Morphology and Biochemistry of Ovulation Morfologia e bioquímica da ovulação

The process of ovulation involves multiple and iterrelated genetic, biochemical, and morphological events: cessation of the proliferation of granulosa cells, resumption of oocyte meiosis, expansion of cumulus cell-oocyte complexes, digestion of the follicle wall, and extrusion of the metaphase-II oocyte. The present narrative review examines these interrelated steps in detail. The combined or isolated roles of the folliclestimulating hormone (FSH) and luteinizing hormone (LH) are highlighted. Genes indiced by the FSH genes are relevant in the cumulus expansion, and LH-induced genes are critical for the resumption ofmeiosis and digestion of the follicle wall. A nonhuman model for follicle-wall digestion and oocyte release was provided.

Keywords:
granulosa cells; follicle-stimulating hormone; luteinizing hormone; oocytes; ovarian follicle

Authorship

Sebastião Freitas de Medeiros

Department of Gynecology and Obstetrics, Faculdade de Medicina, Universidade Federal do Mato Grosso, Cuiabá, Mato Grosso, MT, BrazilUniversidade Federal do Mato GrossoBrazilCuiabá, MT, BrazilDepartment of Gynecology and Obstetrics, Faculdade de Medicina, Universidade Federal do Mato Grosso, Cuiabá, Mato Grosso, MT, Brazil

Instituto Tropical de Medicina Reprodutiva, Cuiabá, Mato Grosso, MT, BrazilInstituto Tropical de Medicina ReprodutivaBrazilCuiabá, MT, BrazilInstituto Tropical de Medicina Reprodutiva, Cuiabá, Mato Grosso, MT, Brazil

http://orcid.org/0000-0003-1292-2515

Bruna Barcelo Barbosa

http://orcid.org/0000-0003-4218-6766

Matheus Antonio Souto de Medeiros

http://orcid.org/0000-0003-4069-7490

Márcia Marly Winck Yamamoto

http://orcid.org/0000-0002-4845-4226

Address for correspondence Sebastião Freitas de Medeiros, MD, Rua Henrique P Guedes, 195, Bairro Duque de Caxias, 78043-306, 900, Mato Grosso, MT, Brazil (e-mail: de.medeiros@terra.com.br).

Conflict of Interests

The authors have no conflict of interests to declare.

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Figures

Figures (9)

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Fig. 1
Structure of the periovulatory follicle showing internal and external theca cell layers, granulosa cells, and the oocyte.

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Fig. 2
Scheme showing the steroidogenesis of theca and granulosa ovarian cells. Abbreviations: P450ssc, cytochrome P450 for cleavage of cholesterol side chains; 3-βSHD, 3 β hydroxysteroid dehydrogenase; 17-HSD3, 17-hydroxysteroid dehydrogenase.

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Fig. 3
Biochemical events initiated by the follicle stimulating hormone (FSH) in the preovulatory follicle. Abbreviations: VEGF, vascular endothelial growth factor; COX-2, cyclaoxygenase-2; PKA, protein kinase A; PKC, protein kinase C.

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Fig. 4
Expression of several genes induced by the luteinizing hormone (LH) peak.

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Fig. 5
Combined actions of the FSH and LH in the expansion of oocyte-cumulus cells.

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Fig. 6
The role of the LH in meiosis resumption.

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Fig. 7
Cell-cell signaling between the oocyte and granulosa cells in the final stage of follicle development.

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Fig. 8
Role of LH-induced genes in the digestion of the follicular wall.

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Fig. 9
A model of follicle rupture during ovulation in the Japanese rice fish, also known as medaka. (A) In the follicle, a few hours before ovulation, progelatinase A is activated by membrane type 1-matrix metalloproteinase (MT1-MMP) on the surface of the oocyte, whereas gelatinase A is immediately inactivated by the tissue inhibitor of matrix metalloproteinases-2b (TIMP-2b). (B) At the time of ovulation, the hydrolysis of basement membrane type-IV collagen is initiated by active gelatinase A at the follicle–ovarian surface contact site. (C) membrane type 2-matrix metalloproteinase (MT2-MMP), which is now expressed on the surface of the granulosa cells, can degrade the type-I collagen that is present in the theca cell layer. (D) As a result, the oocyte is exposed at the contact site, leading to ovulation. Abbreviations: BM, basement membrane; EC, epithelial cell; GC, granulosa cell; OC, oocyte; TC, theca cell. Source: Ogiwara et al.⁴⁹49 Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T. Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci U S A. 2005;102(24):8442-8447. Doi: 10.1073/pnas.0502423102
https://doi.org/10.1073/pnas.0502423102... We would like to thank the National Academy of Sciences of the United States by permission

Fig. 1 Structure of the periovulatory follicle showing internal and external theca cell layers, granulosa cells, and the oocyte.

