Signal transduction by the neurotrophin receptors

Current Opinion in Cell Biology

Volumn 9, Issue 2, 1997, Pages 213-221

  Kaplan, David R ^a   Miller, Freda D ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN; NEUROTROPHIN RECEPTOR;

APOPTOSIS; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CELL TYPE; NERVE CELL; NEUROMA; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030907924     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(97)80065-8     Document Type: Article

References (79)

1. Snider WD: Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 1994, 77:627-638.
2. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS: Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 1994, 76:1001-1011.
3. Martin-Zanca D, Hughes SH, Barbacid M: A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences. Nature 1986, 319:743.
4. Nakagawara K, Arima-Nakagawara M, Scavarda NJ, Azar CG, Cantor AB, Brodeur GM: Association between high levels of expression of the trk gene and favorable outcome in human neuroblastoma. New Engl Jour Med 1993, 328:847-854.
5. Segal RA, Goumnerova LC, Kwon YK, Stiles CD, Pomeroy SL: Expression of the neurotropin receptor trkC is linked to a favorable outcome in medulloblastoma. Proc Natl Acad Sci USA 1994, 91:12867-12871.
6. Chao MV, Hempslead BL: p75 and Trk: a two-receptor system. Trends Neurosci 1995, 18:321-326.
7. Segal R, Greenberg ME: Intracellular signaling pathways activated by neurotrophic receptors. Annu Rev Neurosci 1996, 19:463-489. The most recent comprehensive review on neurotrophic factor signal transduction.
8. Greene LA, Kaplan DR: Early events in rteurotrophin signalling via Trk and p75 receptors. Curr Opin Neurobiol 1995, 5:579-587. A recent review on neurotrophin signaling that is mediated by Trk and NGF.
9. Barbacid M: Neurotrophic factors and their receptors. Curr Opin Cell Biol 1995, 7:148-155.
10. Greene LA, Tischler AS: PC12 pheochromocytoma cells in neurobiological research. Adv Cell Neurobiol 1982, 3:373-414.
11. Nakamura T, Sanokawa R, Sasaki Y, Ayusawa D, Oishi M, Mori N: N-shc: a neuronal-specific adapter molecule that mediates signaling from neurotrophin/trk to ras/MAPK pathway. Oncogene 1996, 13:1111-1121.
12. Baxter RM, Cohen P, Obermeier A, Ullrich A, Downes CP, Doza YN: Phosphotyrosine residues in the nerve-growth-factor receptor (trkA). Their role in the activation of inositol phospholipid metabolism and protein kinase cascades in pheochromocytoma (PC12) cells. Eur J Biochem 1995, 234:84-91.
13. Kaplan DR, Stephens RM: Neurotrophin signal transduction by the Trk receptor. J Neurobiol 1994, 25:1404-1417.
14. Stephens RM, Loeb DM, Copeland TD, Pawson T, Greene LA, Kaplan DR: Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 1994, 12:691-705.
15. Obermeier A, Bradshaw RA, Seedorf V, Choidos A, Schlessinger J, Ullrich A: Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLCγ. EMBO J 1994, 13:1585-1590.
16. Peng X, Greene LA, Kaplan DR, Stephens RM: Deletion of a conserved juxtamembrane sequence in Trk abolishes NGF-promoted neuritogenesis. Neuron 1995, 15:395-406.
17. Nobes CD, Tolkovsky AM: Neutralizing anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur J Neurosci 1995, 7:344-350.
18. Cowley S, Paterson H, Kemp P, Marshall CJ: Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 1994, 77:841-852.
19. Pang L, Sawada T, Decker SJ, Saltiel AR: Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem 1995, 270:13585-13588.
20. Marshall CJ: Specificity of receptor tyrosine kinase signalling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995, 80:179-185.
21. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME: Opposing effects of Erk and JNK-p38 map kinases on apoptosis. Science 1995, 270:1326-1331. Describes a mechanism whereby NGF suppresses apoptosis of PC12 cells. Cell death following NGF deprivation is mediated by increases in JNK and p38 kinase activities, and decreases in MAPK activity. NGF-mediated increases in MAPK activity may stimulate anti-apoptotic signaling pathways.
22. Borasio GD, Markus A, Wittinghofer A, Barde Y-A, Heumann R: Involvement of ras p21 in neurotrophin-induced response of sensory but not sympathetic neurons. J Cell Biol 1993, 121:665-672.
