Acquisition of gonadotropin dependence by early antral follicles and the challenges to promote their growth in vitro
DOI:
https://doi.org/10.1590/1809-6891v25e-75908EAbstract
This review aims to discuss the main factors involved in the development of early antral follicles until gonadotropin dependence. This follicular phase is characterized by intense proliferation of granulosa cells, formation of a fluid- illed cavity, morphological differentiation of cumulus cells, mural granulosa cells and recruitment of theca cells. The interaction between oocyte, granulosa and theca cells is crucial for follicular growth and hormone production. Growth factors produced by the oocyte, such as growth and differentiation factor-9 (GDF-9) and bone morphogenetic protein-15 (BMP-15), regulate granulosa cell proliferation and differentiation and antral cavity development, as well as stimulate the production of follicle-stimulating hormone (FSH) receptors in granulosa cells. In response to FSH, granulosa cells secrete C-type natriuretic peptide (CNP), which acts through its receptor to increase cyclic guanosine monophosphate (cGMP) production and consequently follicular development. Granulosa cells also produce insulin-like growth factor-1 (IGF-1) and increase aromatase enzyme activity, which results in greater sensitivity to gonadotropins and follicular steroidogenesis. The absence of IGF-1 signaling causes cessation of follicular growth at the early antral stage. Many other local factors are involved in the regulation of follicular development. Therefore, this review brings relevant data for a better understanding of the mechanisms involved in the control of early antral follicle growth, emphasizing the role of endocrine and paracrine factors, the oocyte-granulosa cell interaction and the processes of follicular atresia. The challenges for the establishment of efficient culture systems for in vitro growth of early antral follicles are also discussed.
Downloads
References
Sirait B, Wiweko B, Jusuf AA, Iftitah D, Muharam R. Oocyte competence biomarkers associated with oocyte maturation: Frontiers in Cell and Developmental Biology. 2021. 30(9): 710292. doi: https://doi.org/10.3389/fcell.2021.710292
Dode MAN, Rodovalho NC, Ueno VG, Alves RGO. Effect of follicle size in nuclear and cytoplasmic maturation of oocytes from zebu cows, Pesquisa Agropecuaria Brasileira. 2000; 35: 207-214. doi: https://doi.org/10.1590/S0100-204X2000000100023
Pavlok A, Lucas-Hahn A, Niemann H. Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Molecular Reproduction and Development. 1992; 31: 63-67. doi: https://doi.org/10.1002/mrd.1080310111
Němcová L, Hulínska P, Ješeta M, Kempisty B, Kaňka J, Machatková M. Expression of selected mitochondrial genes during in vitro maturation of bovine oocytes related to their meiotic competence. Theriogenology. 2019; 133: 104-112. doi: https://doi.org/10.1016/j.theriogenology.2019.05.001
Varmosfaderani SR, Hajian M, Jafarpour F, Zadegan FG, Nasr-Esfahani MH. Granulosa secreted factors improve the developmental competence of cumulus oocyte complexes from small antral follicles in sheep. PloS one. 2020; 15: e0229043. doi: https://doi.org/10.1371/journal.pone.0229043
Oliveira MEF, Ferreira RM, Mingoti GZ. Local and systemic control of bovine follicular growth and selection. Revista Brasileira de Reprodução Animal. 2011; 35: 418-432. Disponível em www.cbra.org.br
Silva JR, Figueiredo JR, Van Den Hurk R. Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology. 2009; 71(8):1193-208. doi: https://doi.org/10.1016/j.theriogenology.2008.12.01
Baumgartem SC, Stocco C. Granulosa Cells. Encyclopedia of Reproduction. 2018; 2: 8-13. doi: https://doi.org/10.1016/B978-0-12-801238-3.64623-8
Vasconcelos GL, Saraiva MVA, Costa JJN, Passos MJ, Silva AWB, Rossi RODS, et al. Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles. Reproduction, Fertility and Development. 2012; 25: 1194-1203. doi: http://dx.doi.org/10.1071/RD12173
Kim JW, Kang KM, Yoon TK, Shim SH, Lee WS. Study of circulating hepcidin in association with iron excess, metabolic syndrome, and BMP-6 expression in granulosa cells in women with polycystic ovary syndrome. Fertility and Sterility. 2014;102(2):548-554.e2. doi: https://doi.org/10.1016/j.fertnstert.2014.04.031
Sakaguchi K, Huang W, Yang Y, Yanagawa Y, Nagano M. Relationship between in vitro growth of bovine oocytes and steroidogenesis of granulosa cells cultured in medium supplemented with bone morphogenetic protein-4 and follicle stimulating hormone. Theriogenology. 2017; 97: 113-123. doi: http://dx.doi.org/10.1016/j.theriogenology.2017.04.030.
