Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-04T20:22:51.391Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of nerve growth factor (NGF) and its receptors in folliculogenesis

Published online by Cambridge University Press:  01 June 2012

R.N. Chaves ,
A.M.C.V. Alves ,
L.F. Lima ,
H.M.T. Matos ,
A.P.R. Rodrigues  and
J.R. Figueiredo
R.N. Chaves*
Affiliation:
Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Paranjana, 1700, Campus do Itaperi, Fortaleza–CE–Brasil. CEP: 60740–903, Brazil.
A.M.C.V. Alves
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Av. Paranjana 1700, Campus Itaperi, Fortaleza, 60740–903, CE, Brazil.
L.F. Lima
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Av. Paranjana 1700, Campus Itaperi, Fortaleza, 60740–903, CE, Brazil.
H.M.T. Matos
Affiliation:
Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, 48902–300, PE, Brazil.
A.P.R. Rodrigues
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Av. Paranjana 1700, Campus Itaperi, Fortaleza, 60740–903, CE, Brazil.
J.R. Figueiredo
Affiliation:
Laboratory of Manipulation of Oocytes and Preantral Follicles, Faculty of Veterinary, State University of Ceará, Av. Paranjana 1700, Campus Itaperi, Fortaleza, 60740–903, CE, Brazil.
*
All correspondence to: Roberta Nogueira Chaves. Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Laboratório de Manipulação de Oócitos e Folículos Pré-Antrais (LAMOFOPA), Universidade Estadual do Ceará (UECE), Av. Paranjana, 1700, Campus do Itaperi, Fortaleza–CE–Brasil. CEP: 60740–903, Brazil. Tel: +55 85 3101 9852. Fax: +55 85 3101 9840. e-mail address: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Nerve growth factor (NGF) is a prototype member of the neurotrophins family and has important functions in the maintenance of viability and proliferation of neuronal and non-neuronal cells, such as certain ovarian cells. The present review highlights the role of NGF and its receptors on ovarian follicle development. NGF initiates its multiple actions through binding to two classes of receptors: the high affinity receptor tyrosine kinase A (TrkA) and the low-affinity receptor p75. Different intracytoplasmic signalling pathways may be activated through binding to NGF due to variation in the receptors. The TrkA receptor activates predominantly phosphatidylinositol-3-kinase (PI3K) and mitogenic activated protein kinase (MAPK) to promote cell survival and proliferation. The activation of the phospholipase type Cγ (PLCγ) pathway, which results in the production of diacylglycerol (DAG) and inositol triphosphate (IP3), culminates in the release of calcium from the intracytoplasmic cellular stocks. However, the details of activation through p75 receptor are less well known. Expression of NGF and its receptors is localized in ovarian cells (oocyte, granulosa, theca and interstitial cells) from several species, which suggests that NGF and its receptors may regulate some ovarian functions such as follicular survival or development. Thus, the use of NGF in culture medium for ovarian follicles may be of critical importance for researchers who want to promote follicular development in vitro in the future.

Keywords

p75FolliclesNGFOvaryTrkA
Type
Research Article
Information
Zygote , Volume 21 , Issue 2 , May 2013 , pp. 187 - 197
Copyright
Copyright © Cambridge University Press 2012

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

Adhikari, D. & Liu, K. (2009). Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr. Rev. 30, 438–64.CrossRefGoogle ScholarPubMed
