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Obstetrics and Gynegology2022№1
Molecular biological bases for intraovarian...

Molecular biological bases for intraovarian folliculogenesis follicular maturation and recruitment

DOI
https://dx.doi.org/10.18565/aig.2022.01.22-30

Sokolova Yu.V., Martirosyan Ya.O., Nazarenko T.A., Biryukova A.M., Khubaeva D.G., Krasnova V.G.

1) Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of the Russian Federation, Moscow, Russia 2) I.M. Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation (Sechenov University), Moscow, Russia
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.

Keywords

signaling pathways
folliculogenesis
in vitro maturation
Full text (in Russian)

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. Mackion N.S., Fauser B.C. Aspects of ovarian follicle development throughout life. 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. [Nazarenko T.A., Martirosyan Ya.O., Biryukova A.M., Dzhanashvili L.G., Ivanets T.Yu., Sukhova Yu.V. Experience in random-start ovarian stimulation for preserving reproductive material of cancer patients. Obstetrics and Gynegology. 2020; 4: 52-8. (in Russian)]. 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. 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. 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., Bergfelt D.R., Baerwald A.R., Pierson R.A. Comparative study of the dynamics of follicular waves in mares and women. 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. 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. Mackion N.S., Fauser B.C. Aspects of ovarian follicle development throughout life. 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. 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. 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. 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. 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. 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/cub.2014.09.023.
  18. Liu P., Cheng H., Roberts T.M., Zhao J.J. Targeting the phosphoinositide 3-kinase pathway in cancer. 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. 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. 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. 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.o^/10.1038/nm762.
  23. Liang J., Zubovitz J., Petrocelli 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. 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. 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. 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. 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. 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. 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. I GF-1 signaling is essential for FSH stimulation of AKT and steroidogenic genes in granulosa cells. Endocrinol. 2013; 27(3): 511-23. https://dx.doi.org/10.1210/me.2012-1307.
  34. Cargnello M., Roux PP Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. 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. 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. 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. 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. 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. 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. Fertil. Dev. 2018; 30(11): 1503-13. https://dx.doi.org/10.1071/rd17332.
  42. Godkin J. Transforming growth factor beta and the endometrium. 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. 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-p signalling from cell membrane to nucleus through SMAD proteins. 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. 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. 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. Res. Int. 2014; 2014: 213570. https://dx.doi.org/10.1155/2014/213570.

Received 30.09.2021

Accepted 14.12.2021 

About the Authors

Julia V. Sokolova, embryologist, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynaecology, and Perinatology, Ministry of Health of Russia, +7(495)438-13-41, julietsok@gmail.com, 117997, Russia, Moscow, Ac. Oparina str., 4.
Yana O. Martirosyan, Junior Researcher of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynaecology, and Perinatology, Ministry of Health of Russia, +7(925)124-99-99, marti-yana@index.ru, https://orcid.org/0000-0002-9304-4410, 117997, Russia, Moscow, Ac. Oparina str., 4.
Tatiana A. Nazarenko, MD, PhD, Head of the Institute of Reproductive Technologies, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynaecology, and Perinatology, Ministry of Health of Russia, +7(915)322-08-79, t.nazarenko@mail.ru, https://orcid.org/0000-0002-5823-1667, 117997, Russia, Moscow, Ac. Oparina str., 4.
Almina M. Birukova, MD, PhD, Head on Clinical Work of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen,
Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynaecology, and Perinatology, Ministry of Health of Russia, alma21@list.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Diana G. Khubaeva, student, I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University), +7(495)622-98-20, khubaeva.d@mail.ru, 119991, Russia, Moscow, Trubetskaya str., 8-2.
Valeria G. Krasnova, student of the Scientific and Educational Center for ART with the Clinical Division named after F. Paulsen, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynaecology, and Perinatology, Ministry of Health of Russia, +7(925)124-99-99, lkrasnova27@mail.com, 117997, Russia, Moscow, Ac. Oparina str., 4.

Authors’ contributions: Sokolova Yu.V., Martirosyan Ya.O., Nazarenko T.A., Biryukova A.M., Khubaeva D.G., Krasnova V.G. - development of the design of the investigation; obtaining data for analysis; review of publications on the topic of the article; analysis of the findings; writing the text of the manuscript.
Conflicts of interest: The authors declare that there are no possible conflicts of interest.
Funding: The investigation has not been sponsored.
For citation: Sokolova Yu.V., Martirosyan Ya.O., Nazarenko T.A., Biryukova A.M., Khubaeva D.G., Krasnova V.G. Molecular biological bases for intraovarian folliculogenesis, follicular maturation and recruitment.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 1:22-30 (in Russian)
https://dx.doi.org/10.18565/aig.2022.1.22-30

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