Paulino LRFM, de Assis EIT, Azevedo VAN, Silva BR, da Cunha EV, Silva JRV. Why Is It So Difficult To Have Competent Oocytes from In vitro Cultured Preantral Follicles? Reproductive Sciences. 2022; 29(12):3321-3334. doi: https://doi.org/10.1007/s43032-021-00840-8
Pangas SA, Rajkovic A. Matzuk MM. CHAPTER 10 - Follicular development: mouse, sheep, and human models. In: Jimmy D. Neill, Knobil and Neill's Physiology of Reproduction (Third Edition), Academic Press, 2006, pages 383-423, ISBN 9780125154000.
Orisaka M, Jiang JY, Orisaka S, Kotsuji F, Tsang BK. Growth differentiation factor 9 promotes rat preantral follicle growth by up‐regulating follicular androgen biosynthesis. Endocrinology. 2009; 150: 2740‐2748. doi: https://doi.org/10.1210/en.2008-1536
Gougeon A. Dynamics of follicular growth in the human: A model from preliminary results. Human Reproduction. 1986; 1: 81-87. doi: https://doi.org/10.1093/oxfordjournals.humrep.a136365
Campbell BK, Scaramuzzi RJ and Webb R. Control of antral follicle development and selection in sheep and cattle. Journal Reproduction Fertility, Supplement, 1995; 49: 335–350. doi: https://hdl.handle.net/102.100.100/231568?index=1
Webb RB, Nicholas JG, Gong BK, Campbell CG, Gutierrez HA, Garverick DG. Mechanism regulating follicular development and selection of the dominant follicle. Reproduction, Supplement. 2003; 23: 123- 234. doi: https://cir.nii.ac.jp/crid/1573387450361202816
Berlinguer F, Leoni GG, Succu S, Spezzigu A, Madeddu M and Satta V. Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. Journal of Pineal Research. 2009; 46: 383-391. doi https://doi.org/10.1111/j.1600-079X.2009.00674.x
Zeleznik AJ, Plant TM. Control of the Menstrual Cycle. Knobil and Neill's Physiology of Reproduction 2014: 1307‐1362. doi: https://doi.org/10.1016/B978-0-12-571136-4.50008-5
Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics.1997; 15: 201- 204. doi: https://doi.org/10.1038/ng0297-201
McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocrinology Review. 2000; 21: 200-214. doi: https://doi.org/10.1210/edrv.21.2.0394
Fushimi Y, Takagi M, Monniaux D, Uno S, Kokushi E, Shinya U. Effects of dietary contamination by zearalenone and its metabolites on serum anti‐Müllerian hormone: Impact on the reproductive performance of breeding cows. Reproduction. 2021; 50: 834-839. doi: https://doi.org/10.1111/rda.12599
Tetsuka M, Whitelaw PF, Bremner WJ, Millar MR, Smyth CD, Hillier SG. Developmental regulation of androgen receptor in rat ovary. Journal of Endocrinology. 1995; 145: 535‐543. doi: https://doi.org/10.1677/joe.0.1450535
Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. Journal of Clinical Investigation. 1998; 101: 2622‐2629. doi: https://doi.org/10.1172/JCI2081
Wang H, Andoh K, Hagiwara H. Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice. Endocrinology. 2001; 142: 4930‐4936. doi: https://doi.org/10.1210/endo.142.11.8482
Shiina H, Matsumoto T, Sato T. Premature ovarian failure in androgen receptor‐deficient mice. Proceedings of the National Academy of Sciences. 2006; 103: 224‐229. doi: https://doi.org/10.1073/pnas.0506736102
Sen A, Hammes SR. Granulosa cell‐specific androgen receptors are critical regulators of ovarian development and function. Molecular Endocrinology.
