Neurotrophins and their receptors: A convergence point for many signalling pathways

Nature Reviews Neuroscience

Volumn 4, Issue 4, 2003, Pages 299-309

  Chao, Moses V ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED GROWTH FACTOR; CELL SURFACE RECEPTOR; ION CHANNEL; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; PROTEIN P75; NERVE GROWTH FACTOR RECEPTOR;

BRAIN REGION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL SURFACE; CELL SURVIVAL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; GENETICS; HUMAN; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; NERVE REGENERATION; NERVOUS SYSTEM; PAIN; PHYSIOLOGY; PRENATAL DEVELOPMENT;

VERTEBRATA;

ANIMALS; CELL DIFFERENTIATION; HUMANS; NERVE GROWTH FACTORS; NERVE REGENERATION; NERVOUS SYSTEM; NEURONAL PLASTICITY; NEURONS; PAIN; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 0037762690     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1078     Document Type: Article

References (106)

1. McAllister, A., Katz, L. & Lo, D. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22, 295-318 (1999).
2. Poo, M.-M. Neurotrophins as synaptic modulators. Nature Rev. Neurosci. 2, 24-31 (2001).
3. Huang, E. & Reichardt, L. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736 (2001).
4. Chao, M. V. & Hempstead, B. L. p75 and trk: a two-receptor system. Trends Neurosci. 19, 321-326 (1995).
5. Kaplan, D. R. & Miller, F. D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391 (2000).
6. Dechant, G. & Barde, Y.-A. The neurotrophin receptor p75NTR: novel functions and implications for diseases of the nervous system. Nature Neurosci. 5, 1131-1136 (2002).
7. Gall, C. & Isackson, P. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 254, 758-761 (1989).
8. Blochl, A. & Thoenen, H. Characterization of nerve growth factor release from hippocampal neurons: evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur. J. Neurosci. 7, 10464-10472 (1995).
9. Wang, X. H. & Poo, M.-M. Potentiation of developing synapses by postsynaptic release of NT-4. Neuron 19, 825-835 (1998).
10. Gall, C. Regulation of brain neurotrophin expression by physiological activity. Trends Pharmacol. Sci. 13, 401-403 (1992).
11. Schoups, A., Elliott, R., Friedman, W. & Black, I. NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Brain Res. 86, 326-334 (1995).
12. Lein, E., Hohn, A. & Shatz, C. Dynamic regulation of BDNF and NT-3 expression during visual system development. J. Comp. Neurol. 420, 1-18 (2000).
13. Kohara, K., Kitamura, A., Morishima, M. & Tsumoto, T. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291, 2419-2423 (2001).
14. Balkowiec, A. & Katz, D. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22, 10399-10407 (2002).
15. Chen, K. et al. Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits. J. Neurosci. 17, 7288-7296 (1997).
16. Lyons, W. E. et al. Brain-derived neurotrophic factor- deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc. Natl Acad. Sci. USA 96, 15239-15244 (1999).
17. Kernie, S., Liebl, D. & Parada, L. BDNF regulates eating behavior and locomotor activity in mice. EMBO J. 19, 1290-1300 (2000).
18. Rios, M. et al. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15, 1748-1757 (2001).
19. Korte, M. et al. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl Acad. Sci. USA 92, 8856-8860 (1995).
20. Patterson, S. et al. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137-1145 (1996).
21. Heymach, J. V. & Shooter, E. M. The biosynthesis of neurotrophin heterodimers by transfected mammalian cells. J. Biol. Chem. 270, 12297-12304 (1995).
22. Mowla, S. J. et al. Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J. Biol. Chem. 276, 12660-12666 (2001).
23. Dechant, G. et al. Expression and binding characteristics of the BDNF receptor chick trkB. Development 119, 545-558 (1993).
24. Mahadeo, D., Kaplan, L., Chao, M. V. & Hempstead, B. L. High affinity nerve growth factor binding displays a faster rate of association than p140(trk) binding — implications for multisubunit polypeptide receptors. J. Biol. Chem. 269, 6884-6891 (1994).
25. Schropel, A., von Schack, D., Dechant, G. & Barde, Y-A. Early expression of the nerve growth factor receptor ctrkA in chick sympathetic and sensory ganglia. Mol. Cell. Neurosci. 6, 544-556 (1995).
26. Arevalo, J. et al. TrkA immunoglobulin-like ligand binding domains inhibit spontaneous activation of the receptor. Mol. Cell Biol. 20, 5908-5916 (2000).
27. Esposito, D. et al. The cytoplasmic and transmembrane domains of the p75 and TrkA receptors regulate high affinity binding to nerve growth factor. J. Biol. Chem. 276, 32687-32695 (2001).
28. Hempstead, B. L., Martin-Zanca, D., Kaplan, D. R., Parada, L. F. & Chao, M. V. High-affinity NGF binding requires co- expression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-683 (1991).
29. Benedetti, M., Levi, A. & Chao, M. V. Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc. Natl Acad. Sci. USA 90, 7859-7863 (1993).
