107.
There are 36 citations in total.

Details

Primary Language Turkish
Subjects Clinical Sciences
Journal Section Research
Authors

Murat Serkant Ünal 0000-0003-1992-7909

Mücahit Seçme 0000-0002-2084-760X

Publication Date September 30, 2022
Acceptance Date August 25, 2022
Published in Issue Year 2022 Volume: 47 Issue: 3

Cite

MLA Ünal, Murat Serkant and Mücahit Seçme. “Ovaryum yüzey Epiteli Primordial folikül Ve Primer folikül öncüsü yapılara farklılaşıyor Mu?”. Cukurova Medical Journal, vol. 47, no. 3, 2022, pp. 1256-62, doi:10.17826/cumj.1134852.