Molecular biological bases for intraovarian folliculogenesis, follicular maturation and recruitment


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The review discusses new approaches to studying the stages of folliculogenesis and analyzes the contribution of the major signaling pathways to the processes of intraovarian regulation of folliculogenesis, follicle recruitment and maturation. Materials and methods: The review includes data from the foreign and Russia articles found in Pubmed on the topic under consideration and published in recent years. Results: The review analyzes research data on the regulation of the female reproductive system with emphasis on experimental studies of the signaling pathways that regulate intraovarian folliculogenesis and defines prospects for their use in clinical practice. On the basis of new knowledge, the authors consider the possibilities of preventing severe infertility associated with a small number of obtained oocytes and their poor quality, overcoming premature ovarian failure, and protecting the ovaries against gonadotoxic effects. They underline the need for expanding and intensifying the study of the processes of intraovarian folliculogenesis and choosing a gonadotropin-dependent pool of follicles. Conclusion: The presented studies demonstrate the interest of scientists in the investigation of complex issues of intraovarian folliculogenesis and the role of signaling pathways in this process and touch on molecular genetic involvement and transcriptome analysis. It is necessary to further accumulate this knowledge and conduct fundamental studies for the development of reproductive medicine and the resolution of the problems of reproductive pathology, the situations that we cannot explain now or, therefore, effectively treat.

Full Text

Restricted Access

About the authors

Julia V. Sokolova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology Ministry of Health of the Russian Federation

Email: julietsok@gmail.com
embryologist 117997, Russia, Moscow, Ac. Oparina str., 4

Yana O. Martirosyan

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology Ministry of Health of the Russian Federation

Email: marti-yana@yandex.ru
Junior Researcher of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen 117997, Russia, Moscow, Ac. Oparina str., 4

Tatiana A. Nazarenko

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology Ministry of Health of the Russian Federation

Email: t.nazarenko@mail.ru
MD, PhD, Head of the Institute of Reproductive Technologies 117997, Russia, Moscow, Ac. Oparina str., 4

Almina M. Biryukova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology Ministry of Health of the Russian Federation

Email: alma2l@list.ru
MD, PhD, Head on Clinical Work of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen 117997, Russia, Moscow, Ac. Oparina str., 4

Diana G. Khubaeva

I.M. Sechenov First Moscow State Medical University Ministry of Health of the Russian Federation (Sechenov University)

Email: khubaeva.d@mail.ru
student, I 119991, Russia, Moscow, Trubetskaya str., 8-2

Valeria G. Krasnova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology Ministry of Health of the Russian Federation

Email: lkrasnova27@mail.com
student of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen 117997, Russia, Moscow, Ac. Oparina str., 4