Agrawal, L.R., Sladkevicius, P., Engmann, L., Conway, G.S., Payne, N.N., Bekis, J., Tan, S.L., Campbell, S. & Jacobs, H.S. (1998). Serum vascular endothelial growth factor concentrations and ovarian stromal blood flow are increased in women with polycystic ovaries. Hum. Reprod. 13, 651–5.CrossRefGoogle ScholarPubMed
Airaksinen, M.S. & Saarma, M. (2002).The GDNF family: signalling, biological functions and therapeutic value. Nat. Ver. Neurosci. 3, 383–94.CrossRefGoogle ScholarPubMed
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. & Walter, P. (2004). Sinalização por meio de receptores de superfície celular associados a enzimas. Biologia molecular da célula, 4. ed. Porto Alegre, Br: Editora Artes Médicas. pp. 871–92.Google Scholar
Albert, C., Garrido, N., Mercader, A., Rao, C.V., Remohí, J., Simon, C. & Pellicer, A. (2002). The role of endothelial cells in the pathogenesis of ovarian hyperstimulation syndrome. Mol. Hum. Reprod. 8, 409–18.CrossRefGoogle ScholarPubMed
Aloe, L. (2004). Rita Levi-Montalcini: the discovery of nerve growth factor and modern neurobiology. Trends Cell. Biol. 14, 395–9.CrossRefGoogle Scholar
Angeletti, R.H. & Bradshaw, R.A. (1971). Nerve growth factor from mouse submaxillary gland: amino acid sequence. Proc. Natl. Acad. Sci. USA 68, 2417–20.CrossRefGoogle ScholarPubMed
Barboni, B., Mattioli, M., Giogia, L., Turriani, M., Capacchietti, G., Berardinelli, P. & Bernabo, N. (2002). Preovulatory rise of NGF in follicular fluid: possible involvement in the control of oocyte maturation. Microsc. Res. Tech. 59, 516–21.CrossRefGoogle ScholarPubMed
Barker, P.A. (2004). p75NTR is positively promiscuous: novel partners and new insights. Neuron 42, 529–533.CrossRefGoogle ScholarPubMed
Bhakar, A.L., Howell, J.L., Paul, C.E., Salehi, A.H., Becker, E.B., Said, F., Bonni, A. & Barker, P.A. (2003). Apoptosis induced by p75NTR overexpression requires Jun kinase-dependent phosphorylation of Bad. J. Neurosci. 23, 11373–81.CrossRefGoogle ScholarPubMed
Barrett, G.L. (2000). The p75 neurotrophin receptor and neuronal apoptosis. Prog. Neurobiol. 61, 205–29.CrossRefGoogle ScholarPubMed
Baud, V. & Karin, M. (2009). Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 8, 33–40.CrossRefGoogle ScholarPubMed
Bendell, J.J. & Dorrington, J. (1988). Rat thecal/interstitial cells secrete a transforming growth factor-beta-like factor that promotes growth and differentiation in rat granulosa cells. Endocrinology 123, 941–8.CrossRefGoogle ScholarPubMed
Bjorling, D.E., Beckman, M., Clayton, M.K. & Wang, Z.Y. (2002). Modulation of nerve growth factor in peripheral organs by estrogen and progesterone. Neuroscience 110, 155–67.CrossRefGoogle ScholarPubMed
Botchkarev, V.A., Botchkareva, N.V., Albers, K.M., Chen, L.H., Welker, P. & Source, P.R. (2000). A role for p75 neurotrophin receptor in the control of apoptosis-driven hair follicle regression. FASEB J. 14, 1931–42.CrossRefGoogle ScholarPubMed
Brunet, A., Datta, S.R. & Greenberg, M.E. (2001). Transcription-dependent and independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297–305.CrossRefGoogle ScholarPubMed
Bruno, J.B., Celestino, J.J.H., Lima-Verde, I.B., Lima, L.F., Matos, M.H.T., Araújo, V.R., Saraiva, M.V.A., Martins, F.S., Name, K.P.O., Campello, C.C., Báo, S.N., Silva, J.R.V. & Figueiredo, J.R. (2009). Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod. Fert. Dev. 21, 679–87.CrossRefGoogle ScholarPubMed
Calza, L., Giardino, L., Giuliani, A., Aloe, L. & Levi-Montalcini, R. (2001). Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc. Natl. Acad. Sci. USA 98, 4160–5.CrossRefGoogle ScholarPubMed
Caporali, A. & Emanueli, C. (2009). Cardiovascular actions of neurotrophins. Physiol. Rev. 89, 279–308.CrossRefGoogle ScholarPubMed
