Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-23T00:39:04.943Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of jacalin and follicle-stimulating hormone on in vitro goat primordial follicle activation, survival and gene expression

Published online by Cambridge University Press:  29 May 2014

Regislane P. Ribeiro ,
Antonia M.L.R. Portela ,
Anderson W.B. Silva ,
José J.N. Costa ,
José R.S. Passos ,
Ellen V. Cunha ,
Glaucinete B. Souza ,
Márcia V.A. Saraiva ,
Mariana A. M. Donato  and
Christina. A. Peixoto
...Show all authors
Regislane P. Ribeiro
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Antonia M.L.R. Portela
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Anderson W.B. Silva
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
José J.N. Costa
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
José R.S. Passos
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Ellen V. Cunha
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Glaucinete B. Souza
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Márcia V.A. Saraiva
Affiliation:
Biotechnology Nucleus of Sobral–NUBIS, Federal University of Ceara, CEP 62042–280, Sobral, CE, Brazil.
Mariana A. M. Donato
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife, PE, Brazil.
Christina. A. Peixoto
Affiliation:
Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife, PE, Brazil.
Robert van den Hurk
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, PO Box 80.163, Utrecht, The Netherlands.
José R.V. Silva*
Affiliation:
Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041–040, Sobral, CE, Brazil.
*
All correspondence to: J.R.V. Silva. Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041–040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36118000. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study aims to investigate the effects of jacalin and follicle-stimulating hormone (FSH) on activation and survival of goat primordial follicles, as well as on gene expression in cultured ovarian tissue. Ovarian fragments were cultured for 6 days in minimum essential medium (MEM) supplemented with jacalin (10, 25, 50 or 100 μg/ml – Experiment 1) or in MEM supplemented with jacalin (50 μg/ml), FSH (50 ng/ml) or both (Experiment 2). Non-cultured and cultured tissues were processed for histological and ultrastructural analysis. Cultured tissues from Experiment 2 were also stored to evaluate the expression of BMP-15, KL (Kit ligand), c-kit, GDF-9 and proliferating cell nuclear antigen (PCNA) by real-time polymerase chain reaction (PCR). The results of Experiment 1 showed that, compared with tissue that was cultured in control medium, the presence of 50 μg/ml of jacalin increased both the percentages of developing follicles and viability. In Experiment 2, after 6 days, higher percentages of normal follicles were observed in tissue cultured in presence of FSH, jacalin or both, but no synergistic interaction between FSH and jacalin was observed. These substances had no significant effect on the levels of mRNA for BMP-15 and KL, but FSH increased significantly the levels of mRNA for PCNA and c-kit. On the other hand, jacalin reduced the levels of mRNA for GDF-9. In conclusion, jacalin and FSH are able to improve primordial follicle activation and survival after 6 days of culture. Furthermore, presence of FSH increases the expression of mRNA for PCNA and c-kit, but jacalin resulted in lower GDF-9 mRNA expression.

Keywords

CaprineCultureJacalinmRNAOvarian fragmentsPre-antral follicles
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 537 - 549
Copyright
Copyright © Cambridge University Press 2014 

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, 398–408.CrossRefGoogle ScholarPubMed