References

  1. Kwintkiewicz J., Giudice L.C. The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin. Reprod. Med. 2009; 27(1): 43-51. https://dx.doi.org/10.1055/s-0028-1108009.
  2. Macklon N.S., Fauser B.C. Aspects of ovarian follicle development throughout life. Horm. Res. 1999; 52(4): 161-70. https://dx.doi.org/10.1159/000023456.
  3. Назаренко Т.А., Мартиросян Я.О., Бирюкова А.М., Джанашвили Л.Г., Иванец Т.Ю., Сухова Ю.В. Опыт стимуляции яичников в режиме «randomstart» протоколов для сохранения репродуктивного материала онкологических больных. Акушерство и гинекология. 2020; 4: 52-8. https://dx.doi.org/10.18565/aig.2020.4.52-5.
  4. Jin B., Niu Z., Xu B., Chen Q., Zhang A.Comparison of clinical outcomes among dual ovarian stimulation, mild stimulation and luteal phase stimulation protocols in women with poor ovarian response. Gynecol. Endocrinol. 2018; 34(8): 694-7. https://dx.doi.org/10.1080/09513590.2018.1435636.
  5. Baerwald A.R., Adams G.P., Pierson R.A. Characterization of ovarian follicular wave dynamics in women. Biol. Reprod. 2003; 69(3): 1023-31. https://dx.doi.org/10.1095/biolreprod.103.017772.
  6. Ginther O.J., Gastal E.L., Gastal M.O., Bergfeit D.R., Baerwald A.R., Pierson R.A.Comparative study of the dynamics of follicular waves in mares and women. Biol. Reprod. 2004; 71(4): 1195-201. https://dx.doi.org/10.1080/09513590.2018.1435636.
  7. Edwards R.G. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965; 208(5008): 349-51. https://dx.doi.org/10.1016/s0140-6736(65)92903-x.
  8. Abir R., Ben-Aharon I., Garor R., Yaniv I., Ash S., Stemmer S.M. et al. Cryopreservation of in vitro matured oocytes in addition to ovarian tissue freezing for fertility preservation in paediatric female cancer patients before and after cancer therapy. Hum. Reprod. 2016; 31(4): 750-62. https://dx.doi.org/10.1093/humrep/dew007.
  9. Woodruff T.K., Snyder K.A. Oncofertility: fertility preservation for cancer survivors. New York: Springer; 2007. 263p.
  10. Macklon N.S., Fauser B.C. Aspects of ovarian follicle development throughout life. Horm. Res. 1999; 52(4): 161-70. https://dx.doi.org/10.1159/000023456.
  11. Baerwald A.R., Adams G.P., Pierson R.A. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum. Reprod. 2012; 18(1): 73-91. https://dx.doi.org/10.1093/humupd/dmr039.
  12. Adhikari D., Liu K. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr. Rev. 2009; 30(5): 438-64. https://dx.doi.org/10.1210/er.2008-0048.
  13. Johnson J., Canning J., Kaneko T., Pru J.K., Tilly J.L. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004; 428(6979): 145-50. https://dx.doi.org/10.1038/nature02316.
  14. Virant-Klun I., Stimpfel M., Skutella T. Ovarian pluripotent/multipotent stem cells and in vitro oogenesis in mammals. Histol. Histopathol. 2011; 26(8): 107182. https://dx.doi.org/10.14670/hh-26.1071.
  15. Petrucelli N., Daly M.B., Pal T. BRCA1- and BRCA2-Associated hereditary breast and ovarian cancer. In: Adam M.P., Ardinger H.H., Pagon R.A., Wallace S.E., Bean L.J.H., Gripp K.W. et al., eds. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993-2021. 1998 Sep 4 [updated 2016 Dec 15].
  16. Zheng W., Nagaraju G., Liu Z., Liu K. Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary. Mol. Cell. Endocrinol. 2012; 356(1-2): 24-30. https://dx.doi.org/10.1016/j.mce.2011.05.027.
  17. Zhang H., Risal S., Gorre N., Busayavalasa K., Li X., Shen Y. et al. Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr. Biol. 2014; 24(21): 2501-8. https://dx.doi.org/10.1016/j.cub.2014.09.023.
  18. Liu P., Cheng H., Roberts T.M., Zhao J.J. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 2009; 8(8): 627-44. https://dx.doi.org/10.1038/nrd2926.
  19. Cully M., You H., Levine A.J., Mak T.W. Beyond PTEN mutations: The PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat. Rev. Cancer. 2006; 6(3): 184-92. https://dx.doi.org/10.1038/nrc1819.
  20. Mora A., Komander D., van Aalten D.M., Alessi D.R. PDK1, the master regulator of AGC kinase signal transduction. Semin. Cell Dev. Biol. 2004; 15(2): 161-70. https://dx.doi.org/10.1016/j.semcdb.2003.12.022.
  21. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell. 2007; 129(7): 1261-74. https://dx.doi.org/10.1016/j.cell.2007.06.009.
  22. Viglietto G., Motti M.L., Bruni P., Melillo R.M., D’Alessio A., Califano D. et al. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer. Nat. Med. 2002; 8(10): 1136-44. https://dx.doi.org/10.1038/nm762.
  23. Liang J., Zubovitz J., Petr ocelli T., Kotchetkov R., Connor M.K., Han K. et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat. Med. 2002; 8(10): 1153-60. https://dx.doi.org/10.1186/2bcr596.
  24. Shin I., Yakes F.M., Rojo F., Shin N.Y., Bakin A.V., Baselga J., Arteaga C.L. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat. Med. 2002; 8(10): 1145-52. https://dx.doi.org/10.1038/nm759.
  25. Meng Q., Xia C., Fang J., Rojanasakul Y., Jiang B.H. Role of PI3K and AKT specific isoforms in ovarian cancer cell migration, invasion and proliferation through the p70S6K1 pathway. Cell. Signal. 2006; 18(12): 2262-71. https://dx.doi.org/10.1016/j.cellsig.2006.05.019.
  26. Robertson G.P. Functional and therapeutic significance of Akt deregulation in malignant melanoma. Cancer Metastasis Rev. 2005; 24(2): 273-85. https://dx.doi.org/10.1007/s10555-005-1577-9.