30. Bibel, M., Hoppe, E. & Barde, Y. Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J. 18, 616-622 (1999).
31. Baloh, R., Enomoto, H., Johnson, E. & Milbrandt, J. The GDNF family ligands and receptors — implications for neural development. Curr. Opin. Neurobiol. 10, 103-110 (2000).
32. Ginty, D. & Segal, R. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 12, 268-274 (2002).
33. Grimes, M., Beattie, E. & Mobley, W. A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc. Natl Acad. Sci. USA 94, 9909-9914 (1997).
34. Patapoutian, A. & Reichardt, L. Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11, 272-280 (2001).
35. Hempstead, B. The many faces of p75NTR. Curr. Opin. Neurobiol. 12, 260-267 (2002).
36. Roux, P. & Barker, P. Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203-233 (2002).
37. Lonze, B. & Ginty, D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623 (2002).
38. York, R. et al. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392, 622-626 (1998).
39. Majdan, M. & Miller, F. Neuronal life and death decisions: functional antagonism between the Trk and p75 neurotrophin receptors. Int. J. Dev. Neurosci. 17, 153-161 (1999).
40. Dowling, P. et al. Upregulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology 53, 1676-1682 (1999).
41. Roux, P., Colicos, M., Barker, P. & Kennedy, T. p75 neurotrophin receptor expression is induced in apoptotic neurons after seizure. J. Neurosci. 19, 6887-6896 (1999).
42. Beattie, M. et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36, 375-386 (2002).
43. Harrington, A. W., Kim, J. Y. & Yoon, S. O. Activation of Rac GTPase by p75 is necessary for c-jun N-terminal kinase- mediated apoptosis. J. Neurosci. 22, 156-166 (2002).
44. Khursigara, G. et al. A pro-survival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor interacting protein 2. J. Neurosci. 21, 5854-5863 (2001).
45. DeFreitas, M., McQuillen, P & Shatz, C. A novel p75NTR signaling pathway promotes survival, not death, of immunopurified neocortical subplate neurons. J. Neurosci. 21, 5121-5129 (2001).
46. Lee, R., Kermani, P., Teng, K. & Hempstead, B. Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948 (2001).
47. Chao, M. V. Growth factor signaling: where is the specificity? Cell 68, 995-997 (1992).
48. Lohof, A. M., Ip, N. & Poo, M.-M. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353 (1993).
49. Kang, H. & Schuman, E. M. Long-lasting neurotrophin- induced enhancement of synaptic transmission in the adult hippocampus Science 267, 1658-1662 (1995).
50. Levine, E. S., Dreyfus, C. F., Black, I. B. & Plummer, M. R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl Acad. Sci. USA 92, 8074-8077 (1995).
51. Xie, C. et al. Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4. Proc. Natl Acad. Sci. USA 97, 8116-8121 (2000).
52. Korte, M. et al. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl Acad. Sci. USA 93, 12547-12552 (1996).
53. Schuman, E. Neurotrophin regulation of synaptic transmission. Curr. Opin. Neurobiol. 9, 105-109 (1999).
54. Schinder, A. & Poo, M.-M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23, 639-645 (2000).
55. Yang, F. et al. PI-3 kinase and IP3 are both necessary and sufficient to mediate NT3-induced synaptic potentiation. Nature Neurosci. 4, 19-28 (2001).
56. Minichiello, L. et al. Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24, 401-414 (1999).
57. Minichiello, L. et al. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36, 121-137 (2002).
58. Peterson, D. A., Dickinson-Anson, H. A., Leppert, J. T., Lee, K.-F. & Gage, F. H. Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. J. Comp. Neurol. 404, 1-20 (1999).
59. von Schack, D. et al. Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nature Neurosci. 4, 977-978 (2001).
60. Dalva, M. et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956 (2000).
61. Grunwald, I. et al. Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 32, 1027-1040 (2001).
62. Henderson, J. et al. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 1041-1056 (2001).
63. Takasu, M., Dalva, M., Zigmond, R. & Greenberg, M. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491-495 (2002).
64. Montell, C., Birnbaumer, L. & Flockerzi, V. The TRP channels, a remarkably functional family. Cell 108, 595-598 (2002).
65. Li, H., Xu, X. & Montell, C. Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron 24, 261-273 (1999).
66. Caterina, M. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824 (1997).
67. Shu, X. & Mendell, L. Neurotrophins and hyperalgesia. Proc. Natl Acad. Sci. USA 96, 7693-7696 (1999).
68. 2-mediated inhibition. Nature 411, 957-962 (2001).
69. Johagen, M. et al. Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement. Geriat. Cogn. 9, 246-257 (1998).
70. Thoenen, H. & Sendtner, M. Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nature Neurosci. 5, S1046-S1050 (2002).
71. Lin, S. et al. BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20-27 (1998).