; 24: 1393‐1403. doi: https://doi.org/10.1210/me.2010-0006
Walters KA, Middleton LJ, Joseph SR. Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Molecular Biology Reports. 2012; 87: 151. doi: https://doi.org/10.1095/biolreprod.112.102012
Dewailly D, Robin G, Peigne M, Decanter C, Pigny P, Catteau-Jonard S. Interactions between androgens, FSH, anti-Müllerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Human Reproduction Update.
; 22: 709-724. doi: https://doi.org/10.1093/humupd/dmw027
Khan H L, Bhatti S, KhanYL, Abbas S, Munir Z, Sherwani IAR et al. Cell-free nucleic acids and melatonin levels in human follicular fluid predict embryo quality in patients undergoing in-vitro fertilization treatment. J. Gynecol. Obstet. Human Reproduction. 2020; 49: (1), 101624. doi: https://doi.org/10.1016/j.jogoh.2019.08.007
Barros VRP, Cavalcante AYP, Macedo TJS, Barberino RS, Lins TLB, Gouveia BB et al. Immunolocalization of melatonin and follicle-stimulating hormone receptors in caprine ovaries and their effects during in vitro development of isolated pre-antral follicles. Reproduction. 2013; 48: 1025–1033. doi: https://doi.org/10.1111/rda.12209
Barros VRP, Monte APO, Santos JMS, Lins TLBG, Cavalcante, AYP, Gouveia, BB. Melatonin improves development, mitochondrial function and promotes the meiotic resumption of sheep oocytes from in vitro grown secondary follicles. Theriogenology. 2020; 144: 67-73. doi: https://doi.org/10.1016/j.theriogenology.2019.12.006
Sato Y, Cheng Y, Kawamura K, Takae S, Hsueh AJ.. C-type natriuretic peptide stimulates ovarian follicle development. Molecular endocrinology.2012, 26(7), 1158-1166. doi: https://doi.org/10.1210/me.2012-1027
Alam Md, Hasanur JL, Takashi M. GDF9 and BMP15 induce development of antrum-like structures by bovine granulosa cells without oocytes. The Journal of Reproduction and development. 2018; 64(5): 423-431. doi: http://doi.org/10.1262/jrd.2018-078
Reinen PS, Coria MS, Barrionuevo MG, Hernández O, Callejas S, Palma GA. Gene expression of growth factor BMP15, GDF9, FGF2 and their receptors in bovine follicular cells/Gene expression of growth factor BMP15, GDF9, FGF2 and their receptors in bovine follicular cells. MVZ Córdoba. 2018; 3(23): 6778-6787. doi: http://doi.org/10.21897/rmvz.1367.
Morikawa R, Jibak L,Takashi M. Effects of oocyte-derived growth factors on the growth of porcine oocytes and oocyte–cumulus cell complexes in vitro. The Journal of Reproduction and Develoment. 2021; 67(4): 273-281. doi: http://doi.org/10.1262/jrd.2021-026
Ma X, Huashan Y. BMP15 regulates FSHR via TGF-β II receptor and SMAD4 signaling in the prepubertal ovary of Rongchang pigs. Research in Veterinary Science. 2022; 143: 66-73. doi: http://doi.org/10.1016/j.rvsc.2021.12.013
Vitt UA, Mazerbourg S, Klein C, Hsueh AJ. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biology of reproduction. 2002; 67: 473-480. doi: http://doi.org/10.1095/biolreprod67.2.473
Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, et al. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. M Endocrinology 2004;18.3: 653-665. doi: http://doi.org/10.1210/me.2003-0393
Juengel JL, Bodensteiner KJ, Heath DA, Hudson NL, Moeller CL, Smith P, et al.Physiology of GDF9 and BMP15 signalling molecules. A reproduction science 2004; 82: 447-460. doi: http://doi.org/10.1016/j.anireprosci.2004.04.021
Vitt UA, McGee EA, Hayashi M, Hsueh AJ. In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 2000; 141.10: 3814-3820. doi: http://doi.org/10.1210/endo.141.10.7732
Spicer LJ, Aad PY, Allen DT, Mazerbourg S, Payne AH, Hsueh AJ. Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biology of Reproduction 2008;78.2: 243-253. doi: http://doi.org/10.1095/biolreprod.107.063446
Cheng Y, Kawamura K, Taka S, Deguchi M, Yang Q, Kuo C, et. Oocyte-derived R-spondin2 promotes ovarian follicle development. Jornal FASEB 2013;27: 2175-2184. doi: http://doi.org/10.1096/fj.12-223412
Chang HM, Fang L, Cheng JC, Taylor EL, Sun YP, Leung PC. Effects of growth differentiation factor 8 on steroidogenesis in human granulosa-lutein cells. Fertility and sterility 2016;105: 520-528. Doi: http://doi.org/10.1016/j.fertnstert.2015.10.034
Mishra SR, Thakur N, Somal A, Parmar MS, Reshma R, Rajesh G, et al. "Expression and localization of fibroblast growth factor (FGF) family in buffalo ovarian follicle during different stages of development and modulatory role of FGF2 on steroidogenesis and survival of cultured buffalo granulosa cells. Research in Veterinary Science 2016; 108: 98-111. doi: http://doi.org/10.1016/j.rvsc.2016.08.012
Mattar D., Samir M., Laird M., Knight PG. Modulatory effects of TGF-β1 and BMP6 on thecal angiogenesis and steroidogenesis in the bovine ovary. Reproduction. 2020;159(4), 397-408. doi: https://doi.org/10.1530/REP-19-0311
Sugiyama M, Sumiya M, Shirasuna K, Kuwayama T, Iwata H. Addition of granulosa cell mass to the culture medium of oocytes derived from early antral follicles increases oocyte growth, ATP content, and acetylation of H4K12. Zygote 2016;24.6: 848-856. doi: http://doi.org/10.1017/S0967199416000198
Yang Y, Kanno C, Huang W, Kang SS, Yanagawa Y, Nagano M. Effect of bone morphogenetic protein-4 on in vitro growth, steroidogenesis and subsequent developmental competence of the oocyte-granulosa cell complex derived from bovine early antral follicles. Reproductive Biology and Endocrinology 2016; 14:1: 1-8. doi; http://doi.org/10.1186/s12958-016-0137-1
Laird, M., Glister, C., Cheewasopit, W., Satchell, L. S., Bicknell, A. B., Knight, P. G. Free inhibin α subunit is expressed by bovine ovarian theca cells and its knockdown suppresses androgen production. Scientific reports, 2019. 9(1), 19793. doi: https://doi.org/10.1038/s41598-019-55829-w