Chao, V.M. (2003). Neurotrophins and their receptors: a convergence point for many signaling pathways. Nature Rev. 4, 299–309.CrossRefGoogle Scholar
Chaves, R.N., Alves, A.M., Duarte, A.B., Araújo, V.R., Celestino, J.J., Matos, M.H., Lopes, C.A., Campello, C.C., Name, K.P., Báo, S.N. & Figueiredo, J.R. (2010). Nerve growth factor promotes the survival of goat preantral follicles cultured in vitro. Cells Tissues Organs 192, 272–82.CrossRefGoogle ScholarPubMed
Chiaretti, A., Piastra, M., Caresta, E., Nanni, L. & Aloe, L. (2002). Improving ischaemic skin revascularisation by nerve growth factor in a child with crush syndrome. Arch. Dis. Child. 87, 446–8.CrossRefGoogle Scholar
Chung, J., Grammer, T., Lemon, K., Kazlauskas, A. & Blenis, J. (1994). PDGF- and insulin-dependent pp70S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370, 71–5.CrossRefGoogle ScholarPubMed
Corbit, K.C., Foster, D.A. & Rosner, M.R. (1999). Protein kinase C delta mediates neurogenic but not mitogenic activation of mitogen-activated protein kinase in neuronal cells. Mol. Cell. Biol. 19, 4209–8.CrossRefGoogle Scholar
Cordon-Cardo, C., Tapley, P., Jing, S., Nanduri, V., O'Rourke, E., Lamballe, F., Kovary, K., Jones, K., Reichardt, L.F. & Barbacid, M. (1991). The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neuro- trophin-3. Cell 66, 173–83.CrossRefGoogle Scholar
Covaceuszach, S., Cassetta, A., Cattaneo, A. & Lamba, D. (2004). Purification, crystallization, X-ray diffraction analysis and phasing of a Fab fragment of monoclonal neuroantibody alphaD11 against nerve growth factor. Acta Crystallogr. D. Biol. Crystallogr. 60, 1323–7.CrossRefGoogle ScholarPubMed
Crews, C., Alessandrini, A. & Erikson, E. (1992). The primary structure of MEK, a protein kinase that phosphorylates the ERK gene product. Science 258, 478–80.CrossRefGoogle Scholar
Dissen, G.A., Garcia-Rudaz, C., Paredes, A., Mayer, C., Mayerhofer, A. & Ojeda, S.R. (2009). Excessive ovarian production of nerve growth factor facilitates development of cystic ovarian morphology in mice and is a feature of polycystic ovarian syndrome in humans. Endocrinology 150, 2906–14.CrossRefGoogle ScholarPubMed
Dissen, G.A., Hill, D.F., Costa, M.E., Ma, Y.J. & Ojeda, S.R. (1991). Nerve growth factor receptors in the peripubertal rat ovary. Mol. Endocrinol. 5, 1642–50.CrossRefGoogle ScholarPubMed
Dees, W.L., Hiney, J.K., Schultea, T.D., Meyerhofer, A., Danilchik, M., Dissen, G.A. & Ojeda, S.R. (1995). The primate ovary contains a population of catecholaminergic neuron-like cells expression nerve growth factor receptors. Endocrinology 136, 5760–8.CrossRefGoogle ScholarPubMed
Dissen, G.A., Hirshfield, A.N., Malamed, S. & Ojeda, S.R. (1995). Expression of neurotrophins and their receptors in the mammalian ovary is developmentally regulated: changes at the time of folliculogenesis. Endocrinology 136, 4681–92.CrossRefGoogle ScholarPubMed
Dissen, G.A., Parrott, J.A., Skinner, M.K., Hill, D.F., Costa, M.E. & Ojeda, S.R. (2000). Direct effects of nerve growth factor on thecal cells from antral ovarian follicles. Endocrinology 141, 4736–50.CrossRefGoogle ScholarPubMed
Dissen, G.A., Romero, C., Hirshfiel, A.N. & Ojeda, S.R. (1996). A role for TrkA nerve growth factor receptors in mammalian ovulation. Endocrinology 137, 198–209.CrossRefGoogle ScholarPubMed
Dissen, G.A., Romero, C., Hirshfield, A.N. & Ojeda, S.R. (2001). Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142, 2078–86.CrossRefGoogle ScholarPubMed
Dissen, G.A., Romero, C., Paredes, A. & Ojeda, S.R. (2002). Neurotrophic control of ovarian development. Microsc. Res. Tech. 59, 509–15.CrossRefGoogle ScholarPubMed
