Современные воззрения на ранние этапы фолликулогенеза и механизмы формирования преждевременной недостаточности яичников

Марченко Л.А., Машаева Р.И., Чернуха Г.Е. Современные воззрения на ранние этапы фолликулогенеза и механизмы формирования преждевременной недостаточности яичников. Гинекология. 2020; 22 (5): 57–60. DOI: 10.26442/20795696.2020.5.200440

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Marchenko L.A., Mashaeva R.I., Chernukha G.E. Current views on the molecular mechanisms of the initial stages of folliculogenesis. Gynecology. 2020; 22 (5): 67–60. DOI: 10.26442/20795696.2020.5.200440

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Аннотация

Яичник – уникальная структура женского организма, в которой одновременно представлены различные морфогистологические единицы – от примордиальных до доминантных фолликулов. В последние десятилетия внимание ученых направлено на изучение механизмов фолликулогенеза на гонадотропин-зависимой стадии. В то время как более сложные и продолжительные процессы, определяющие судьбу фолликула, происходят от момента их рекрутирования до преантральной стадии зрелости (около 290 дней), до доминантной зрелости проходит еще 60 дней. В настоящее время доказано, что внутри фолликула устанавливается межклеточная коммуникация, предполагающая двунаправленный обмен информацией между ооцитом и его «компаньонами» – гранулезными и тека-клетками посредством ауто- и паракринных взаимодействий c помощью различных генов, факторов роста и цитокинов. Цель обзора – изучить интрафолликулярные факторы, контролирующие ранние этапы фолликулогенеза, и их нарушения, которые в конечном счете могут привести к развитию преждевременной недостаточности яичников.

Ключевые слова: фолликулогенез, преждевременная недостаточность яичников, ооцит, яичник, яйцеклетка.

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The ovary is a unique structure of the female body, which simultaneously presents various morphohistological units-from primordial to dominant follicles. Over the past decades, scientists have focused on studying the mechanisms of folliculogenesis at the gonadotropin-dependent stage. While more complex and lengthy processes that determine the fate of the follicle occur from the moment of their recruitment to the preantral stage of maturity (about 290 days), another 60 days pass before the dominant maturity. Currently, it has been proved that intercellular communication is established within the follicle, which involves a bidirectional exchange of information between the oocyte and its “companions” – granulose and Teka cells through auto-and paracrine interactions using various genes, growth factors and cytokines. The purpose of this review was to study intrafollicular factors that control the early stages of folliculogenesis and other disorders that may ultimately lead to the development of premature ovarian failure.

Key words: premature ovarian failure, folliculogenesis, premature ovarian failure, oocyte, ovary, ovum.