Albertini, D.F., Combelles, C.M., Benecchi, E. & Carabatsos, M.J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–53.CrossRefGoogle ScholarPubMed
Andrade, E.R., Seneda, M.M. & Alfieri, A.A. (2005). Interactions of indole acetic acid with EGF and FSH in the culture of ovine preantral follicles. Theriogenology. 64, 1104–13.CrossRefGoogle ScholarPubMed
Barros, V.R.P., Cavalcante, A.Y.P., Macedo, T.J.S., Barberino, R.S., Lins, T.L.B., Gouveia, B.B., Menezes, V.G., Queiroz, M.A.A., Araújo, V.R., Palheta, R.C. Jr, Leite, M.C.P. & Matos, M.H.T. (2013). Immunolocalization of melatonin and follicle-stimulating hormone receptors in caprine ovaries and their effects during in vitro development of isolated pre-antral follicles. Reprod. Dom. Anim. 48, 1025–33.CrossRefGoogle ScholarPubMed
Blackmore, D.G., Baillie, L.R., Holt, J.E., Dierkx, L., Aitken, R.J. & Mclaughlin, E.A. (2004). Biosynthesis of the canine zona pellucida requires the integrated participation of both oocytes and granulosa cells. Biol. Reprod. 71, 661–8.CrossRefGoogle ScholarPubMed
Bristol-Gould, S. & Woodruff, T.K. (2006). Folliculogenesis in the domestic cat (Felis catus). Theriogenology 66, 5–13.CrossRefGoogle ScholarPubMed
Bruno, J.B., Matos, M.H.T., Chaves, R.N., Celestino, J.J.H., Saraiva, M.V.A., Lima-Verde, I.B., Araújo, V.R. & Figueiredo, J.R. (2009). Angiogenic factors and ovarian follicle development. Anim. Reprod. 6, 371–9.Google Scholar
Bunn-Moreno, M.M. & Campos-Neto, A. (1981). Lectin(s) extracted from seeds Artocarpus integrifolia (jackfruit): potent and selective stimulator(s) of distinct human T and B cell functions. J. Immunol. 127, 427–9.CrossRefGoogle Scholar
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.CrossRefGoogle ScholarPubMed
Celestino, J.J.H., Matos, M.H.T., Saraiva, M.V.A. & Figueiredo, J.R. (2009). Regulation of ovarian folliculogenesis by Kit ligand and the c-Kit system in mammals. Anim. Reprod. 6, 431–9.Google Scholar
Cunha, E.V., Costa, J.J.N., Rossi, R.O.D.S., Silva, A.W.B., Passos, J.R.S., Portela, A. M.L.R., Pereira, D.C.S.T., Donato, M.A.M., Campello, C.C., Saraiva, M.V.A., Peixotos, C.A., Silva, J.R.V. & Santos, R.P. (2013). Phytohemagglutinin improves the development and ultrastructure of in vitro-cultured goat (Capra hircus) preantral follicles. Braz. J. Med. Biol. Res. 46, 245–52.CrossRefGoogle ScholarPubMed
Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. & Matzuk, M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–5.CrossRefGoogle ScholarPubMed
Fatehi, A.N., Van den Hurk, R., Colenbrander, B., Daemen, A.J., Van Tol, H.T., Monteiro, R.M., Roelen, B.A. & Bevers, M.M. (2005). Expression of bone morphogenetic protein 2 (BMP-2), 4 (BMP-4) and BMP receptors in the bovine ovary but absence of effects of BMP-2 and BMP-4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872–89.CrossRefGoogle Scholar
Figueiredo, J.R., Rodrigues, A.P.R., Santos, R.R., Lopes, C. & Silva, J.R.V. (2006). Estado atual da biotécnica de manipulação de oócitos inclusos em folículos pré-antrais. Acta Sci. Vet. 34, 71–84.Google Scholar
Frota, I.M.A., Leitão, C.C.F., Costa, J.J.N., van den Hurk, R., Brito, I.R., Saraiva, M.V.A., Figueiredo, J.R. & Silva, J.R.V. (2011). Effects of BMP-7 and FSH on the development of goat preantral follicles and levels of mRNA for FSH-R, BMP-7 and BMP receptors after culture. Anim. Reprod. 8, 25–31.Google Scholar
Fu, L.L., Zhou, C.C., Yao, S., Yu, J.Y., Liu, B. & Bao, J.K. (2011). Plant lectins: targeting programmed cell death pathways as antitumor agents. Int. J. Biochem. Cell. Biol. 43, 1442–9.CrossRefGoogle ScholarPubMed