Dodson, W.C. & Schomberg, D.W. (1987). The effect of transforming growth factor-beta on follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells. Endocrinology 120, 512–6.CrossRefGoogle ScholarPubMed
Fahnestock, M., Yu, G. & Coughlin, M.D. (2004). ProNGF: a neurotrophic or an apoptotic molecule? Prog. Brain Res. 146, 101–10.CrossRefGoogle ScholarPubMed
Garcia-Rudaz, C., Dorfman, M., Nagalla, S., Svechnikov, K., Söder, O., Ojeda, S.R. & Dissen, G.A. (2011). Excessive ovarian production of nerve growth factor elicits granulosa cell apoptosis by setting in motion a tumor necrosis factor α/stathmin-mediated death signaling pathway. Reproduction 142, 319–31.CrossRefGoogle Scholar
Emanueli, C., Salis, M.B., Pinna, A., Graiani, G., Manni, L. & Madeddu, P. (2002). Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hind limbs. Circulation 106, 2257–62.CrossRefGoogle Scholar
Garcıa-Suarez, O., Germana, A., Hannestad, J., Ciriaco, E., Laura, R., Naves, J., Esteban, I., Silos-Santiago, I. & Veja, J.A. (2000). TrkA is necessary for the normal development of the murine thymus. J. Neuroimmunol. 108, 11–21.CrossRefGoogle ScholarPubMed
Gitay-Goren, H., Kim, I.C., Miggans, S.T. & Schomberg, D.W. (1993). Transforming growth factor beta modulates gonadotropin receptor expression in porcine and rat granulosa cells differently. Biol. Reprod. 48, 1284–9.CrossRefGoogle ScholarPubMed
Glebova, N.O. & Ginty, D.D. (2005). Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 28, 191–222.CrossRefGoogle ScholarPubMed
GrandPré, T., Li, S. & Strittmatter, S.M. (2002). Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417, 547–51.CrossRefGoogle ScholarPubMed
Greco, A., Villa, R. & Pierotti, M.A. (1996). Genomic organization of the human NTRK1 gene. Oncogene 13, 2463–6.Google ScholarPubMed
Haase, G., Pettmann, B., Raoul, C. & Henderson, C.E. (2008). Signaling by death receptors in the nervous system. Curr. Opin. Neurobiol. 18, 284–91.CrossRefGoogle ScholarPubMed
Halböök, F., Lundin, L.G. & Kullander, K. (1998). Lampetra fluviatilis neurotrophin homolog, descendant of a neurotrophin ancestor, discloses the early molecular evolution of neurotrophins in the vertebrate subphylum. J. Neurosci. 18, 8700–11.CrossRefGoogle Scholar
He, X.E. & Garcia, K.C. (2004). Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304, 870–5.CrossRefGoogle ScholarPubMed
Hirshfield, A.N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.CrossRefGoogle ScholarPubMed
Holgado-Madruga, M., Moscatello, D.K., Emlet, D.R., Dieterich, R. & Wong, A.J. (1997). Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc. Natl. Acad. Sci. USA 94, 12419–124.CrossRefGoogle ScholarPubMed
Ibañez, C.F. (1998). Emerging themes in structural biology of neurotrophic factors. Trends Neurosci. 21, 438–44.CrossRefGoogle ScholarPubMed
Julio-Pieper, M., Lozada, P., Tapia, V., Veja, M., Miranda, C., Vantman, D., Ojeda, S.R. & Romero, C. (2009). Nerve growth factor induces vascular endothelial growth factor expression in granulosa cells via a TrkA receptor/mitogen-activated protein kinase-extracellularly regulated kinase 2-dependent pathway. J. Clin. Endocrinol. Metab. 94, 3065–71.CrossRefGoogle Scholar
Kaplan, D.R., Hempstead, B.L., Martin-Zanca, D., Chao, M.V. & Parada, L.F. (1991). The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252, 554–8.CrossRefGoogle ScholarPubMed
Kaplan, D.R. & Miller, F.D. (2000). Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381–91.CrossRefGoogle ScholarPubMed
Karin, M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature 441, 431–6.CrossRefGoogle ScholarPubMed