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Список литературы

1. Адамян Л.В., Дементьева В.О., Смольникова В.Ю. и др. Новые возможности хирургии в восстановлении утраченных функций яичников при преждевременной недостаточности яичников у женщин репродуктивного возраста. Доктор.ру. 2019; 11 (166): 44–9.
[Adamian L.V., Dement'eva V.O., Smol'nikova V.Iu. et al. Novye vozmozhnosti khirurgii v vosstanovlenii utrachennykh funktsii iaichnikov pri prezhdevremennoi nedostatochnosti iaichnikov u zhenshchin reproduktivnogo vozrasta. Doktor.ru. 2019; 11 (166): 44–9 (in Russian).]
2. Williams CJ, Erickson GF. Morphology and Physiology of the Ovary. https://www.ncbi.nlm.nih.gov/books/NBK278951/
3. Зубарев И.В. Роль хронических поражений печени матери в нарушении становления эндокринной и репродуктивной функции яичников потомства в условиях эксперимента. Автореф. дис. … канд. биол. наук. Оренбург, 2012.
[Zubarev I.V. Rol' khronicheskikh porazhenii pecheni materi v narushenii stanovleniia endokrinnoi i reproduktivnoi funktsii iaichnikov potomstva v usloviiakh eksperimenta. Avtoref. dis. … kand. biol. nauk. Orenburg, 2012 (in Russian).]
4. Choi JK, Agarwal P, Huang H et al. The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials 2014; 35 (19): 5122–8.
5. Faddy MJ, Gosden R. A mathematical model of follicle dynamics in the human ovary. Hum Reprod 1995; 10 (4): 770–5.
6. Wallace WHB, Kelsey TW. Human ovarian reserve from conception to the menopause. PloS One 2010; 5 (1): e8772.
7. The ESHRE Guideline Group on POI, Webber L, Davies M, Anderson R et al. ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod 2016; 31 (5): 926–37. DOI: 10.1093/humrep/dew027
8. Tingen C, Kim A, Woodruff TK. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009; 15 (12): 795–803.
9. Ford EA, Beckett EL, Roman SD et al. Advances in human primordial follicle activation and premature ovarian insufficiency. Reproduction 2020; 159 (1): R15–29.
10. Штаут М.И., Курило Л.Ф. Состав соматических и половых клеток гонад человека в пре- и постнатальный период. Онтогенез. 2019; 2: 127–40.
[Shtaut M.I., Kurilo L.F. Sostav somaticheskikh i polovykh kletok gonad cheloveka v pre- i postnatal'nyi period. Ontogenez. 2019; 2: 127–40 (in Russian).]
11. Ye H, Zheng T, Li W et al. Ovarian Stem Cell Nests in Reproduction and Ovarian Aging. Cell Physiol Biochem 2017; 43 (5): 1917–25.
12. De Felici M, Klinger FG, Farini D et al. Establishment of oocyte population in the fetal ovary: primordial germ cell proliferation and oocyte programmed cell death. Reprod BioMed Online 2005; 10 (2): 182–91.
13. Grive KJ, Freiman RN. The developmental origins of the mammalian ovarian reserve. Development 2015; 142 (15): 2554–63.
14. Suzuki N, Yoshioka N, Takae S et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod 2015; 30 (3): 608–15.
15. Borum K. Oogenesis in the mouse: A study of the meiotic prophase. Exp Cell Res 1961. 24 (3): 495–507.
16. Ideta A, Yamashita S, Seki-Soma M et al. Generation of exogenous germ cells in the ovaries of sterile NANOS3-null beef cattle. Sci Rep 2016; 6 (1): 1–9.
17. Rehnitz J, Alcoba DD, Brum IS et al. FMR1 and AKT/mTOR signalling pathways: potential functional interactions controlling folliculogenesis in human granulosa cells. Reprod BioMed Online 2017; 35 (5): 485–93.
18. Боровая Т.Г. Половая система. Руководство по гистологии. СПб.: СпецЛит, 2011; с. 398–425.
[Borovaia T.G. The reproductive system. Histology guide. Saint Petersburg: SpetsLit, 2011; p. 398–425 (in Russian).]
19. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1986; 1 (2): 81–7.
20. Sanfins A, Rodrigues P, Albertini DF. GDF-9 and BMP-15 direct the follicle symphony. J Assist Reprod Genet 2018; 35 (10): 1741–50.
21. Dalman A, Totonchi M, Valojerdi M. Human Ovarian Theca-Derived Multipotent Stem Cells Have The Potential To Differentiate Into Oocyte-Like Cells In Vitro. Cell J 2019; 20 (4): 527–36.
22. Hao X, Anastácio A, Liu K et al. Ovarian Follicle Depletion Induced by Chemotherapy and the Investigational Stages of Potential Fertility-Protective Treatments – A Review. Int J Mol Sci 2019; 20 (19): 4720.
23. Wang J-J, Ge W, Liu J-C et al. Complete in vitro oogenesis: retrospects and prospects. Cell Death Differ 2017; 24 (11): 1845–52.
