Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-22T10:57:06.008Z Has data issue: false hasContentIssue false

Influence of gonadotropins on ovarian follicle growth and development in vivo and in vitro

Published online by Cambridge University Press:  08 June 2017

Maxim Filatov*
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia.
Yulia Khramova
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia.
Elena Parshina
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia.
Tatiana Bagaeva
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia.
Maria Semenova
Affiliation:
Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia.
*
All correspondence to: Maxim Filatov. Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1, bld. 12, Moscow 119991, Russia. *Tel: +7 495 939 39 00. E-mail: maxfilat@yandex.ru

Summary

Gonadotropins are the key regulators of ovarian follicles development. They are applied in therapeutic practice in assisted reproductive technology clinics. In the present review we discuss the basic gonadotropic hormones – recombinant human follicle-stimulating hormone, its derivatives, luteinizing hormone and gonadotropin serum of pregnant mares, their origin, and application in ovarian follicle systems in in vitro culture systems.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adriaens, I., Cortvrindt, R. & Smitz, J. (2004). Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum. Reprod. 19, 398408.Google Scholar
Bedecarrats, G.Y., O'Neill, F.H., Norwitz, E.R., Kaiser, U.B., Teixeira, J. (2003). Regulation of gonadotropin gene expression by Müllerian inhibiting substance. Proc. Natl. Acad. Sci. USA 100, 9348–53.Google Scholar
Bhide, P. & Homburg, R. (2016). Anti-Müllerian hormone and polycystic ovary syndrome. Best. Pract. Res. Clin. Obstet. Gynaecol. 37, 3845.CrossRefGoogle ScholarPubMed
Casarini, L., Santi, D., Marino, M. (2015). Impact of gene polymorphisms of gonadotropins and their receptors on human reproductive success. Reproduction 150, 175–84.Google Scholar
Choi, J. & Smitz, J. (2014). Luteinizing hormone and human chorionic gonadotropin: origins of difference. Mol. Cel. Endocrinol. 383, 203–13.Google Scholar
Cimino, I., Casoni, F., Liu, X., Messina, A., Parkash, J., Jamin, S.P., Catteau-Jonard, S., Collier, F., Baroncini, M., Dewailly, D., Pigny, P., Prescott, M., Campbell, R., Herbison, A.E., Prevot, V. & Giacobini, P. (2016). Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat. Commun. 7, 10055–66.Google Scholar
Cortvrindt, R.G., Hu, Y., Liu, J. & Smitz, J.E. (1998). Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotropin. Fertil. Steril. 70, 1114–25.CrossRefGoogle ScholarPubMed
Dierich, A., Sairam, M.R., Monaco, L., Fimia, G.M., Gansmuller, A., LeMeur, M. & Sassone-Corsi, P. (1998). Impairing follicle-stimulating hormone (FSH) signalling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. USA 95, 13612–7.Google Scholar
Dunn, L. & Fox, K.R. (2009). Techniques for fertility preservation in patients with breast cancer. Curr. Opin. Obstet. Gynecol. 21, 6873.CrossRefGoogle ScholarPubMed
Dunning, K.R., Akison, L.K., Russell, D.L., Norman, R.J. & Robker, R.L. (2011). Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Biol. Reprod. 85, 548–55.CrossRefGoogle ScholarPubMed
Durlinger, A.L., Kramer, P., Karels, B., de Jong, F.H., Uilenbroek, J.T., Grootegoed, J.A. & Themmen, A.P. (1999). Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 140, 5789–96.Google Scholar