Kim, S.J., Park, K., Rudkin, B.B., Dey, B.R., Sporn, M.B. & Roberts, A.B. (1994). Nerve growth factor induces transcription of transforming growth factor-beta 1 through a specific promoter element in PC12 cells. J. Biol. Chem. 269, 3739–44.CrossRefGoogle ScholarPubMed
Kohn, J., Aloyz, R.S., Toma, J.G., Haak-Frendscho, M. & Miller, F.D. (1999). Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation. J. Neurosci. 19, 5393–408.CrossRefGoogle ScholarPubMed
Krizsan-Agbas, D., Pedchenko, T., Hasan, W. & Smith, P.G. (2003). Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur. J. Neurosci. 18, 2760–8.CrossRefGoogle ScholarPubMed
Lara, H.E., McDonald, J.K. & Ojeda, S.R. (1990). Involvement of nerve growth factor in female sexual development. Endocrinology. 126, 364–75.CrossRefGoogle ScholarPubMed
Lee, K.F., Li, E., Huber, L.J., Landis, S.C., Sharpe, A.H., Chao, M.V. & Jaenisch, R. (1992). Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737–49.CrossRefGoogle ScholarPubMed
Lee, R., Kermani, P., Teng, K.K. & Hempstead, B.L. (2001). Regulation of cell survival by secreted proneurotrophins. Science. 294, 1945–8.CrossRefGoogle ScholarPubMed
Lenz, G. (2000). Mecanismos de Transdução de Sinal Ativados por Purinas, Pirimidinas e Fatores de Crescimento em Culturas de Astrócitos. [in Portuguese]. Porto Alegre, Brazil: Federal University of Rio Grande do Sul. Thesis.Google Scholar
Levanti, M.B., Germanà, A., Abbate, F., Montalbano, G., Veja, J.A. & Germanà, G. (2005). TrkA and p75 NTR in the ovary of adult cow and pig. J. Anat. 207, 93–6.CrossRefGoogle Scholar
Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science. 237, 1154–1162.CrossRefGoogle ScholarPubMed
Levi-Montalcini, R. & Calissano, P. (1986). Nerve growth factor as a paradigm for other polypeptide growth factors. Trends Neurosci. 9, 473–7.CrossRefGoogle Scholar
Lopez-Ilasaca, M., Crespo, P., Pellici, P.G., Gutkind, J.S. & Wetzker, R. (1997). Linkage of G Protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase. Science 275, 394–7.CrossRefGoogle Scholar
Ludwig, M., Jelkmann, W., Bauer, O. & Diedrich, K. (1999). Prediction of severe ovarian hyperstimulation syndrome by free serum vascular endothelial growth factor concentration on the day of human chorionic gonadotrophin administration. Hum. Reprod. 14, 2437–41.CrossRefGoogle ScholarPubMed
Marte, B.M. & Downward, J. (1997). PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem. Sci. 22, 355–8.CrossRefGoogle ScholarPubMed
Matos, M.H., Lima-Verde, I.B., Bruno, J.B., Lopes, C.A., Martins, F.S., Santos, K.D., Rocha, R.M., Silva, J.R., Báo, S.N. & Figueiredo, J.R. (2007). Follicle stimulating hormone and fibroblast growth factor-2 interact and promote goat primordial follicle development in vitro. Reprod. Fertil. Dev. 19, 677–84.CrossRefGoogle ScholarPubMed
Mayerhofer, A., Dissen, G.A., Costa, M.E. & Ojeda, S.R. (1997). A role for neurotransmitters in early follicular development: Induction of functional follicle-stimulating hormone receptors in newly formed follicles of the rat ovary. Endocrinology 138, 3320–9.CrossRefGoogle ScholarPubMed
McDonald, N.Q., Lapatto, R., Murray-Rust, J., Gunning, J., Wlodawer, A. & Blundell, T.L. (1991). New protein fold revealed by a 2.3-Å resolution crystal structure of nerve growth factor. Nature 354, 411–4.CrossRefGoogle Scholar
Molloy, N.H., Read, D.E. & Gorman, A.M. (2011). Nerve growth factor in cancer cell death and survival. Cancers 3, 510–530.CrossRefGoogle ScholarPubMed
Mouri, A., Nomoto, H. & Furukawa, S. (2007). Processing of nerve growth factor: the role of basic amino acid clusters in the pro-region. Biochem. Biophys. Res. Commun. 353, 1056–62.CrossRefGoogle ScholarPubMed