  27. Hosaka T., Biggs W.H., Tieu D., Boyer A.D., Varki N.M., Cavenee W.K., Arden K.C. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. USA. 2004; 101(9): 2975-80. https://dx.doi.org/10.1073/pnas.0400093101.
  28. Castrillon D.H., Miao L., Kollipara R., Horner J.W., DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science. 2003; 301(5630): 215-8. https://dx.doi.org/10.1126/science.1086336.
  29. Myatt S.S., Brosens J.J., Lam E.W. Sense and sensitivity: FOXO and ROS in cancer development and treatment. Antioxid. Redox Signal. 2011; 14(4): 675-87. https://dx.doi.org/10.1089/ars.2010.3383.
  30. Annunziata M., Granata R., Ghigo E. The IGF system. Acta Diabetol. 2011; 48(1): 1-9. https://dx.doi.org/10.1007/s00592-010-0227-z.
  31. Zhao Y., Zhang Y., Li J., Zheng N., Xu X., Yang J. et al. MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling. J. Cell. Physiol. 2018; 233(1): 226-37. https://dx.doi.org/10.1002/jcp.25868.
  32. Kwintkiewicz J., Giudice L.C. The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin. Reprod. Med. 2009; 27: 43-51. https://dx.doi.org/10.1055/s-0028-1108009.
  33. Zhou P., Baumgarten S.C., Wu Y.G., Bennett J., Winston N., Hirshfeld-Cytron J., Stocco C. IGF-I signaling is essential for FSH stimulation of AKT and steroidogenic genes in granulosa cells. Mol. Endocrinol. 2013; 27(3): 511-23. https://dx.doi.org/10.1210/me.2012-1307.
  34. Cargnello M., Roux P.P. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 2011; 75: 50-83. https://dx.doi.org/10.1128/mmbr.00031-10.
  35. Boutros T., Chevet E., Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 2008; 60(3): 261-310. http://dx.doi.org/10.1124/pr.107.00106.
  36. Liu Y., Shepherd E.G., Nelin L.D. MAPK phosphatases-regulating the immune response. Nat. Rev. Immunol. 2007; 7(3): 202-12. https://dx.doi.org/10.1038/nri2035.
  37. Fan H.Y., Liu Z., Shimada M., Sterneck E., Johnson P.F., Hedrick S.M., Richards J.S. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science. 2009; 324(5929): 938-41. https://dx.doi.org/10.1126/science.1171396.
  38. Du X.Y., Huang J., Xu L.Q., Tang D.F., Wu L., Zhang L.X. et al. The protooncogene c-src is involved in primordial follicle activation through the PI3K, PKC and MAPK signaling pathways. Reprod. Biol. Endocrinol. 2012; 10: 58. https://dx.doi.org/10.1186/1477-7827-10-58.
  39. Li-Ping Z., Da-Lei Z., Jian H., Liang-Quan X., Ai-Xia X., Xiao-Yu D. et al. Proto-oncogene c-erbB2 initiates rat primordial follicle growth via PKC and MAPK pathways. Reprod. Biol. Endocrinol. 2010; 8: 66. https://dx.doi.org/10.1186%2F1477-7827-10-58.
  40. Ryan K.E., Glister C., Lonergan P., Martin F., Knight P.G., Evans A.C. Functional significance of the signal transduction pathways Akt and Erk in ovarian follicles: In vitro and in vivo studies in cattle and sheep. J. Ovarian Res. 2008; 1(1): 2. https://dx.doi.org/10.1186/1757-2215-1-2.
  41. Bezerra M.E.S., Barberino R.S., Menezes V.G., Gouveia B.B., Macedo T.J.S., Santos J.M.S. et al. Insulin-like growth factor-1 (IGF-1) promotes primordial follicle growth and reduces DNA fragmentation through the phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT) signalling pathway. Reprod. Fertil. Dev. 2018; 30(11): 1503-13. https://dx.doi.org/10.1071/rd17332.
  42. Godkin J. Transforming growth factor beta and the endometrium. Rev. Reprod. 1998; 3(1): 1-6. https://dx.doi.org/10.1530/ror.0.0030001.
  43. Shull M.M., Doetschman T. Transforming growth factor-beta1 in reproduction and development. Mol. Reprod. Dev. 1994; 39(2): 239-46. https://dx.doi.org/10.1002/mrd.1080390218.
  44. Heldin C.H., Miyazono K., ten Dijke P. TGF-ß signalling from cell membrane to nucleus through SMAD proteins. Nature. 1997; 390(6659): 465-71. https://dx.doi.org/10.1038/37284.
  45. Drummond A.E. TGFbeta signalling in the development of ovarian function. Cell Tissue Res. 2005; 322(1): 107-15. https://dx.doi.org/10.1007/s00441-005-1153-1.
  46. Kaivo-oja N., Jeffery L.A., Ritvos O., Mottershead D.G. Smad signalling in the ovary. Reprod. Biol. Endocrinol. 2006; 4, 21. https://dx.doi.org/10.1186/1477-7827-4-21.
  47. Danielpour D., Song K. Cross-talk between IGF-I and TGF-beta signaling pathways. Cytokine Growth Factor Rev. 2006; 17(1-2): 59-74. https://dx.doi.org/10.1016/j.cytogfr.2005.09.007.
  48. Wang Z.P., Mu X.Y., Guo M., Wang Y.J., Teng Z., Mao G.P. et al. Transforming growth factor-beta signaling participates in the maintenance of the primordial follicle pool in the mouse ovary. J. Biol. Chem. 2014; 289(12): 8299-311. https://dx.doi.org/10.1074/jbc.M113.532952.
  49. Vo K.C.T., Kawamura K. In vitro activation early follicles: from the basic science to the clinical perspectives.Int. J. Mol. Sci. 2021; 22(7): 3785. https://dx.doi.org/10.3390/ijms22073785.
  50. Goldman K.N., Chenette D., Arju R., Duncan F.E., Keefe D.L., Grifo J.A., Schneider R.J. mTORC1/2 inhibition preserves ovarian function and fertility during genotoxic chemotherapy. Proc. Natl. Acsd. Sci. USA. 2017; 114(12): 3186-91. https:/dx.doi.org/10.1073/pnas.1617233114.
  51. Chronowska E. High-throughput analysis of ovarian granulosa cell transcriptome. Biomed. Res.Int. 2014; 2014: 213570. https://dx.doi.org/10.1155/2014/213570.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2022 Bionika Media

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies