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Fibroblast growth factor-2 promotes in vitro activation of cat primordial follicles

Published online by Cambridge University Press:  13 April 2022

M.C. Müller ,
A.P.O. Monte ,
T.L.B.G. Lins ,
T.J.S. Macedo ,
V.R.P. Barros ,
V.C. Ferreira ,
D. Baraúna Jr. ,
C.R.O. Santos ,
A.R. Silva  and
M.H.T. Matos Open the ORCID record for M.H.T. Matos [Opens in a new window]
M.C. Müller
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
A.P.O. Monte
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
T.L.B.G. Lins
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
T.J.S. Macedo
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
V.R.P. Barros
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
V.C. Ferreira
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
D. Baraúna Jr.
Affiliation:
University Veterinary Clinic, Department of Veterinary Medicine, Federal University of São Francisco Valley, Petrolina, PE, Brazil
C.R.O. Santos
Affiliation:
University Veterinary Clinic, Department of Veterinary Medicine, Federal University of São Francisco Valley, Petrolina, PE, Brazil
A.R. Silva
Affiliation:
Laboratory of Animal Germplasm Conservation (LCGA), Universidade Federal Rural do Semi-Árido, Mossoró, RN, Brazil
M.H.T. Matos*
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, PE, Brazil
*
Author for correspondence: M.H.T. Matos. Universidade Federal do Vale do São Francisco (UNIVASF). Colegiado de Medicina Veterinária – Laboratório de Biologia Celular, Citologia e Histologia. Rodovia BR 407, Km 12, Lote 543 – Projeto de Irrigação Nilo Coelho – S/N, C1. CEP: 56300–990 – Petrolina – PE – Brasil. E-mail: [email protected]
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Summary

This study evaluated the effect of fibroblast growth factor-2 (FGF-2) on the morphology, primordial follicle activation and growth after in vitro culture of domestic cat ovarian tissue. Ovaries (n = 12) from prepubertal domestic cats were collected and fragmented. One fragment was fixed for histological analysis (fresh control). The remaining fragments were incubated in control medium alone or with 10, 50 or 100 ng/ml FGF-2 for 7 days. After in vitro culture, the following endpoints were analyzed: morphology, activation by counting primordial and developing follicles, and growth (follicle and oocyte diameters). Treatment with 100 ng/ml FGF-2 maintained (P > 0.05) the percentage of normal follicles similar to fresh control. Follicle survival was greater (P < 0.05) after culture in 100 ng/ml FGF-2 than in 50 ng/ml FGF-2. The percentage of primordial follicles decreased (P < 0.05) and the percentage of developing follicles increased (P < 0.05) in all treatments compared with fresh tissue. The proportion of developing follicles increased (P < 0.05) in tissues incubated with 100 ng/ml FGF-2 compared with control medium and other FGF-2 concentrations. Furthermore, culture in 10 or 100 ng/ml FGF-2 resulted in increased (P < 0.05) follicle and oocyte diameters compared with fresh tissues and MEM+. In conclusion, FGF-2 at 100 ng/ml maintains follicle survival and promotes the in vitro activation and growth of cat primordial follicles.

Keywords

FelineFGF-2FolliculogenesisParacrine factorViability
Type
Short Communication
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 730 - 734
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Baird, A. and Hsueh, A. J. (1986). Fibroblast growth factor as an intraovarian hormone: Differential regulation of steroidogenesis by an angiogenic factor. Regulatory Peptides, 16(3–4), 243–250. doi: 10.1016/0167-0115(86)90023-6 CrossRefGoogle ScholarPubMed
Barberino, R. S., Santos, J. M. S., Lins, T. L. B. G., Menezes, V. G., Monte, A. P. O., Gouveia, B. B., Palheta, R. C. Jr and Matos, M. H. T. (2020). Epigallocatechin-3-gallate (EGCG) reduces apoptosis of preantral follicles through the phosphatidylinositol-3-kinase/protein kinase B (PI3K/AKT) signaling pathway after in vitro culture of sheep ovarian tissue. Theriogenology, 155(1), 25–32. doi: 10.1016/j.theriogenology.2020.05.037 CrossRefGoogle ScholarPubMed
Bristol-Gould, S. and Woodruff, T. K. (2006). Folliculogenesis in the domestic cat (Felis catus). Theriogenology, 66(1), 5–13. doi: 10.1016/j.theriogenology.2006.03.019 CrossRefGoogle Scholar
Chaves, R. N., Martins, F. S., Saraiva, M. V. A., Celestino, J. J. H., Lopes, C. A. P., Correia, J. C., Verde, I. B., Matos, M. H. T., Báo, S. N., Name, K. P. O., Campello, C. C., Silva, J. R. V. and Figueiredo, J. R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro . Reproduction, Fertility and Development, 20(5), 640–647. doi: 10.1071/rd07195 CrossRefGoogle ScholarPubMed
Chaves, R. N., de Matos, M. H., Buratini, J. and de Figueiredo, J. R. (2012). The fibroblast growth factor family: Involvement in the regulation of folliculogenesis. Reproduction, Fertility and Development, 24(7), 905–915. doi: 10.1071/RD11318 CrossRefGoogle ScholarPubMed
Fujihara, M., Comizzoli, P., Wildt, D. E. and Songsasen, N. (2012). Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium. Reproduction in Domestic Animals, 47 Suppl. 6, 102–108. doi: 10.1111/rda.12022 CrossRefGoogle Scholar
Fujihara, M., Comizzoli, P., Keefer, C. L., Wildt, D. E. and Songsasen, N. (2014). Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biology of Reproduction, 90, 1–10.CrossRefGoogle ScholarPubMed
Fujihara, M., Yamamizu, K., Comizzoli, P., Wildt, D. E. and Songsasen, N. (2018). Retinoic acid promotes in vitro follicle activation in the cat ovary by regulating expression of matrix metalloproteinase 9. PLoS ONE, 13(8), e0202759. doi: 10.1371/journal.pone.0202759 CrossRefGoogle ScholarPubMed
Garor, R., Abir, R., Erman, A., Felz, C., Nitke, S. and Fisch, B. (2009). Effects of basic fibroblast growth factor on in vitro development of human ovarian primordial follicles. Fertility and Sterility, 91(5) Suppl., 1967–1975. doi: 10.1016/j.fertnstert.2008.04.075 CrossRefGoogle ScholarPubMed
Gospodarowicz, D. and Bialecki, H. (1979). Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology, 104(3), 757–764. doi: 10.1210/endo-104-3-757 CrossRefGoogle ScholarPubMed
Grosbois, J. and Demeestere, I. (2018). Dynamics of PI3K and Hippo signaling pathways during in vitro human follicle activation. Human Reproduction, 33(9), 1705–1714. doi: 10.1093/humrep/dey250 CrossRefGoogle ScholarPubMed
Grosbois, J., Devos, M. and Demeestere, I. (2020). Implications of nonphysiological ovarian primordial follicle activation for fertility preservation. Endocrine Reviews, 41(6), 847–872. doi: 10.1210/endrev/bnaa020 CrossRefGoogle ScholarPubMed
IUCN (International Union for Conservation of Nature and Natural Resources). (2016). The IUCN red list of threatened species. http://www.iucnredlist.org/ Google Scholar
Jiang, Z. L., Ripamonte, P., Buratini, J., Portela, V. M. and Price, C. A. (2011). Fibroblast growth factor-2 regulation of Sprouty and NR4A genes in bovine ovarian granulosa cells. Journal of Cellular Physiology, 226(7), 1820–1827. doi: 10.1002/jcp.22509 CrossRefGoogle ScholarPubMed
Kawamura, K., Cheng, Y., Suzuki, N., Deguchi, M., Sato, Y., Takae, S., Ho, C. H., Kawamura, N., Tamura, M., Hashimoto, S., Sugishita, Y., Morimoto, Y., Hosoi, Y., Yoshioka, N., Ishizuka, B. and Hsueh, A. J. W. (2013). Hippo signaling disruption and AKT stimulation of ovarian follicles for infertility treatment. Proceedings of the National Academy of Sciences of the United States of America, 110(43), 17474–17479. doi: 10.1073/pnas.1312830110 CrossRefGoogle ScholarPubMed
Lavranos, T. C., Rodgers, H. F., Bertoncello, I. and Rodgers, R. J. (1994). Anchorage-independent culture of bovine granulosa cells: The effects of basic fibroblast growth factor and dibutyryl cAMP on cell division and differentiation. Experimental Cell Research, 211(2), 245–251. doi: 10.1006/excr.1994.1084 CrossRefGoogle ScholarPubMed
Leonel, E. C. R., Vilela, J. M. V., Carrilho, D. J. and Lucci, C. M. (2018). Cat ovarian follicle ultrastructure after cryopreservation with ethylene glycol and dimethyl sulfoxide. Cryobiology, 83, 9–14. doi: 10.1016/j.cryobiol.2018.07.003 CrossRefGoogle ScholarPubMed
Li, J., Kawamura, K., Cheng, Y., Liu, S., Klein, C., Liu, S., Duan, E. K. and Hsueh, A. J. W. (2010). Activation of dormant ovarian follicles to generate mature eggs. Proceedings of the National Academy of Sciences of the United States of America, 107(22), 10280–10284. doi: 10.1073/pnas.1001198107 CrossRefGoogle ScholarPubMed
Lu, C. L., Yan, J., Zhi, X., Xia, X., Wang, T. R., Yan, L. Y., Yu, Y., Ding, T., Gao, J. M., Li, R. and Qiao, J. (2015). Basic fibroblast growth factor promotes macaque follicle development in vitro . Reproduction, 149(5), 425–433. doi: 10.1530/REP-14-0557 CrossRefGoogle ScholarPubMed
Matos, M. H. T., Van Den Hurk, R., Lima-Verde, I. B., Luque, M. C. A., Santos, K. D. B., Martins, F. S., Báo, S. N., Lucci, C. M. and Figueiredo, J. R. (2007). Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles. Cells, Tissues, Organs, 186(2), 112–120. doi: 10.1159/000103016 CrossRefGoogle ScholarPubMed
McLaughlin, M., Albertini, D. F., Wallace, W. H. B., Anderson, R. A. and Telfer, E. E. (2018). Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Molecular Human Reproduction, 24(3), 135–142. doi: 10.1093/molehr/gay002 CrossRefGoogle Scholar
Mishra, S. R., Thakur, N., Somal, A., Parmar, M. S., Reshma, R., Rajesh, G., Yadav, V. P., Bharti, M. K., Bharati, J., Paul, A., Chouhan, V. S., Sharma, G. T., Singh, G. and Sarkar, M. (2016). 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, 108, 98–111. doi: 10.1016/j.rvsc.2016.08.012 CrossRefGoogle ScholarPubMed
Monniaux, D., Clément, F., Dalbiès-Tran, R., Estienne, A., Fabre, S., Mansanet, C. and Monget, P. (2014). The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: What is the link? Biology of Reproduction, 90(4), 85. doi: 10.1095/biolreprod.113.117077 CrossRefGoogle ScholarPubMed
Nilsson, E., Parrott, J. A. and Skinner, M. K. (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Molecular and Cellular Endocrinology, 175(1–2), 123–130. doi: 10.1016/s0303-7207(01)00391-4 CrossRefGoogle ScholarPubMed
Peluso, J. J., Pappalardo, A. and Fernandez, G. (2001). Basic fibroblast growth factor maintains calcium homeostasis and granulosa cell viability by stimulating calcium efflux via a PKC delta-dependent pathway. Endocrinology, 142(10), 4203–4211. doi: 10.1210/endo.142.10.8460 CrossRefGoogle Scholar
Portela, V. M., Machado, M., Buratini, J., Zamberlam, G., Amorim, R. L., Gonçalves, P. and Price, C. A. (2010). Expression and function of fibroblast growth factor 18 in the ovarian follicle in cattle. Biology of Reproduction, 83(3), 339–346. doi: 10.1095/biolreprod.110.084277 CrossRefGoogle ScholarPubMed
Price, C. A. (2016). Mechanisms of fibroblast growth factor signaling in the ovarian follicle. Journal of Endocrinology, 228(2), R31–R43. doi: 10.1530/JOE-15-0414 CrossRefGoogle ScholarPubMed
Santos, J. M., Menezes, V. G., Barberino, R. S., Macedo, T. J., Lins, T. L. B. G., Gouveia, B. B., Barros, V. R., Santos, L. P., Gonçalves, R. J. and Matos, M. H. T. (2014). Immunohistochemical localization of fibroblast growth factor-2 in the sheep ovary and its effects on pre-antral follicle apoptosis and development in vitro . Reproduction in Domestic Animals, 49(3), 522–528. doi: 10.1111/rda.12322 CrossRefGoogle ScholarPubMed
Silva, H. V. R., Silva, A. R., da Silvada, L. D. M. and Comizzoli, P. (2019). Semen cryopreservation and banking for the conservation of Neotropical carnivores. Biopreservation and Biobanking, 17(2), 183–188. doi: 10.1089/bio.2018.0104 CrossRefGoogle ScholarPubMed
Thuwanut, P., Comizzoli, P., Wildt, D. E., Keefer, C. L. and Songsasen, N. (2017). Stem cell factor promotes in vitro ovarian follicle development in the domestic cat by upregulating c-kit mRNA expression and stimulating the phosphatidylinositol 3-kinase/AKT pathway. Reproduction, Fertility and Development, 29(7), 1356–1368. doi: 10.1071/RD16071 CrossRefGoogle ScholarPubMed
Tilly, J. L., Billig, H., Kowalski, K. I. and Hsueh, A. J. (1992). Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine kinase-dependent mechanism. Molecular Endocrinology, 6(11), 1942–1950. doi: 10.1210/mend.6.11.1480180 Google ScholarPubMed
Wildt, D. E., Swanson, W., Brown, J., Sliwa, A. and Vargas, A. (2010). Felids ex situ: Managed programmes, research and species recovery. In MacDonald, D. W. and Loveridge, A. J., (eds). Biology and conservation of wild felids. Oxford University Press.Google Scholar
Zhao, Q., Ma, Y., Sun, N. X., Ye, C., Zhang, Q., Sun, S. H., Xu, C., Wang, F. and Li, W. (2014). Exposure to bisphenol A at physiological concentrations observed in Chinese children promotes primordial follicle growth through the PI3K/Akt pathway in an ovarian culture system. Toxicology in Vitro, 28(8), 1424–1429. doi: 10.1016/j.tiv.2014.07.009 CrossRefGoogle Scholar