Nilsson, E., Dole, G. & Skinner, M.K. (2009). Neurotrophin NT3 promotes ovarian primordial to primary follicle transition. Reproduction 138, 697–707.CrossRefGoogle ScholarPubMed
Nimnual, A.S., Yatsula, B.A. & Bar-Sagi, D. (1998). Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279, 560–3.CrossRefGoogle ScholarPubMed
Nomoto, H., Takaiwa, M., Mouri, A. & Furukawa, S. (2007). Pro-region of neurotrophins determines the processing efficiency. Biochem. Biophys. Res. Commun. 356, 919–24.CrossRefGoogle ScholarPubMed
Nykjaer, A., Lee, R., Teng, K.K., Jansen, P., Madsen, P., Nielsen, M.S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T.E., Hempstead, B.L. & Petersen, C.M. (2004). Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843–8.CrossRefGoogle ScholarPubMed
Ojeda, S.R. & Dissen, G.A. (1994). Developmental regulation of the ovary via growth factor tyrosine kinase receptors. Trends Endocrinol. Metab. 5, 317–23.CrossRefGoogle ScholarPubMed
Ojeda, S.R., Romero, C., Tapia, V. & Dissen, G.A. (2000). Neurotrophic and cell–cell dependent control of early follicular development. Mol. Cell. Endocrinol. 163, 67–71.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
Paredes, A., Romero, C., Dissen, G.A., DeChiara, T.M., Reichardt, L., Cornea, A., Ojeda, S.R. & Xu, B. (2004). TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. Dev. Biol. 267, 430–49.CrossRefGoogle ScholarPubMed
Rabin, S., Cleghorn, V. & Kaplan, D. (1993). SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol. 13, 2203–13.Google ScholarPubMed
Redmer, D.A., Doraiswamy, V., Bortnem, B.J., Fisher, K., Jablonka-Shariff, A., Grazul-Bilska, A.T. & Reynolds, L.P. (2001). Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol. Reprod. 65, 879–89.CrossRefGoogle ScholarPubMed
Ren, L.Q., Medan, M.S., Weng, Q., Jin, W., Li, C.M., Watanabe, G. & Taya, K. (2005). Immunolocalization of nerve growth factor (NGF) and its receptors (TrkA and p75LNGFR) in the reproductive organs of Shiba goats. J. Reprod. Dev. 51, 399–404.CrossRefGoogle ScholarPubMed
Robinson, K.N., Manto, K., Buchsbaum, R.J., MacDonald, J.I. & Meakin, S.O. (2005). Neurotrophin-dependent tyrosine phosphorylation of Ras guanine-releasing factor 1 and associated neurite outgrowth is dependent on the HIKE domain of TrkA. J. Biol. Chem. 280, 225–35.CrossRefGoogle ScholarPubMed
Rodriguez-Viciana, P., Warne, P.H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M.J., Waterfield, M.D. & Downward, J. (1994). Phosphatidylinositol-3-OH kinase as a direct target of Ras, Nature 370, 527–32.CrossRefGoogle ScholarPubMed
Romero, C.A., Paredes, A., Dissen, G.A. & Ojeda, S.R. (2002). Nerve growth factor induces the expression of functional FSH receptors in newly formed follicles of the rat ovary. Endocrinology 143, 1485–94.CrossRefGoogle ScholarPubMed
Roux, P.P. & Barker, P.A. (2002). Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203–33.CrossRefGoogle ScholarPubMed
Salas, C.M., Julio-Pieper, M., Valladares, M., Pommer, R., Veja, M., Mastronardi, C., Kerr, B., Ojeda, S.R., Lara, H.E. & Romero, C. (2006). Nerve growth factor-dependent activation of TrkA receptors in the human ovary results in synthesis of FSH receptors and estrogen secretion. J. Clin. Endocrinol. Metab. 91, 2396–403.CrossRefGoogle ScholarPubMed
Seo, K., Choi, J., Park, M. & Rhee, C. (2001).Angiogenesis effects of nerve growth factor (NGF) on rat corneas. J. Vet. Sci. 2, 125–30.CrossRefGoogle ScholarPubMed
Shi, Z., Jin, W., Watanabe, G., Suzuki, A.K., Takahashi, S. & Taya, K. (2004). Expression of nerve growth factor (NGF) and its receptors TrkA and p75 in ovaries of the cyclic golden hamster (Mesocricetus auratus) and the regulation of their production by luteinizing hormone. J. Reprod. Dev. 50, 605–11.CrossRefGoogle ScholarPubMed