23. Kuo W-L, Abe M, Rhee J, Eves EM, McCarthy SA, Yan M, Templeton DJ, McMahon M, Rosner MR: Raf, but not MEK or ERK, is sufficient for differentiation of hippocampal neuronal cells. Mol Cell Biol 1996, 16:1458-1470. Tests the hypothesis that sustained MEK and MAPK activities are sufficient for neuronal differentiation. In immortalized hippocampal cells, prolonged activation of MEK and MAPK was insufficient for differentiation. Prolonged activiation of Raf-1, however, induced differentiation.
24. Vaillancourt RR, Heasley LE, Zamarripa J, Storey B, Valius M, Kazlauskas A, Johnson GL: Mitogen-activated protein kinase activation is insufficient for growth factor receptor-mediated PC12 cell differentiation. Mol Cell Biol 1995, 15:3644-3653.
25. Marsh NH, Palfrey CH: Neurotrophin-3 and brain-derived neurotrophic factor activate multiple signal transduction events but are not survival factors for hippocampal pyramidal neurons. J Neurochem 1996, 67:952-963.
26. Pollack JD, Rane SG: p21ras signaling is necessary but not sufficient to mediate neurotrophin induction of calcium channels in PC12 cells. J Biol Chem 1996, 271:8008-8014.
27. Creedon DJ, Johnson EM, Lawrence JC: Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J Biol Chem 1996, 271:20713-20718.
28. Virdee K, Tolkovsky AM: Inhibition of p42 and p44 MAP kinases by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurons. J Neurochem 1996, 67:1801-1805.
29. Klinz FJ, Wolff P, Heumann R: Nerve growth factor-stimulated mitogen-activated protein kinase activity is not necessary for neurite outgrowth of chick dorsal root ganglion sensory and sympathetic neurons. J Neurosci Res 1996, 46:720-726.
30. Belliveau DJ, Krivko I, Kohn J, Lachance C, Pozniak C, Rusakov D, Kaplan D, Miller FD: NGF and NT-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 1997, 136:375-388. First report that, in neurons, both NGF and NT-3 mediate several different biological responses through the same receptor, TrkA. Each factor induced prolonged TrkA activity, suggesting that specific receptor substrates, rather than sustained activation of a particular substrate, are responsible for differentiation responses.
31. Zirrgiebel U, Ohga Y, Carter B, Berninger B, Inagaki N, Thoenen H, Lindholm D: Characterization of trkB receptor-mediated signaling pathways in rat cerebellar granule neurons: involvement of protein kinase C in neuronal survival. J Neurochem 1995, 65:2241-2250.
32. Vambutas V, Kaplan DR, Sells MA, Chernoff J: Nerve growth factor stimulates tyrosine phosphorylation and activation of Src homology-containing protein tyrosine phosphatase 1 in PC12 cells. J Biol Chem 1995, 270:25629-25633.
33. Teng KK, Courtney JC, Van Bergen en Henegouwen P, Birge RB, Hempstead BL: Dissociation of NGF induced signal transduction from neurite elongation by expression of a mutant adaptor protein v-Crk in PC12 cells. Mol Cell Neurosci 1996, 8:157-170. Examination of the role of the 'adaptor' protein Crk in neuronal differentiation of PC12 cells. Expression of a dominant-inhibitory Crk protein inhibited neurite elongation and normal aggregation of actin filaments at the growth cones, without inhibiting the activity of known Trk signaling proteins or NGF-induced gene induction.
34. Kimura K, Hattori S, Kabuyama Y, Shizawa Y, Takayanagi J, Nakamura S, Toki S, Matsuda Y, Onodera K, Fukui Y: Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J Biol Chem 1994, 269:18961-18967.
35. Yao RI, Cooper GM: Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 1995, 267:5206-5208.
36. Franke TF, Kaplan DK, Cantley LC, Toker A: Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 1997, 275:665-668.
37. Dudek H, Datta SD, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DK, Greenberg ME: Regulation of neuronal survival by the serine-threonine kinase Akt. Science 1997, 275:661-665. Reports that expression of the serine/threonine kinase Akt in primary cerebellar neurons is both necessary and sufficient for much of the survival response of these neurons to neurotrophic factors.
38. D'Mello SR, Borodezt K, Soltoff S: Insulin-like growth factor and potassium depolarization maintain neuronal survival by distinct signaling pathways: possible involvement of PI3-kinase in IGF-I signaling. J Neurosci 1997, 17:1548-1560.
39. Matsushima H, Bogenmann E: Expression of trkA cDNA in neuroblastoma mediates differentiation in vitro and in vivo. Mol Cell Biol 1993, 13:7447-7456.