24. Sonigo C, Beau I, Binart N et al. Anti-Müllerian Hormone in Fertility Preservation: Clinical and Therapeutic Applications. Clin Med Insights Reprod Health 2019; 13.
25. Каменицкий И.С. Выявление факторов формирования фолликулов в яичниках детей: кисспептина, рецептора кисспептина, ароматазы, рецептора антимюллерова гормона. СПб.: 2017.
[Kamenitsky I.S. Identification of follicular formation factors in the ovaries of children: kisspeptin, kisspeptin receptor, aromatase, anti-Müllerian hormone receptor. Saint Petersburg, 2017 (in Russian).]
26. Cheng Y, Kawamura K, Takae S et al. Oocyte-derived R-spondin2 promotes ovarian follicle development. FASEB J 2013; 27 (6): 2175–84.
27. Jagarlamudi K, Rajkovic A. Oogenesis: Transcriptional regulators and mouse models. Mol Cell Endocrinol 2011; 356: 31–9.
28. Kawashima I, Kawamura K. Regulation of follicle growth through hormonal factors and mechanical cues mediated by Hippo signaling pathway. Syst Biol Reprod Med 2018; 64 (1): 3–11.
29. Williams CJ, Erickson GF. Morphology and Physiology of the Ovary. 2012 Jan 30. In: Feingold KR, Anawalt B, Boyce A (Eds.) Endotext. South Dartmouth (MA): MDText.com, Inc., 2000.
30. Марченко Л.А., Машаева Р.И. Клинико-лабораторная оценка овариального резерва с позиции репродуктолога. Акушерство и гинекология. 2018; 8.
[Marchenko L.A., Mashaeva R.I. Kliniko-laboratornaia otsenka ovarial'nogo rezerva s pozitsii reproduktologa. Akusherstvo i ginekologiia. 2018; 8 (in Russian).]
31. Skinner MK. Regulation of Primordial Follicle Assembly and Development. Hum Reprod Update 2005; 11 (5): 461–71.
32. Steinkampf MP, Mendelson CR, Simpson ER. Effects of Epidermal Growth Factor and Insulin-like Growth Factor I on the Levels of mRNA Encoding Aromatase Cytochrome P-450 of Human Ovarian Granulosa Cells. Mol Cell Endocrinol 1988; 59 (1–2): 93–9.
33. Ipsa E, Cruzat VF, Kagize JN et al. Growth Hormone and Insulin-Like Growth Factor Action in Reproductive Tissues. Front Endocrinol 2019; 10: 777.
34. Hsueh AJW, Kawamura K, Cheng Y et al. Intraovarian Control of Early Folliculogenesis. Endocrine Rev 2015; 36 (1): 1–24.
35. Денисенко М.В., Курцер М.А., Курило Л.Ф. Динамика формирования фолликулярного резерва яичников. Андрология и генитальная хирургия. 2016; 17 (2): 20–8.
[Denisenko M.V., Kurtser M.A., Kurilo L.F. Trends in the formation of the ovarian follicular reserve. Andrology and Genital Surgery. 2016; 17 (2): 20–8 (in Russian).]
36. Taghavi SA, Ashrafi M, Mehdizadeh M et al. Toll-like receptors expression in follicular cells of patients with poor ovarian response. Int J Fertil Steril 2014; 8 (2): 183–92.
37. Dupont J, Scaramuzzi RJ. Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle. Biochem J 2016; 473 (11): 1483–501.
38. Sreerangaraja Urs DB, Wu W-H, Komrskova K et al. Mitochondrial Function in Modulating Human Granulosa Cell Steroidogenesis and Female Fertility. Int J Mol Sci 2020. 21 (10): 3592.
39. Ganesan S, Keating AF. Ovarian mitochondrial and oxidative stress proteins are altered by glyphosate exposure in mice. Toxicol Appl Pharmacol 2020; 402: 115116.
40. Czuchlej SC, Volonteri MC, Scaia MF, Ceballos NR. Characterization of StAR protein of Rhinella arenarum (Amphibia, Anura). Gen Comp Endocrinol 2020; 295: 113535.
41. Selvaraj V, Stocco DM, Clark BJ. Current knowledge on the acute regulation of steroidogenesis. Biol Reprod 2018; 99 (1): 13–26.
42. Papadopoulos V, Aghazadeh Y, Fan J et al. Translocator protein-mediated pharmacology of cholesterol transport and steroidogenesis. Mol Cell Endocrinol 2015; 408: 90–8.
43. Lounas A, Vernoux N, Germain M et al. Mitochondrial sub-cellular localization of cAMP-specific phosphodiesterase 8A in ovarian follicular cells. Sci Rep 2019; 9 (1): 1–10.
44. Sugiura K, Su Y-Q, Diaz FJ et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007; 134 (14): 2593.
45. Park M, Shin E, Won M et al. FOXL2 Interacts with Steroidogenic Factor-1 (SF-1) and Represses SF-1-Induced CYP17 Transcription in Granulosa Cells. Mol Endocrinol 2010; 24 (5): 1024–36.
46. Baker SJ, Spears N. The role of intra-ovarian interactions in the regulation of follicle dominance. Hum Reprod Update 1999; 5 (2): 153–65.