72. Tucker, K. & Fadool, D. Neurotrophin modulation of voltage- gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J. Physiol. (Lond.) 54, 413-429 (2002).
73. Figurov, A., Pozzo-Miller, L., Olafsson, T., Wang, B. & Lu, B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709 (1996).
74. Gottschalk, W., Pozzo-Miller, L., Figurov, A. & Lu, B. Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J. Neurosci. 18, 6830-6839 (1998).
75. Xu, B. et al. The role of brain-derived neurotrophic factors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J. Neurosci. 20, 6888-6897 (2000).
76. Kovalchuk, Y., Hanse, E., Kafitz, K. & Konnerth, A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729-1734 (2002).
77. Balkowiec, A., Kunze, D. & Katz, D. Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons. J. Neurosci. 20, 1904-1911 (2000).
78. Carroll, R., Beattie, E., von Zastrow, M. & Malenka, R. Role of AMPA receptor endocytosis in synaptic plasticity. Nature Rev. Neurosci. 2, 315-324 (2001).
79. v1.9. Nature 419, 687-693 (2002).
80. Kafitz, K., Rose, C., Thoenen, H. & Konnerth, A. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401, 918-921 (1999).
81. Choi, D.-Y., Toledo-Aral, J., Segal, R. & Halegoua, S. Sustained signaling by phospholipase C-y mediates nerve growth factor-triggered gene expression. Mol. Cell Biol. 21, 2695-2705 (2001).
82. Toledo-Aral, J., Brehm, P., Halegoua, S. & Mandel, G. A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron 14, 607-611 (1995).
83. Arevalo, J. et al. A novel mutation within the extracellular domain of TrkA causes constitutive receptor activation. Oncogene 20, 1229-1234 (2001).
84. Daub, H., Weiss, F. U., Wallasch, C. & Ullrich, A. Role of transactivation of the EGF receptor in signalling by G-protein coupled receptors. Nature 379, 557-560 (1996).
85. Luttrell, L., Daaka, Y. & Lefkowitz, R. Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr. Opin. Cell Biol. 11, 177-183 (1999).
86. Lee, F. & Chao, M. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl Acad. Sci. USA 92, 3555-3560 (2001).
87. Lee, F. S., Ragagopal, R., Kim, A. H., Chang, P & Chao, M. V. Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J. Biol. Chem. 277, 9096-9102 (2002).
88. Takei, N. et al. Pituitary adenylate cyclase-activating polypeptide promotes the survival of basal forebrain cholinergic neurons in vitro and in vivo: comparison with effects of nerve growth factor. Eur. J. Neurosci. 12, 2273-2280 (2000).
89. Williams, L. R. et al. Continuous infusion of NGF prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl Acad. Sci. USA 83, 9231-9235 (1986).
90. Kotecha, S. et al. A D2 class dopamine receptor transactivates a receptor tyrosine kinase to inhibit NMDA receptor transmission. Neuron 35, 1111-1122 (2002).
91. Otto, C. et al. Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J. Neurosci. 21, 5520-5527 (2001).
92. Hashimoto, H., Shintani, N. & Baba, A. Higher brain functions of PACAP and a homologous Drosophila memory gene amnesiac: insights from knockouts and mutants. Biochem. Biophys. Res. Commun. 297, 427-432 (2002).
93. Ledent, C. et al. Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor. Nature 388, 674-678 (1997).
94. Airaksinen, M. & Saarma, M. The GDNF family: signalling, biological functions and therapeutic value. Nature Rev. Neurosci. 3, 383-394 (2002).
95. Tsui-Pierchala, B., Milbrandt, J. & Johnson, E. NGF utilizes c-Ret via a novel GFL-independent, inter-RTK signaling mechanism to maintain the trophic status of mature sympathetic neurons. Neuron 33, 261-273 (2002).
96. Duman, R., Heninger, G. & Nestler, E. A molecular and cellular theory of depression. Arch. Gen. Psychiatry 54, 597-606 (1997).
97. Cai, D., Shen, Y, DeBellard, M., Tang, S. & Filbin, M. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22, 89-101 (1999).
98. Luo, Y., Raible, D. & Raper, J. Collapsin, a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227 (1993).
99. Tuttle, R. & O'Leary, D. Neurotrophins rapidly modulate growth cone response in the axon guidance molecule, collapsin-1. Mol. Cell. Neurosci. 11, 1-8 (1998).
100. Dontchev, V. & Letourneau, P. Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J. Neurosci. 22, 6659-6669 (2002).
101. Fournier, A., GrandPre, T & Strittmatter, S. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346 (2001).
102. Wang, K. et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417, 941-944 (2002).
103. Liu, B., Fournier, A., GrandPre, T. & Strittmatter, S. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Nature 297, 1190-1193 (2002).
104. Domeniconi, M. et al. Myelin-associated glycoprotein interacts with the Nogo-66 receptor to inhibit neurite outgrowth. Neuron 35, 283-290 (2002).
105. Wang, K., Kim, J., Sivasankaran, R., Segal, R. & He, Z. p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78 (2002).
106. NTR and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nature Neurosci. 5, 1302-1308 (2002).