Hussein, T.S., Froiland, D.A., Amato, F., Thompson, J.G. & Gilchrist, R.B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining amorphogenic paracrine gradient of bone morphogenetic proteins. J. Cell. Sci. 118, 5257–68.CrossRefGoogle Scholar
Hutt, K.J., McLaughlin, E.A. & Holland, M.K. (2006). Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol. Hum. Reprod. 12, 61–9.CrossRefGoogle ScholarPubMed
Jeyaprakash, A.A., Jayashree, G., Mahanta, S.K., Swaminathan, C.P.K., Sekar, A.S. & Vijayan, M. (2005). Structural basis for the energetics of jacalin–sugar interactions: promiscuity versus specificity. J. Mol. Biol. 347, 181–8.CrossRefGoogle Scholar
Jiménez-Movilla, M.J., Aviles, M., Gomez-Torres, M.J., Fernandez-Colom, P.J., Castells, M.T., Juan, J., Romeu, A. & Ballestal, J. (2004). Carbohydrate analysis of the zona pellucid and cortical granules of human oocytes by means of ultrastructural cytochemistry. Hum. Reprod. 19, 1842–55.CrossRefGoogle Scholar
Jin, X., Han, C.S., Yu, F.Q., Wei, P., Hu, Z.Y. & Liu, Y.X. (2005). Anti-apoptotic action of stem cell factor on oocytes in primordial follicles and its signal transduction. Mol. Reprod. Dev. 70, 82–90.CrossRefGoogle ScholarPubMed
Kalich-Philosoph, L., Roness, H., Carmely, A., Fishel-Bartal, M., Ligumsky, H., Paglin, S., Wolf, I., Kanety, H., Sredni, B. & Meirow, D. (2013). Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci. Trans. Med. 5, 185–62.CrossRefGoogle ScholarPubMed
Kim, J.Y. (2012). Control of ovarian primordial follicle activation. Clin. Exp. Reprod. 39, 10–4.CrossRefGoogle ScholarPubMed
Knight, G.P. & Glister, C. (2006). Focus on TGF-β signalling. TGF-β superfamily members and ovarian follicle development. Reproduction 132, 191–206.CrossRefGoogle Scholar
Kristensen, S. G., Andersen, K., Clement, C. A., Franks, S., Hardy, K. & Andersen, C.Y. (2013). Expression of TGF-beta superfamily growth factors, their receptors, the associated SMADs and antagonists in five isolated size-matched populations of pre-antral follicles from normal human ovaries. Mol. Hum. Reprod. doi:10.1093/molehr/gat089.CrossRefGoogle Scholar
Li, W.W., Yu, J.Y., Xu, H.L. & Bao, J.K. (2011). Concanavalin A: a potential antineoplastic agent targeting apoptosis, autophagy and anti-angiogenesis for cancer therapeutics. Biochem. Biophys. Res. Commun. 414, 282–6.CrossRefGoogle ScholarPubMed
Lima, I.M.T., Celestino, J.H., Figueiredo, J.R. & Rodrigues, A.P.R. (2010). Role of bone morphogenetic protein 15 (BMP-15) and Kit ligand (KL) in the regulation of folliculogenesis in mammalian. Rev. Bras. Reprod. Anim. 34, 3–20.Google Scholar
Lima, I.M.T., Brito, I.R., Rodrigues, G.Q., Silva, C.M.G., Magalhães-Padilha, D., Lima, L.F., Celestino, J.J.H., Faustino, L.R., Campello, C.C., Silva, J.R.V., Figueiredo, J.R. & Rodrigues, A.P.R. (2011). Presence of c-kit mRNA in goat ovaries and improvement of in vitro preantral follicle survival and development with kit ligand. Mol. Cell. Endocrinol. 345, 38–47.CrossRefGoogle ScholarPubMed
Lima, L.F., Rocha, R.M.P., Alves, A.M.V.A., Saraiva, M.V.A., Araújo, V.R., Lima, I.M.T., Lopes, C.A.P., Báo, S.N., Campello, C.C., Rodrigues, A.P.R. & Figueiredo, J.R. (2013). Dynamized follicle-stimulating hormone affects the development of ovine preantral follicles cultured in vitro. Homeopathy. 102, 41–8.CrossRefGoogle ScholarPubMed
Lis, H. & Sharon, N. (1986). Biological properties of lectins. In The Lectins: Properties, Functions and Applications in Biology and Medicine pp. 265–85. London: Academic Press.CrossRefGoogle Scholar
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Maga, G. & Hubscher, U. (2003). Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell. Sci. 116, 3051–60.CrossRefGoogle ScholarPubMed
Magalhães, D.M., Araújo, V.R. & Verde, I.B.L. (2009). Different follicle stimulating hormone (FSH) sources influence caprine preantral follicle viability and development in vitro. Pesq. Vet. Bras. 46, 378–86.Google Scholar