Sun T, Diaz FJ. Ovulatory signals alter granulosa cell behavior through YAP1 signaling. Reproductive Biology Endocrinology. 2019; 17(1):113. doi: https://doi.org/10.1186/s12958-019-0552-1
McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, et al. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction. 2005; 129(4): 481-7. doi: https://doi.org/10.1530/rep.1.0511
Hoque SAM, Kawai T, Zhu Z, Shimada M. Mitochondrial protein turnover is critical for granulosa cell proliferation and differentiation in antral follicles. Journal of the Endocrine Society. 2018; 3(2): 324-339. doi: https://doi.org/10.1210/js.2018-00329
Alam MH, Miyano T. Interaction between growing oocytes and granulosa cells in vitro. Reproductive Medicine and Biology. 2019; 19(1): 13-23. doi: https://doi.org/10.1002/rmb2.12292
Orisaka M, Hattori K, Fukuda S, Mizutani T, Miyamoto K, Sato T, et al. Dysregulation of ovarian follicular development in female rat: LH decreases FSH sensitivity during preantral-early antral transition. Endocrinology. 2013; 154(8): 2870-80. doi: https://doi.org/10.1210/en.2012-2173
Urata Y, Salehi R, Lima PDA, Osuga Y, Tsang BK. Neuropeptide Y regulates proliferation and apoptosis in granulosa cells in a follicular stage-dependent manner. Journal of Ovarian Research. 2020; 13(1): 5. doi: https://doi.org/10.1186/s13048-019-0608-z
Baddela VS, Sharma A, Michaelis M, Vanselow J. HIF1 driven transcriptional activity regulates steroidogenesis and proliferation of bovine granulosa cells. Scientific Reports. 2020; 10(1): 3906. doi: https://doi.org/10.1038/s41598-020-60935-1
Braw-Tal R, Roth Z. Gene expression for LH receptor, 17 alpha-hydroxylase and StAR in the theca interna of preantral and early antral follicles in the bovine ovary. Reproduction. 2005; 129(4): 453-61. doi: https://doi.org/10.1530/rep.1.00464
Samie KA, Tabandeh MR, Afrough M. Betaine ameliorates impaired steroidogenesis and apoptosis in mice granulosa cells induced by high glucose concentration. Systems Biology in Reproductive Medicine. 2020; 66(6): 400-409. doi: https://doi.org/10.1080/19396368.2020.1811423
Douville G, Sirard MA. Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles. Journal of Ovarian Research. 2014; 7: 50. doi: https://doi.org/10.1186/1757-2215-7-50
Jeon MJ, Choi YS, Yoo JJ, Atala A, Jackson JD. Optimized culture system to maximize ovarian cell growth and functionality in vitro. Cell Tissue Research. 2021; 385(1): 161-171. doi: https://doi.org/10.1007/s00441-021-03415-w
Wang N, Zhao F, Lin P, Zhang G, Tang K, Wang A, et al. Knockdown of XBP1 by RNAi in Mouse Granulosa Cells Promotes Apoptosis, Inhibits Cell Cycle, and Decreases Estradiol Synthesis. International Journal of Molecular Sciences. 2017; 18(6): 1152. doi: https://doi.org/10.3390/ijms18061152
Kishi H, Kitahara Y, Imai F, Nakao K, Suwa H. Expression of the gonadotropin receptors during follicular development. Reproductive Medicine and Biology. 2017; 17(1): 11-19. doi: https://doi.org/10.1002/rmb2.12075
Ginther OJ, Beg MA, Bergfelt DR, Donadeu FX, Kot K. Follicle selection in monovular species. Biology of Redroduction. 2001; 65(3): 638-47. doi: https://doi.org/10.1186/s12958-018-0332-3
Rivera GM, Fortune JE. Selection of the dominant follicle and insulin-like growth factor (IGF)-binding proteins: evidence that pregnancy-associated plasma protein A contributes to proteolysis of IGF-binding protein 5 in bovine follicular fluid. Endocrinology. 2003; 144(2): 437-46. doi: https://doi.org/10.1210/en.2002-220657
Zhou P, Baumgarten SC, Wu Y, 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. Molecular Endocrinology. 2013; 27(3): 511-23. doi: https:// https://doi.org/10.1210/me.2012-1307