40. Yan GZ, Ziff EB: NGF regulates the PC12 cell cycle machinery through specific inhibition of the cdk kinases and induction of cyclin D1. J Neurosci 1995, 15:6200-6212.
41. Muragaki Y, Chou TT, Kaplan DR, Trojanowski JQ, Lee VM-Y: Nerve growth factor induces apoptosis in human medulloblastoma cell lines that express trkA receptors. J Neurosci 1997, 17:530-542. First report that expression of TrkA in a neural tumor cell induces NGF-mediated apoptosis.
42. Lachyankar MB, Ross AH, Litofsky NS, Condon PJ, Quesenberry PJ, Recht LD: TrkA expression decreases the in vivo aggressiveness of C6 glioma cells. Cancer Res 1997, in press. Demonstration that TrkA expression in a glioblastoma cell line decreases the aggressiveness, invasiveness, and perhaps survival of these cells in vivo.
43. Kogner P, Barbany G, Dominici C, Castello MA, Rashella G, Persson H: Coexpression of messenger RNA for Trk protooncogene and low affinity nerve growth factor receptor in neuroblastoma with favorable prognosis. Cancer Res 1993, 53:2044-2050.
44. Hoehner JC, Olsen L, Sandstedt B, Kaplan DR, Pahlman S: Association of neurotrophin receptor expression and differentiation in human neuroblastoma. Am J Path 1995, 147:102-113.
45. Kramer K, Gerald W, Lesauteur L, Saragovi HU, Dheung NKV: Prognostic value of TrkA protein detection by monoclonal antibody 5c3 in neuroblastoma. Clin Cancer Res 1996, 8:1361-1367
46. Suzuki T, Bogenmann E, Shimada H, Stram D, Seeger RC: Lack of high affinity nerve growth factor receptors in aggressive neuroblastomas. J Natl Cancer Inst 1993, 85:377-384.
47. Ryden M, Sehgal R, Dominici C, Schilling FH, Ibanez CF, Kogner P: Expression of mRNA for the neurotrophin receptor trkC in neuroblastomas with favourable tumour stage and good prognosis. Brit J Cancer 1996, 74:773-779.
48. TrkB affects survival, differentiation, and invasiveness of human neuroblastoma cells. Cancer Res 1995, 55:1798-1806. Indicates that TrkB, in contrast to TrkA, is a potent survival- and invasiveness-inducing receptor for neuroblastoma cells.
49. Wosikowski K, Giannakakou P, Valle P, Biedler JL, Spengler BA, Lucarelli E, Bates SE, Thiele CJ: Brain-derived neurotrophic factor protects neuroblastoma cells from vinblastine toxicity. Cancer Res 1996, 56:3737-3742.
50. Nakagawara A, Azar CG, Scavarda NJ, Brodeur GM: Expression and function of trk-B and BDNF in human neuroblastomas. Mol Cell Biol 1994, 14:759-767.
51. Kaplan DR, Matsumoto K, Lucarelli E, Thiele CJ: Induction of TrkB by retinoic acid mediates biological responsiveness to neurotrophins and differentiation of neuroblastoma cells. Neuron 1993, 11:321-331.
52. Hempstead BL, Martin-Zanca D, Kaplan DR, Parada LF, Chao MV: High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 1991, 350:678-683.
53. LNGFR regulates Trk signal transduction and NGF-induced neuronal differentiation in MAH cells. Neuron 1994, 12:733-745.
54. Barker PA, Shooter EM: Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 1994, 13:203-215.
55. Hantzopoulos PA, Suri C, Glass MP, Goldfarb MP, Yancopolous GD: The low affinity NGF receptor, p75, can collaborate with each of the Trks to potentiate functional responses to the neurotrophins. Neuron 1994, 13:187-201.
56. Benedetti M, Levi A, Chao MV: Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc Natl Acad Sci USA 1993, 90:7859-7863.
57. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD: Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 1993, 10:137-149.
58. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R: Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 1992, 69:737-749.
59. Dobrowsky RT, Werner MH, Castellino AM, Chao MV, Hannun Y: Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 1994, 265:1569-1599.
60. Dobrowsky RT, Jenkins GM, Hannun YA: Neurotrophins induce sphingomyelin hydrolysis: modulation by co-expression of p75 with Trk receptors. J Biol Chem 1995, 270:22135-22142. First evidence that the activity of Trk antagonizes p75NTR-mediated signal transduction. Coactivation of TrkA and p75NTR suppressed p75NTR-induced sphingomyelin hydrolysis, while activation of p75NTR in the absence of TrkA activation resulted in sphingomyelin hydrolysis.