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1. Adamian L.V., Dement'eva V.O., Smol'nikova V.Iu. et al. Novye vozmozhnosti khirurgii v vosstanovlenii utrachennykh funktsii iaichnikov pri prezhdevremennoi nedostatochnosti iaichnikov u zhenshchin reproduktivnogo vozrasta. Doktor.ru. 2019; 11 (166): 44–9 (in Russian).
2. Williams CJ, Erickson GF. Morphology and Physiology of the Ovary. https://www.ncbi.nlm.nih.gov/books/NBK278951/
3. Zubarev I.V. Rol' khronicheskikh porazhenii pecheni materi v narushenii stanovleniia endokrinnoi i reproduktivnoi funktsii iaichnikov potomstva v usloviiakh eksperimenta. Avtoref. dis. … kand. biol. nauk. Orenburg, 2012 (in Russian).
4. Choi JK, Agarwal P, Huang H et al. The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials 2014; 35 (19): 5122–8.
5. Faddy MJ, Gosden R. A mathematical model of follicle dynamics in the human ovary. Hum Reprod 1995; 10 (4): 770–5.
6. Wallace WHB, Kelsey TW. Human ovarian reserve from conception to the menopause. PloS One 2010; 5 (1): e8772.
7. The ESHRE Guideline Group on POI, Webber L, Davies M, Anderson R et al. ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod 2016; 31 (5): 926–37. DOI: 10.1093/humrep/dew027
8. Tingen C, Kim A, Woodruff TK. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009; 15 (12): 795–803.
9. Ford EA, Beckett EL, Roman SD et al. Advances in human primordial follicle activation and premature ovarian insufficiency. Reproduction 2020; 159 (1): R15–29.
10. Shtaut M.I., Kurilo L.F. Sostav somaticheskikh i polovykh kletok gonad cheloveka v pre- i postnatal'nyi period. Ontogenez. 2019; 2: 127–40 (in Russian).
11. Ye H, Zheng T, Li W et al. Ovarian Stem Cell Nests in Reproduction and Ovarian Aging. Cell Physiol Biochem 2017; 43 (5): 1917–25.
12. De Felici M, Klinger FG, Farini D et al. Establishment of oocyte population in the fetal ovary: primordial germ cell proliferation and oocyte programmed cell death. Reprod BioMed Online 2005; 10 (2): 182–91.
13. Grive KJ, Freiman RN. The developmental origins of the mammalian ovarian reserve. Development 2015; 142 (15): 2554–63.
14. Suzuki N, Yoshioka N, Takae S et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod 2015; 30 (3): 608–15.
15. Borum K. Oogenesis in the mouse: A study of the meiotic prophase. Exp Cell Res 1961. 24 (3): 495–507.
16. Ideta A, Yamashita S, Seki-Soma M et al. Generation of exogenous germ cells in the ovaries of sterile NANOS3-null beef cattle. Sci Rep 2016; 6 (1): 1–9.
17. Borovaia T.G. The reproductive system. Histology guide. Saint Petersburg: SpetsLit, 2011; p. 398–425 (in Russian).
19. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1986; 1 (2): 81–7.
20. Sanfins A, Rodrigues P, Albertini DF. GDF-9 and BMP-15 direct the follicle symphony. J Assist Reprod Genet 2018; 35 (10): 1741–50.
21. Dalman A, Totonchi M, Valojerdi M. Human Ovarian Theca-Derived Multipotent Stem Cells Have The Potential To Differentiate Into Oocyte-Like Cells In Vitro. Cell J 2019; 20 (4): 527–36.
22. Hao X, Anastácio A, Liu K et al. Ovarian Follicle Depletion Induced by Chemotherapy and the Investigational Stages of Potential Fertility-Protective Treatments – A Review. Int J Mol Sci 2019; 20 (19): 4720.
23. Wang J-J, Ge W, Liu J-C et al. Complete in vitro oogenesis: retrospects and prospects. Cell Death Differ 2017; 24 (11): 1845–52.
24. Sonigo C, Beau I, Binart N et al. Anti-Müllerian Hormone in Fertility Preservation: Clinical and Therapeutic Applications. Clin Med Insights Reprod Health 2019; 13.
25. Kamenitsky I.S. Identification of follicular formation factors in the ovaries of children: kisspeptin, kisspeptin receptor, aromatase, anti-Müllerian hormone receptor. Saint Petersburg, 2017 (in Russian).