Edson, M.A., Nagaraja, A.K. & Matzuk, M.M. (2009). the mammalian ovary from genesis to revelation. Endocr. Rev. 30, 624712.Google Scholar
Edwards, L.J., Kind, K.L., Armstrong, D.T. & Thompson, J.G. (2004). The effects of recombinant human follicle stimulating hormone (rhFSH) on embryo development in mice. Physiol. Endocrinol. Metab. 288, 845–51.Google Scholar
Ezcurra, D. & Humaidan, P. (2014). A review of luteinising hormone and human chorionic gonadotropin when used in assisted reproductive technology. Reprod. Biol. Endocrinol. 12, 112.Google Scholar
Fabbri, R. (2006). Cryopreservation of human oocytes and ovarian tissue. Cell Tissue Bank 7, 113–22.Google Scholar
Fan, H.Y., Liu, Z., Shimada, M., Sterneck, E., Johnson, P.F., Hedrick, S.M. & Richards, J.S. (2009). MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324, 938–41.Google Scholar
Filatov, M.A., Khramova, Y.V., Kiseleva, M.V., Malinova, I.V., Komarova, E.V. & Semenova, M.L. (2016). Female fertility preservation strategies: cryopreservation and ovarian tissue in vitro culture, current state of the art and future perspectives. Zygote 4, 119.Google Scholar
Filatov, M.A., Khramova, Y.V. & Semenova, M.L. (2015). In vitro mouse ovarian follicle growth and maturation in alginate hydrogel: current state of the art. Acta Naturae 7, 4856.Google Scholar
Gal, A., Lin, P., Barger, A.M, MacNeill, A.L. & Ko, C. (2014). Vaginal fold histology reduces the variability introduced by vaginal exfoliative cytology in the classification of mouse estrous cycle stages. Toxicol. Pathol. 42, 1212–20.Google Scholar
Hayes, E., Kushnir, V., Ma, X., Biswas, A., Prizant, H., Gleicher, N. & Sen, A. (2016). Intra-cellular mechanism of anti-Müllerian hormone (AMH) in regulation of follicular development. Mol. Cell. Endocrinol. 433, 5665.Google Scholar
Hornick, J.E., Duncan, F.E., Shea, L.D. & Woodruff, T.K. (2013). Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction 145, 126.CrossRefGoogle ScholarPubMed
Hu, J., Ma, X., Bao, J.C., Li, W., Chen, D., Gao, Z., Lei, A., Yang, C. & Wang, H. (2011). Insulin–transferrin–selenium (ITS) improves maturation of porcine oocytes in vitro . Zygote 19, 191–7.Google Scholar
Ilgaz, N.S., Aydos, O.S., Karadag, A., Taspinar, M., Eryilmaz, O.G. & Sunguroglu, A. (2015). Impact of follicle-stimulating hormone receptor variants in female infertility. J. Assist. Reprod. Genet. 32, 1659–68.Google Scholar
Jin, S.Y., Lei, L., Shikanov, A., Shea, L.D. & Woodruff, T.K. (2010). A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil. Steril. 93, 2633–9.Google Scholar
Kelley, R.L., Kind, K.L., Lane, M., Robker, R.L., Thompson, J.G. & Edwards, L.J. (2006). Recombinant human follicle-stimulating hormone alters maternal ovarian hormone concentrations and the uterus and perturbs fetal development in mice. Physiol. Endocrinol. Metab. 291, 761–70.Google Scholar
Knight, P.G. & Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191206.CrossRefGoogle ScholarPubMed
Kosheleva, N.V., Ilina, I.V., Zurina, I.M., Roskova, A.E., Gorkun, A.A., Ovchinnikov, A.V., Agranat, M.B. & Saburina, I.N. (2016). Laser-based technique for controlled damage of mesenchymal cell spheroids: a first step in studying reparation in vitro . Biol. Open. 7, 9931000.Google Scholar