61. Miller FD: NGF and neuronal gene expression. Prog Brain Res 1994, 103:23-33.
62. Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhauser N, Bohm-Matthaei R, Baeuerle PA, Barde YA: Selective activation of NF-κB by nerve growth factor through the neurotrophin receptor p75. Science 1996, 272:542-545. The first report of a Trk-independent signaling pathway induced by p75NTR in primary neural cells. NGF, but not BDNF and NT-3, stimulated the activity of the NFκB transcription factor in rat Schwann cells.
63. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV: Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 1996, 383:716-719. First evidence that p75NTR activity, in the absence of Trk receptor signaling, induces apoptosis of neural cells. p75NTR also stimulated the generation of ceramide and the activity of JNK.
64. Ross AH, Daou M-C, McKinnon CA, Condon PJ, Lachyankar MB, Stephens RM, Kaplan DR, Wolf DE: The neurotrophin receptor, gp75, forms a complex with the receptor tyrosine kinase TrkA. J Cell Biol 1996, 132:945-953. Reports the specific ligand-independent association of TrkA and p75NTR on cell surfaces. Both extracellular and intracellular domains of TrkA and p75NTR were required for the interactions between these receptors.
65. Wolf DE, McKinnon CA, Daou M-C, Stephens RM, Kaplan DR, Ross AH: Interaction with TrkA immobilizes gp75 in the high affinity growth factor receptor complex. J Biol Chem 1995, 270:2133-2138.
66. Miller FD, Mathew TC, Toma JG: Regulation of nerve growth factor gene expression by NGF in the developing peripheral nervous system. J Cell Biol 1991, 112:303-312.
67. Higgins GA, Koh S, Chen KS, Gage FH: NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat Neuron 1989, 3:247-256.
68. Rabizadeh S, Oh J, Zhong LT, Yang J, Bitler CM, Butcher LL, Bredesen DE: Induction of apoptosis by the low-affinity NGF receptor. Science 1993, 261:345-348.
69. Von Bartheld CS, Kiroshita Y, Prevette D, Yin QW, Oppenheim RW, Bothwell M: Positive and negative effects of neurotrophins on the isthmo-optic nucleus in chick embryos. Neuron 1994, 12:639-654.
70. Frade JM, Rodriguez-Tebar A, Barde Y-A: Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 1996, 383:166-168. Shows that, during development, endogenous NGF causes the death of rat retinal neurons that express p75NTR but not TrkA.
71. Barrett GL, Bartlett PF: The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development Proc Natl Acad Sci USA 1994, 91:6501-6505.
72. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL: A c-jun dominant negative mutant protect sympathetic neurons against programmed cell death. Neuron 1995, 14:927-939. Describes an essential role for the transcription factor c-jun in the induction of apoptosis of sympathetic neurons following NGF deprivation. Expression of c-jun was sufficient to induce cell death, while expression of dominant-inhibitory c-jun prevented cell death.
73. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM: Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 1994, 127:1717-1727.
74. Van der Zee CEM, Ross GM, Riopelle RJ, Hagg T: Survival of cholinergic forebrain neurons in developing p75NGFR-deficient mice. Science 1996, 274:1729-1732. Reports that mice lacking p75NTR have an increased number of cholinergic forebrain neurons, suggesting that p75NTR is an apoptosis-inducing receptor during neuronal development.
75. Anton ES, Weskamp G, Reichardt LF, Matthew WD: Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA 1994, 91:2795-2799.
76. Itoh K, Brackenbury R, Akeson RA: Induction of L1 mRNA in PC12 cells by NGF is modulated by cell-cell contact and does not require the high-affinity NGF receptor. J Neurosci 1995, 15:2504-2512.
77. Blochl A, Sirrenberg C: Neurotrophins stimulate the release of dopamine from rat mesencephalic neurons via trk and P75LNTR receptors. J Biol Chem 1996, 271:21100-21107.
78. Herrmann JL, Mentr DG, Hamda J-I, Marchetti D, Nakajima M, Nicolson GL: Mediation of NGF-stimulated extracellular matrix invasion by the human melanoma low-affinity p75 neurotrophin receptor: melanoma p75 functions independently of trkA. Mol Biol Cell 1993, 4:1205-1216.
79. Cunningham ME, Stephens RM, Kaplan DR, Greene LA: Autophosphorylation of activation loop tyrosines regulates signaling by the Trk NGF receptor. J Biol Chem 1997, in press.