Silva, B.V., Horta, B.A.C., Alencastro, R.B. & Pinto, A.C. (2009). Proteínas quinases: características estruturais e inibidores químicos. Quim. Nova. 32, 453–62.CrossRefGoogle Scholar
Simi, A. & Ibañez, C.F. (2010). Assembly and activation of neurotrophic factor receptor complexes. Dev. Neurobiol. 70, 323–31.CrossRefGoogle ScholarPubMed
Skinner, M.K., Lobb, D. & Dorrington, J.H. (1987). Ovarian thecal/interstitial cells produce an epidermal growth factor-like substance. Endocrinology 121, 1892–9.CrossRefGoogle ScholarPubMed
Snider, W.D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627–38.CrossRefGoogle ScholarPubMed
Sofroniew, M.V., Howe, C.L. & Mobley, W.C. (2001). Nerve Growth Factor signalling, neuroprotection, and neural repair. Ann. Rew. Neurosci. 24, 1217–81.CrossRefGoogle ScholarPubMed
Sortino, M.A., Condorelli, F., Vancheri, C., Chiarenza, A., Bernardini, R., Consoli, U. & Canonico, P.L. (2000). Mitogenic effect of nerve growth factor (NGF) in LNCaP prostate adenocarcinoma cells: role of the high- and low-affinity NGF receptors. Mol. Endocrinol. 14, 124–36.CrossRefGoogle ScholarPubMed
Spears, N., Molinek, M.D., Robinson, L.L., Fulton, N., Cameron, H., Shimoda, K., Telfer, E.E., Anderson, R.A. & Price, D.J. (2003). The role of neurotrophin receptors in female germ-cell survival in muse and human. Development 130, 5481–91.CrossRefGoogle Scholar
Terenghi, G. (1999). Peripheral nerve regeneration and neurotrophic factors. J. Anat. 194, 1–14.CrossRefGoogle ScholarPubMed
Tessarollo, L. (1998). Pleiotropic functions of neurotrophins in development. Cytokine Growth Factor Rev. 9, 125–37.CrossRefGoogle ScholarPubMed
Valent, A. & Bernheim, A. (1997). Mapping of the tyrosine kinase receptors TRKA (NTRK1), TRKB (NTRK2) and TRKC (NTRK3) to human chromosomes 1q22, 9q22 and 15q25 by fluorescence in situ hybridization. Eur. J. Human Genet. 5, 102–4.CrossRefGoogle ScholarPubMed
Vilar, M., Charalampopoulos, I., Kenchappa, R.S., Simi, A., Karaca, E., Reversi, A., Choi, S., Bothwell, M., Mingarro, I., Friedman, W.J., Schiavo, G., Bastiaens, P.I., Verveer, P.J., Carter, B.D. & Ibanez, C.F. (2009). Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron. 62, 72–83.CrossRefGoogle ScholarPubMed
Weng, Q., Shi, Z.Q., Tukada, J., Watanabe, G. & Taya, K. (2009). Immunodetection of NGF, trkA, p75 and inhibin α-subunit in interstitial cells of golden hamsters treated with hCG. J. Reprod. Dev. 55, 20.CrossRefGoogle ScholarPubMed
Wood, K.W., Sarnecki, C., Roberts, T.M. & Blenis, J. (1992). Ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 68, 1041–50.CrossRefGoogle ScholarPubMed
Xing, J., Kornhauser, J.M., Xia, Z., Thiele, E.A. & Greenberg, M.E. (1998). Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18, 1946–55.CrossRefGoogle ScholarPubMed
Yamada, M., Ohnishi, H., Sano, S., Nakatani, A., Ikeuchi, T. & Hatanaka, H. (1997). Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272, 30334–9.CrossRefGoogle ScholarPubMed
York, R.D., Molliver, D.C., Grewal, S.S., Stenberg, P.E., McCleskey, E.W. & Stork, P.J.S. (2000). Role of phosphoinositide 3-kinase and endocytosis in nerve growth factor-induced extracellular signal-regulated kinase activation via Ras and Rap1. Mol. Cell. Biol. 20, 8069–83.CrossRefGoogle ScholarPubMed
Yuan, C., Hu, H. & Xu, G. (2001). Single amino-acid substitution in the N-terminal arm altered the tetramer stability of rat muscle lactate dehydrogenase A. Sci. China C. Life Sci. 44, 576–84.CrossRefGoogle ScholarPubMed
Yuan, J., Lipinski, M. & Degterev, A. (2003). Diversity in the mechanisms of neuronal cell death. Neuron 40, 401–13.CrossRefGoogle ScholarPubMed