Fig. 2 Scheme showing the steroidogenesis of theca and granulosa ovarian cells. Abbreviations: P450ssc, cytochrome P450 for cleavage of cholesterol side chains; 3-βSHD, 3 β hydroxysteroid dehydrogenase; 17-HSD3, 17-hydroxysteroid dehydrogenase.

Source: Medeiros et al.⁷7 de Medeiros SF, Gil-Junior AB, Barbosa JS, Isaías ED, Yamamoto MM. New insights into steroidogenesis in normo- and hyperandrogenic polycystic ovary syndrome patients. Arq Bras Endocrinol Metabol. 2013;57(06):437-444. Doi: 10.1590/s0004-27302013000600005
https://doi.org/10.1590/s0004-2730201300...

Fig. 3 Biochemical events initiated by the follicle stimulating hormone (FSH) in the preovulatory follicle. Abbreviations: VEGF, vascular endothelial growth factor; COX-2, cyclaoxygenase-2; PKA, protein kinase A; PKC, protein kinase C.

Fig. 4 Expression of several genes induced by the luteinizing hormone (LH) peak.

Source: Richards et al.²³23 Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN. Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol. 1998;145(1-2):47-54. Doi: 10.1016/s0303-7207(98)00168-3
https://doi.org/10.1016/s0303-7207(98)00... Abbreviations: PO, preovulatory; PR, progesterone receptor; PGS, prostaglandins; C/EBPβ, CAAT enhancer-binding protein β; p27KIP1, cyclin-dependent kinase inhibitor 1B; Start 5, steroidogenic enzymes; IGF, insulin growth factor; COX, cyclooxygenase.

Fig. 5 Combined actions of the FSH and LH in the expansion of oocyte-cumulus cells.

Source: Richards et al.²³23 Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN. Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol. 1998;145(1-2):47-54. Doi: 10.1016/s0303-7207(98)00168-3
https://doi.org/10.1016/s0303-7207(98)00... Abbreviations: HA, hyaluronic acid; GDF, growth defferentation factor; BMP, bone morphogenetic protein; PE, prostaglandin E receptor.

Fig. 6 The role of the LH in meiosis resumption.

Source: Coticchio et al.²⁸28 Coticchio G, Dal-Canto M, Guglielmo MC, Mignini-Renzini M, Fadini R. Human oocyte maturation in vitro. Int J Dev Biol. 2012;56(10-12):909-918. Doi: 10.1387/ijdb.120135gv
https://doi.org/10.1387/ijdb.120135gv... Abbreviations: TGFβ, transforming growth factor β; EGF, epidermal growth factor.

Fig. 7 Cell-cell signaling between the oocyte and granulosa cells in the final stage of follicle development.

Source: Adapted from: Sutton et al.²⁹29 SuttonML,Gilchrist RB, Thompson JG. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Update. 2003;9(01):35-48. Doi: 10.1093/humupd/dmg009
https://doi.org/10.1093/humupd/dmg009... Abbreviations: GDF-9, growth differentiation factor 9; BMP-15, bone morphogenetic protein 15; FGF-8B, fibroblast growth factor 8B.

Fig. 8 Role of LH-induced genes in the digestion of the follicular wall.

Fig. 9 A model of follicle rupture during ovulation in the Japanese rice fish, also known as medaka. (A) In the follicle, a few hours before ovulation, progelatinase A is activated by membrane type 1-matrix metalloproteinase (MT1-MMP) on the surface of the oocyte, whereas gelatinase A is immediately inactivated by the tissue inhibitor of matrix metalloproteinases-2b (TIMP-2b). (B) At the time of ovulation, the hydrolysis of basement membrane type-IV collagen is initiated by active gelatinase A at the follicle–ovarian surface contact site. (C) membrane type 2-matrix metalloproteinase (MT2-MMP), which is now expressed on the surface of the granulosa cells, can degrade the type-I collagen that is present in the theca cell layer. (D) As a result, the oocyte is exposed at the contact site, leading to ovulation. Abbreviations: BM, basement membrane; EC, epithelial cell; GC, granulosa cell; OC, oocyte; TC, theca cell. Source: Ogiwara et al.⁴⁹49 Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T. Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci U S A. 2005;102(24):8442-8447. Doi: 10.1073/pnas.0502423102
https://doi.org/10.1073/pnas.0502423102... We would like to thank the National Academy of Sciences of the United States by permission

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Morphology and Biochemistry of Ovulation Morfologia e bioquímica da ovulação

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[1] Address for correspondence Sebastião Freitas de Medeiros, MD, Rua Henrique P Guedes, 195, Bairro Duque de Caxias, 78043-306, 900, Mato Grosso, MT, Brazil (e-mail: de.medeiros@terra.com.br).