26. Cheng Y, Kawamura K, Takae S et al. Oocyte-derived R-spondin2 promotes ovarian follicle development. FASEB J 2013; 27 (6): 2175–84.
27. Jagarlamudi K, Rajkovic A. Oogenesis: Transcriptional regulators and mouse models. Mol Cell Endocrinol 2011; 356: 31–9.
28. Kawashima I, Kawamura K. Regulation of follicle growth through hormonal factors and mechanical cues mediated by Hippo signaling pathway. Syst Biol Reprod Med 2018; 64 (1): 3–11.
29. Williams CJ, Erickson GF. Morphology and Physiology of the Ovary. 2012 Jan 30. In: Feingold KR, Anawalt B, Boyce A (Eds.) Endotext. South Dartmouth (MA): MDText.com, Inc., 2000.
30. Marchenko L.A., Mashaeva R.I. Kliniko-laboratornaia otsenka ovarial'nogo rezerva s pozitsii reproduktologa. Akusherstvo i ginekologiia. 2018; 8 (in Russian).
31. Skinner MK. Regulation of Primordial Follicle Assembly and Development. Hum Reprod Update 2005; 11 (5): 461–71.
32. Steinkampf MP, Mendelson CR, Simpson ER. Effects of Epidermal Growth Factor and Insulin-like Growth Factor I on the Levels of mRNA Encoding Aromatase Cytochrome P-450 of Human Ovarian Granulosa Cells. Mol Cell Endocrinol 1988; 59 (1–2): 93–9.
33. Ipsa E, Cruzat VF, Kagize JN et al. Growth Hormone and Insulin-Like Growth Factor Action in Reproductive Tissues. Front Endocrinol 2019; 10: 777.
34. Hsueh AJW, Kawamura K, Cheng Y et al. Intraovarian Control of Early Folliculogenesis. Endocrine Rev 2015; 36 (1): 1–24.
35. Denisenko M.V., Kurtser M.A., Kurilo L.F. Trends in the formation of the ovarian follicular reserve. Andrology and Genital Surgery. 2016; 17 (2): 20–8 (in Russian).
36. Taghavi SA, Ashrafi M, Mehdizadeh M et al. Toll-like receptors expression in follicular cells of patients with poor ovarian response. Int J Fertil Steril 2014; 8 (2): 183–92.
37. Dupont J, Scaramuzzi RJ. Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle. Biochem J 2016; 473 (11): 1483–501.
38. Sreerangaraja Urs DB, Wu W-H, Komrskova K et al. Mitochondrial Function in Modulating Human Granulosa Cell Steroidogenesis and Female Fertility. Int J Mol Sci 2020. 21 (10): 3592.
39. Ganesan S, Keating AF. Ovarian mitochondrial and oxidative stress proteins are altered by glyphosate exposure in mice. Toxicol Appl Pharmacol 2020; 402: 115116.
40. Czuchlej SC, Volonteri MC, Scaia MF, Ceballos NR. Characterization of StAR protein of Rhinella arenarum (Amphibia, Anura). Gen Comp Endocrinol 2020; 295: 113535.
41. Selvaraj V, Stocco DM, Clark BJ. Current knowledge on the acute regulation of steroidogenesis. Biol Reprod 2018; 99 (1): 13–26.
42. Papadopoulos V, Aghazadeh Y, Fan J et al. Translocator protein-mediated pharmacology of cholesterol transport and steroidogenesis. Mol Cell Endocrinol 2015; 408: 90–8.
43. Lounas A, Vernoux N, Germain M et al. Mitochondrial sub-cellular localization of cAMP-specific phosphodiesterase 8A in ovarian follicular cells. Sci Rep 2019; 9 (1): 1–10.
44. Sugiura K, Su Y-Q, Diaz FJ et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007; 134 (14): 2593.
45. Park M, Shin E, Won M et al. FOXL2 Interacts with Steroidogenic Factor-1 (SF-1) and Represses SF-1-Induced CYP17 Transcription in Granulosa Cells. Mol Endocrinol 2010; 24 (5): 1024–36.
46. Baker SJ, Spears N. The role of intra-ovarian interactions in the regulation of follicle dominance. Hum Reprod Update 1999; 5 (2): 153–65.

Авторы

Л.А. Марченко*, Р.И. Машаева, Г.Е. Чернуха

ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии имени академика В.И. Кулакова» Минздрава России, Москва, Россия
*l.a.marchenko@yandex.ru

________________________________________________

Larisa A. Marchenko*, Roza I. Mashaeva, Galina E. Chernukha

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*l.a.marchenko@yandex.ru

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