Guan HY, Xia HX, Chen XY, Wang L, Tang ZJ, Zhang W. Toll-like receptor 4 inhibits estradiol secretion via NF-κB signaling in human granulosa cells. Frontiers in Endocrinology. 2021; 12: 629554. doi: https://doi.org/10.3389/fendo.2021.629554
Forrest KK, Flores VV, Gurule SC, Soto-Navarro S, Shuster CB, Gifford CA, et al. Effects of lipopolysaccharide on follicular estrogen production and developmental competence in bovine oocytes. Animal Reproduction Science. 2022; 237: 106927. doi: https://doi.org/10.1016/j.anireprosci.2022.106927
Meng L, Jan SZ, Hamer G, van Pelt AM, van der Stelt I, Keijer J, Teerds KJ. Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostly through apoptosis. Biology of Reproduction. 2018; 1;99(4):853-863. doi: https://doi.org/10.1093/biolre/ioy116
Spanel-Borowski K. Follicle stages and follicular atresia. In Atlas of the Mammalian Ovary Morphological Dynamics and Potential Role of Innate Immunity. Spanel-Borowski K, Germany, 2012, pp. 9-22. doi: https://link.springer.com/book/10.1007/978-3-642-30535-1
Silva JR, Báo SN, Lucci CM, Carvalho FC, Andrade ER, Ferreira MA, Figueiredo JR. Morphological and ultrastructural changes occurring during degeneration of goat preantral follicles preserved in vitro. Animal Reproduction Science. 2001; 66(3-4):209-223. doi: https://doi.org/10.1016/s0378-4320(01)00102-6
Pajokh M, Mesbah F, Bordbar H, Talaei-Khozani T. Different cell death types determination in juvenile mice ovarian follicles. Iranian Journal of Veterinary Research. 2018;19(4): 298-303. doi: PMC6361600.
Zhou J, Peng X, Mei S. Autophagy in ovarian follicular development and atresia. International Journal of Biological Sciences. 2019; 15: 726-737. doi: https://doi.org/10.7150/ijbs.30369
Soares PHA, Junqueira FS. Reproductive features of the bovine female: Review. Pubvet. 2019; 13: 1-6. doi: https://doi.org/10.31533/pubvet.v13n02a257.1-6
Landry DA, Sirard M. Follicle capacitation: A meta-analysis to investigate the transcriptome dynamics following FSH decline in bovine granulosa cells. Biology of Reproduction. 2018; 99: 877-887. doi: https://doi.org/10.1093/biolre/ioy090
Meng L, Jan SZ, Hamer G, Van Pelt AM, Van der Stelt I, Keijer J. et al. Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostlythrough apoptosis. Biology of Reproduction. 2018; 99: 853-863. doi: https://doi.org/10.1093/biolre/ioy116
Harada M, Miyano T, Matsumura K, Osaki S, Miyake M, Kato S. Bovine oocytes from early antral follicles grow to meiotic competence in vitro: effect of FSH and hypoxanthine. Theriogenology. 1997; 48: 743-755. doi: https://doi.org/10.1016/S0093-691X(97)00298-7
Yamamoto K, Otoi T, Koyama N, Horikita N, Tachikawa S, Miyano T. Development to live young from bovine small oocytes after growth, maturation and fertilization in vitro. Theriogenology. 1999; 52: 81-89. doi: https://doi.org/10.1016/S0093-691X(99)00111-9
Alm H, Kątska-Książkiewicz L, Ryńska B, Tuchscherer A. Survival and meiotic competence of bovine oocytes originating from early antral ovarian follicles. Theriogenology. 2006; 65: 1422-1434. doi: https://doi.org/10.1016/j.theriogenology.2005.08.014
de Sá NA, Ferreira AC, Sousa FG, Duarte AB, Paes VM, Cadenas J, et al. First pregnancy after in vitro culture of early antral follicles in goats: positive effects of anethole on follicle development and steroidogenesis. Molecular Reproduction and Development. 2020; 87: 966-977. Doi: https://doi.org/10.1002/mrd.23410
