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

Zygote

Volumn 21, Issue 2, 2013, Pages 187-197

  Chaves, R N ^a   Alves, A M C V ^a   Lima, L F ^a   Matos, H M T ^b   Rodrigues, A P R ^a   Figueiredo, J R ^a  

^a STATE UNIVERSITY OF CEARÁ   (Brazil)

^b Federal University of Sao Francisco Valley   (Brazil)

Author keywords

Follicles; NGF; Ovary; p75; TrkA

Indexed keywords

EID: 84876753570     PISSN: 09671994     EISSN: 14698730     Source Type: Journal    
DOI: 10.1017/S0967199412000111     Document Type: Article

References (108)

1. Adhikari, D. & Liu, K. (2009). Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr. Rev. 30, 438-64
2. 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
3. Airaksinen, M.S. & Saarma, M. (2002).The GDNF family: Signalling, biological functions and therapeutic value. Nat. Ver. Neurosci. 3, 383-94
4. 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
5. 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
6. Aloe, L. (2004). Rita Levi-Montalcini: The discovery of nerve growth factor and modern neurobiology. Trends Cell. Biol. 14, 395-9
7. 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
8. 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
9. Barker, P.A. (2004). p75NTR is positively promiscuous: Novel partners and new insights. Neuron 42, 529-533
10. 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 kinasedependent phosphorylation of Bad. J. Neurosci. 23, 11373-81
11. Barrett, G.L. (2000). The p75 neurotrophin receptor and neuronal apoptosis. Prog. Neurobiol. 61, 205-29
12. Baud, V. & Karin, M. (2009). Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 8, 33-40
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. Caporali, A. & Emanueli, C. (2009). Cardiovascular actions of neurotrophins. Physiol. Rev. 89, 279-308
20. Chao, V.M. (2003). Neurotrophins and their receptors: A convergence point for many signaling pathways. Nature Rev. 4, 299-309
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. Crews, C., Alessandrini, A. & Erikson, E. (1992). The primary structure ofMEK, a protein kinase that phosphorylates the ERK gene product. Science 258, 478-80
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. Dissen, G.A., Romero, C., Paredes, A. & Ojeda, S.R. (2002). Neurotrophic control of ovarian development. Microsc. Res. Tech. 59, 509-15
36. 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
37. Fahnestock, M., Yu, G. & Coughlin, M.D. (2004). ProNGF: A neurotrophic or an apoptotic molecule? Prog. Brain Res. 146, 101-10
38. 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 -/stathmin-mediated death signaling pathway. Reproduction 142, 319-31
39. 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
40. Garcia-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
41. 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
42. Glebova, N.O. & Ginty, D.D. (2005). Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 28, 191-222
43. GrandPré, T., Li, S. & Strittmatter, S.M. (2002). Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417, 547-51
44. Greco, A., Villa, R. & Pierotti, M.A. (1996). Genomic organization of the human NTRK1 gene. Oncogene 13, 2463-6
45. Haase, G., Pettmann, B., Raoul, C. & Henderson, C.E. (2008). Signaling by death receptors in the nervous system. Curr. Opin. Neurobiol. 18, 284-91
46. 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
47. He, X.E. & Garcia, K.C. (2004). Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304, 870-5
48. Hirshfield, A.N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43-101
49. 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
50. Ibañez, C.F. (1998). Emerging themes in structural biology of neurotrophic factors. Trends Neurosci. 21, 438-44
51. 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/mitogenactivated protein kinase-extracellularly regulated kinase 2-dependent pathway. J. Clin. Endocrinol. Metab. 94, 3065-71
52. 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
53. Kaplan, D.R. & Miller, F.D. (2000). Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-91
54. Karin, M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature 441, 431-6
55. 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
56. 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
57. 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
58. Lara, H.E., McDonald, J.K. & Ojeda, S.R. (1990). Involvement of nerve growth factor in female sexual development. Endocrinology. 126, 364-75
59. 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
60. Lee R., Kermani, P., Teng, K.K. & Hempstead, B.L. (2001). Regulation of cell survival by secreted proneurotrophins. Science.294, 1945-8.
61. 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
62. 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
63. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science. 237, 1154-1162
64. Levi-Montalcini, R. & Calissano, P. (1986). Nerve growth factor as a paradigm for other polypeptide growth factors. Trends Neurosci. 9, 473-7
65. 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
66. 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
67. Marte, B.M. & Downward, J. (1997). PKB/Akt: Connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem. Sci. 22, 355-8
68. 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
69. 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
70. 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
71. Molloy, N.H., Read, D.E. & Gorman, A.M. (2011). Nerve growth factor in cancer cell death and survival. Cancers 3, 510-530
72. 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
73. Nilsson, E., Dole, G. & Skinner, M.K. (2009). Neurotrophin NT3 promotes ovarian primordial to primary follicle transition. Reproduction 138, 697-707
74. 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
75. Nomoto, H., Takaiwa, M., Mouri, A. & Furukawa, S. (2007). Pro-region of neurotrophins determines the processing efficiency. Biochem. Biophys. Res. Commun. 356, 919-24
76. 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
77. Ojeda, S.R. & Dissen, G.A. (1994). Developmental regulation of the ovary via growth factor tyrosine kinase receptors. Trends Endocrinol. Metab. 5, 317-23
78. 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
79. 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
80. 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
81. Rabin, S., Cleghorn, V. & Kaplan, D. (1993). SNT, a differentiation-specific target of neurotrophic factorinduced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol. 13, 2203-13
82. 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
83. 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
84. 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
85. 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
86. 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
87. Roux, P.P. & Barker, P.A. (2002). Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203-33
88. 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
89. 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
90. 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
91. 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
92. Simi, A. & Ibañez, C.F. (2010). Assembly and activation of neurotrophic factor receptor complexes. Dev. Neurobiol. 70, 323-31
93. Skinner, M.K., Lobb, D. & Dorrington, J.H. (1987). Ovarian thecal/interstitial cells produce an epidermal growth factor-like substance. Endocrinology 121, 1892-9
94. Snider, W.D. (1994). Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77, 627-38
95. Sofroniew, M.V., Howe, C.L. & Mobley, W.C. (2001). Nerve Growth Factor signalling, neuroprotection, and neural repair. Ann. Rew. Neurosci. 24, 1217-81
96. 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 lowaffinity NGF receptors. Mol. Endocrinol. 14, 124-36
97. 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
98. Terenghi, G. (1999). Peripheral nerve regeneration and neurotrophic factors. J. Anat. 194, 1-14
99. Tessarollo, L. (1998). Pleiotropic functions of neurotrophins in development. Cytokine Growth Factor Rev. 9, 125-37
100. 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
101. 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
102. Weng, Q., Shi, Z.Q., Tukada, J., Watanabe, G. & Taya, K. (2009). Immunodetection of NGF, trkA, p75 and inhibin -subunit in interstitial cells of golden hamsters treated with hCG. J. Reprod. Dev. 55, 20
103. 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
104. Xing, J., Kornhauser, J.M., Xia, Z., Thiele, E.A. & Greenberg, M.E. (1998). Nerve growth factor activates extracellular signal-regulated kinase and p38mitogen-Activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18, 1946-55
105. 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 brainderived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272, 30334-9
106. 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 factorinduced extracellular signal-regulated kinase activation via Ras and Rap1. Mol. Cell. Biol. 20, 8069-83
107. 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
108. Yuan, J., Lipinski, M. & Degterev, A. (2003). Diversity in the mechanisms of neuronal cell death. Neuron 40, 401-13