Kreeger, P.K., Fernandes, N.N., Woodruff, T.K. & Shea, L.D. (2005). Regulation of mouse follicle development by follicle-stimulating hormone in three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol. Reprod. 73, 942–50.Google Scholar
Lee, M.M., Donahoe, P.K., Hasegawa, T., Silverman, B., Crist, G.B., Best, S., Hasegawa, Y., Noto, R.A., Schoenfeld, D. & MacLaughlin, D.T. (1996). Müllerian inhibiting substance in humans: normal levels from infancy to adulthood. J. Clin. Endocrinol. Metab. 81, 571–6.Google Scholar
Li, L., Zhou, X., Wang, X., Wang, J., Zhang, W., Wang, B., Cao, Y. & Kee, K. (2016). A dominant negative mutation at the ATP binding domain of AMHR2 is associated with a defective anti-Müllerian hormone signaling pathway. Mol. Hum. Reprod. 22, 669–78.Google Scholar
Liu, X., Qiao, P., Jiang, A., Jiang, J., Han, H., Wang, L. & Ren, C. (2015). Paracrine regulation of steroidogenesis in theca cells by granulosa cells derived from mouse preantral follicles. BioMed. Res. Int. 2015, 18.Google ScholarPubMed
Loreti, N., Ambao, V., Andreone, L., Trigo, R., Bussmann, U. & Campo, S. (2013b). Effect of sialylation and complexity of FSH oligosaccharides on inhibin production by granulosa cells. Reproduction 145, 127–35.Google Scholar
Loreti, N., Fresno, C., Barrera, D., Andreone, L., Albarran, S.L., Fernandez, E.A., Larrea, F. & Campo, S. (2013a). The glycan structure in recombinant human FSH affects endocrine activity and global gene expression in human granulosa cells. Mol. Cel. Endocrinol. 366, 6880.Google Scholar
Lunenfeld, B. (2004). Historical perspectives in gonadotrophin therapy. Hum. Reprod. Update 10, 453–67.Google Scholar
Łebkowska, A. & Kowalska, I. (2017). Anti-Müllerian hormone and polycystic ovary syndrome. Endokrynol. Pol. 68, 74–8.Google Scholar
Macklon, N.S., Stouffer, R.L., Giudice, L.C. & Fauser, B.C. (2006). the science behind 25 years of ovarian stimulation for in vitro fertilization. Endocr. Rev. 27, 170207.Google Scholar
Meczekalski, B., Czyzyk, A., Kunicki, M., Podfigurna-Stopa, A., Plociennik, L., Jakiel, G., Maciejewska-Jeske, M. & Lukaszuk, K. (2016). Fertility in women of late reproductive age: the role of serum anti-Müllerian hormone (AMH) levels in its assessment. J. Endocrinol. Invest. 39, 1259–65.Google Scholar
Morgan, S., Campbell, L., Allison, V., Murray, A. & Spears, N. (2015). Culture and co-culture of mouse ovaries and ovarian follicles. J. Vis. Exp. 97, 110.Google Scholar
Park, K.E., Ku, S.U., Jung, K.C., Liu, H.C., Kim, Y.Y., Kim, Y.J., Kim, S.H., Choi, Y.M., Kim, J.G. & Moon, S.Y. (2013). Effects of urinary and recombinant gonadotropins on in vitro maturation outcomes of mouse preantral follicles. Reprod. Sci. 20, 909–16.Google Scholar
Pierre, A., Peigne, M., Grynberg, M., Arouche, N., Taieb, J., Hesters, L., Gonzales, J., Picard, J.Y., Dewailly, D., Fanchin, R., Catteau-Jonard, S. & di Clemente, N. (2013). Loss of LH-induced down-regulation of anti-müllerian hormone receptor expression may contribute to anovulation in women with polycystic ovary syndrome. Hum. Reprod. 28, 762–9.Google Scholar
Rajpert-De Meyts, E., Jorgensen, N., Graem, N., Muller, J., Cate, R.L. & Skakkebaek, N.E. (1999). Expression of anti-Müllerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J. Clin. Endocr. Metab. 84, 3836–44.Google Scholar
Richards, J.S., Russell, D.L., Ochsner, S., Hsieh, M., Doyle, K.H., Falender, A.E., Lo, Y.K. & Sharma, S.C. (2002). Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent. Prog. Horm. Res. 57, 195220.Google Scholar