Cadenas J, Leiva-Revilla J. Vieira LA, Apolloni LB, Aguiar FLN, Alves BG, et al. Caprine ovarian follicle requirements differ between preantral and early antral stages after IVC in medium supplemented with GH and VEGF alone or in combination. Theriogenology. 2017; 87: 321-332. doi: https://doi.org/10.1016/j.theriogenology.2016.09.008
Ferreira, ACA, Cadenas J, Sá NA, Correia HH, Guerreiro DD, Lobo CH, et al. In vitro culture of isolated preantral and antral follicles of goats using human recombinant FSH: Concentration-dependent and stage-specific effect. Animal Reproduction Science. 2018; 196: 120-129. doi: https://doi.org/10.1016/j.anireprosci.2018.07.004
Lopes EPF, Rodrigues GQ, de Brito DCC, Rocha RMP, Ferreira ACA, de Sá NA, et al. Vitrification of caprine secondary and early antral follicles as a perspective to preserve fertility function. Reproductive Biology. 2020; 20: 371-378. doi: https://doi.org/10.1016/j.repbio.2020.05.001
Cordeiro EB, Silva BR, Paulino LR, Barroso PA, Barrozo LG, de Lima Neto MF, and Silva JR. Effects of N-acetylcysteine on growth, viability and reactive oxygen species levels in small antral follicles cultured in vitro. Asian Pacific Journal of Reproduction, 2023; 12(1), 42. doi: https://doi.org/10.1016/j.anireprosci.2021.106801
Jiang Y, He Y, Pan X, Wang P, Yuan X, Ma B. Advances in oocyte maturation in vivo and in vitro in mammals. International Journal of Molecular Sciences. 2023; 21;24(10):9059. doi: https://doi.org/10.3390/ijms24109059
Huang W, Nagano M, Kang SS, Yanagawa Y, Takahashi Y. Effects of in vitro growth culture duration and prematuration culture on maturational and developmental competences of bovine oocytes derived from early antral follicles. Theriogenology 2013; 80:793–9. doi: https://doi.org/10.1016/j.theriogenology.2013.07.004
Senbon S, Miyano T. Bovine oocytes in early antral follicles grow in serum- free media: effect of hypoxanthine on follicular morphology & oocyte growth. Zygote 2002;10:301–9. doi: https://doi.org/10.1017/S0967199402004033
Bezerra FTG, Silva AWB, Rissi VB, Rosa PA, Cesaro MP, Costa JJN, Gonçalves PBD and Silva JRV. Cilostamide and follicular hemisections inhibit oocyte meiosis resumption and regulate gene expression and cAMP levels in bovine cumulus–oocyte complexes. Livestock Science, 2016; 184, 112–118. doi: https://doi.org/10.1016/j.livsci.2015.12.014
Barrozo LG, Silva BR, Paulino LR, Barbalho EC, Nascimento DR, Costa FC, and Silva JR. N-acetyl cysteine reduces levels of reactive oxygen species and improves in vitro maturation of oocytes from medium-sized bovine antral follicles. Zygote, 2022; 30(6), 882-890. doi: https://doi.org/10.1017/S0967199422000429
He Y, Meng K, Wang X, Dong, Z, Zhang, Y, Quan F. Comparison of bovine small antral follicle development in two-and three-dimensional culture systems. Annals of the Brazilian Academy of Sciences. 2020; 92, e20180935. doi: https://doi.org/10.1590/0001-3765202020180935
Bezerra FTG, Lima FEO, Paulino LRFM, Silva BR, Silva AWB, Souza ALP, Van Den Hurk R and Silva JRV. In vitro culture of secondary follicles and prematuration of cumulus–oocyte complexes from antral follicles increase the levels of maturation-related transcripts in bovine oocytes. Molecular Reproduction and Development. 2019; 86 (12), 1874–1886. doi: https://doi.org/10.1002/mrd.23284
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Brazilian Animal Science/ Ciência Animal Brasileira
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g. in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).