Magalhães-Padilha, D.M., Fonseca, G.R., Haag, K.T., Wischral, A., Gastal, M.O., Jones, K.L., Geisler-Lee, J., Figueiredo, J.R. & Gastal, E.L. (2012). Long-term in vitro culture of ovarian cortical tissue in goats: effects of FSH and IGF-I on preantral follicular development and FSH and IGF-I receptor mRNA expression. Cell Tissue Res. 350, 503–11.CrossRefGoogle ScholarPubMed
Mao, J., Wu, G., Smith, M.F., McCauley, T.C., Cantley, T.C., Prather, R.S., Didion, B.A. & Day, B.N. (2002). Effects of culture medium, serum type, and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biol. Reprod. 67, 1197–203.CrossRefGoogle ScholarPubMed
Markholt, S., Grøndahl, M.L., Ernst, E.H., Andersen, C.Y., Ernst, E. & Lykke-Hartmann, K. (2012). Global gene analysis of oocytes from early stages in human folliculogenesis shows high expression of novel genes in reproduction. Mol. Hum. Reprod. 18, 96–110.CrossRefGoogle ScholarPubMed
Matos, M.H.T., Lima-Verde, I.B., Luque, M.C.A., Maia-Jr, J.E., Silva, J.R.V., Celestino, J.J.H., Martins, F.S., Báo, S.N., Lucci, C.M. & Figueiredo, J.R. (2007a). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173–82.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. & Figueiredo, J.R. (2007d). Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles. Cells Tissues Organs 18, 112–20.CrossRefGoogle Scholar
McGee, E., Spears, N., Minami, S., Hsu, S.Y., Chun, S.Y., Billig, H. & Hsueh, A.J.W. (1997). Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′-5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 138, 2417–24.CrossRefGoogle ScholarPubMed
McMahon, H.E., Hashimoto, O., Mellon, P.L. & Shimasaki, S. (2008). Oocyte-specific overexpression of mouse bone morphogenetic protein-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice. Endocrinology 149, 2807–15.CrossRefGoogle Scholar
McNatty, K.P., Juengel, J.L., Reader, K.L., Lun, S., Myllymaa, S., Lawrence, S.B., Western, A., Meerasahib, M.F., Mottershead, D.G. & Groome, N. (2005a). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129, 473–80.CrossRefGoogle ScholarPubMed
Misquith, S.P., Rani, , & G. Surolia, A. (1994). Carbohydrate binding specificity of the B-cell maturation mitogen from Artocarpus integrifolia seeds. J. Biol. Chem. 269, 30393–401.CrossRefGoogle ScholarPubMed
Muskhelishvili, L., Wingard, S.K. & Latendresse, J.R. (2005). Proliferating cell nuclear antigen a marker for ovarian follicle counts. Toxicol. Pathol. 33, 365–8.CrossRefGoogle ScholarPubMed
Myllymaa, S., Pasternack, A., Mottershead, D.G., Poutanen, M., Pulkki, M.M., Pelliniemi, L.J., Ritvos, O. & Laitinen, M.P.E. (2010). Inhibition of oocyte growth factors in vivo modulates ovarian folliculogenesis in neonatal and immature mice. Reproduction 139, 587–98.CrossRefGoogle ScholarPubMed
Oktay, K., Schenken, R.S. & Nelson, J.F. (1995). Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol. Reprod. 53, 295–301.CrossRefGoogle ScholarPubMed
Orisaka, M., Tajima, K., Tsang, B.K. & Kotsuji, F. (2009). Oocyte–granulosa–theca cell interactions during preantral follicular development. J. Ovar. Res. 2, 1–7.Google ScholarPubMed
Otsuka, F., McTavish, K. & Shimasaki, S. (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Reprod. Dev. 78, 9–21.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 40, 262–71.Google Scholar
Peng, X., Yang, M., Wang, L., Tong, C. & Guo, Z. (2010). In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium. J. Assist. Reprod. Genet. 27, 247–57.CrossRefGoogle Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 2002–7.CrossRefGoogle ScholarPubMed
Roque-Barreira, M.C. & Campos-Neto, A. (1985). Jacalin: an IgA-binding lectin. J. Immunol. 134, 1740–3.CrossRefGoogle ScholarPubMed