Roche, J.F. (1996). Control and regulation of folliculogenesis – a symposium in perspective. Rev. Reprod. 1, 1927.Google Scholar
Ruman, J.I., Pollak, S., Trousdale, R.K., Klein, J. & Lustbader, J.W. (2005). Effects of long-acting recombinant human follicle-stimulating hormone analogs containing N-linked glycosylation on murine folliculogenesis. Fertil. Steril. 83, 1303–9.Google Scholar
Sanchez, F., Romero, S., Albuz, F.K. & Smitz, J. (2012). In vitro follicle growth under non-attachment conditions and decreased FSH levels reduces Lhcgr expression in cumulus cells and promotes oocyte developmental competence. Assist. Reprod. Genet. 29, 141–52.Google Scholar
Segers, I., Adriaenssens, T., Wathlet, S. & Smitz, J. (2012). Gene expression differences induced by equimolar low doses of LH or hCG in combination with FSH in cultured mouse antral follicles. J. Endocrinol. 215. 269–80.CrossRefGoogle ScholarPubMed
Shikanov, A., Xu, M., Woodruff, T.K. & Shea, L.D. (2009). interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476–85.Google Scholar
Skory, R.M., Xu, Y., Shea, L.D. & Woodruff, T.K. (2015). Engineering the ovarian cycle using in vitro follicle culture. Hum. Reprod. 30, 1386–95.Google Scholar
Sun, F., Betzendahl, I., Shen, Y., Cortvrindt, R., Smitz, J. & Eichenlaub-Ritter, U. (2004). Preantral follicle culture as a novel in vitro assay in reproductive toxicology testing in mammalian oocytes. Mutagenesis 19, 1325.CrossRefGoogle ScholarPubMed
Trousdale, R.K., Yu, B., Pollak, S.V., Husami, N., Vidali, A. & Lustbader, J.V. (2009). Efficacy of native and hyperglycosylated follicle stimulating hormone analogues for promoting fertility in female mice. Fertil. Steril. 91, 265–70.CrossRefGoogle ScholarPubMed
Visser, J.A. & Themmen, A.P. (2005). Anti-Müllerian hormone and folliculogenesis. Mol. Cell. Endocrinol. 234, 81–6.Google Scholar
Wang, S., Yang, S., Lai, Z., Ding, T., Shen, W., Shi, L., Jiang, J., Ma, L., Tian, Y., Du, X., Luo, A. & Wang, S. (2013). Effects of culture and transplantation on follicle activation and early follicular growth in neonatal mouse ovaries. Cell Tissue Res. 354, 609–21.Google Scholar
Weenen, C., Laven, J.S., Von Bergh, A.R., Cranfield, M., Groome, N.P., Visser, J.A., Kramer, P., Fauser, B.C. & Themmen, A.P. (2004). Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 10, 7783.Google Scholar
West, E.R., Xu, M., Woodruff, T.K. & Shea, L.D. (2007). Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials 28, 4439–48.Google Scholar
Wolfenson, C., Groisman, J., Couto, A.S., Hedenfalk, M., Cortvrindt, R.G., Smitz, J.E. & Jespersen, S. (2005). Batch-to-batch consistency of human-derived gonadotrophin preparations compared with recombinant preparations. Reprod. Biomed. Online 10, 442–54.Google Scholar
Xu, J., Lawson, M.S., Yeoman, R.R., Molskness, T.A., Ting, A.Y., Stouffer, R.L. & Zelinski, M.B. (2013). Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 28, 2187–200.Google Scholar
Xu, M., Banc, A., Woodruff, T.K. & Shea, L.D. (2009). Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol. Bioeng. 103, 378–86.CrossRefGoogle ScholarPubMed
Zhang, Y.L., Liu, X.M., Ji, S.Y., Sha, Q.Q., Zhang, J. & Fan, H.Y. (2015). ERK1/2 activities are dispensable for oocyte growth but are required for meiotic maturation and pronuclear formation in mouse. J. Genet. Genom. 42, 477–85.CrossRefGoogle Scholar