Saraiva, M.V.A, Celestino, J.J.H. & Chaves, R.N. (2008). Influence of different concentrations of LH and FSH on in vitro caprine primordial ovarian follicle development. Small Rum. Res. 78, 87–95.CrossRefGoogle Scholar
Saraiva, M.V., Celestino, J.J., Araújo, V.R., Chaves, R.N., Almeida, A.P., Lima-Verde, I.B., Duarte, A.B., Silva, G.M., Martins, F.S., Bruno, J.B., Matos, M.H., Campello, C.C., Silva, J.R. & Figueiredo, J.R. (2011). Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles. Zygote 19, 205–14.CrossRefGoogle ScholarPubMed
Saxon, A., Tsui, F. & Martinez-Maza, O. (1987). Jacalin, an IgA-binding lectin, inhibits differentiation of human B cells by both a direct effect and by activating T-supressor cells. Cell. Immunol. 104, 134–41.CrossRefGoogle Scholar
Sell, A.M. & Costa, C.P. (2002). Efeito inflamatório local induzido pelas lectinas PHA, WGA e jacalina. Arq. Ciênc. Saúde Unipar 6, 47–51.Google Scholar
Sharma, V. & Surolia, A. (1997). Analyses of carbohydrate recognition by legume lectins: size of the combining site loops and their primary specificity. J. Mol. Biol. 267, 433–45.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Báo, S.N., Lucci, C.M., Carvalho, F.C.A., Andrade, E.R., Ferreira, M.A.L. & Figueiredo, J.R. (2001) Morphological and ultrastructural changes occurring during degeneration of goat preantral follicles preserved in vitro. Anim. Reprod. Sci. 66, 209–23.CrossRefGoogle ScholarPubMed
Silva, J.R.V., Van den Hurk, R., Matos, M.H.T., Santos, R.R., Pessoa, C., Moraes, M.O. & Figueiredo, J.R. (2004). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–704.CrossRefGoogle ScholarPubMed
Songsasen, N., Fickes, A., Pukazhenthi, B.S. & Wildt, D.E. (2009). Follicular morphology, oocyte diameter and localization of fibroblast growth factors in the domestic dog ovary. Reprod. Domest. Anim. 44, 65–70.CrossRefGoogle ScholarPubMed
Stulnig, T., Schuweiger, M. & Hirsch-Kauffmann, M. (1993). Duchenne muscular dystrophy: lack of differences in the expression of endogenous carbohydrate- and heparin-binding proteins (lectins) in culture fibroblast. Eur. J. Cell Biol. 62, 173–81.Google Scholar
Tse, A.C-K. & Ge, W. (2010). Spatial localization of EGF family ligands and receptors in the zebrafish ovarian follicle and their expression profiles during folliculogenesis. Gen. Comp. Endoc. 167, 397–407.CrossRefGoogle ScholarPubMed
van den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Velasquez, E.V., Ríos, M., Ortiz, M.E., Lizama, C., Nuñez, E., Abramovich, D., Orge, F., Oliva, B., Orellana, R., Villalon, M., Moreno, R.D., Tesone, M., Rokka, A., Corthals, G., Croxatto, H.B., Parborell, F. & Owen, G.I. (2013). Concanavalin-A induces granulosa cell death and inhibits FSH-mediated follicular growth and ovarian maturation in female rats. Endocrinology 154, 1885–96.CrossRefGoogle ScholarPubMed
Wandji, S.A., Srsen, V., Voss, A.K., Eppig, J.J. & Fortune, J.E. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol Reprod. 55, 942–8.CrossRefGoogle ScholarPubMed
Wang, C. & Roy, S.K. (2006). Expression of growth differentiation factor 9 in the oocytes is essential for the development of primordial follicles in the hamster ovary. Endocrinology 147, 1725–34.CrossRefGoogle ScholarPubMed
Yagi, M., Campos-Neto, A. & Gollahon, K. (1995). Morphological and biochemical changes in a hematopoietic cell line induced by jacalin, a lectin derived from Artocarpus integrifolia. Biochem. Biophysical Res. Comm. 209, 263–70.CrossRefGoogle Scholar
Young, N.M., Johnston, R.A.Z. & Watson, D.C. (1991). The amino acid sequences of jacalin and the Madura pomira agglutinin. Fed. Eur. Biochem. Soc. 282, 382–4.CrossRefGoogle Scholar