Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord

European Journal of Neuroscience

Volumn 20, Issue 7, 2004, Pages 1769-1778

  Slack, Sarah E ^a   Pezet, Sophie ^a   McMahon, Stephen B ^a   Thompson, Stephen W N ^a   Malcangio, Marzia ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Novartis Institute   (United Kingdom)

Author keywords

Central sensitization; Neurotrophin; Plasticity; Signalling

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEUROTROPHIN; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; IN VITRO STUDY; MALE; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; ELECTRIC STIMULATION; GLUTAMIC ACID; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POSTERIOR HORN CELLS; PROTEIN KINASE C; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 8144230420     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03656.x     Document Type: Article

References (51)

1. Anson, L.C., Chen, P.E., Wyllie, D.J., Colquhoun, D. & Schoepfer, R. (1998) Identification of amino acid residues of the NR2A subunit that control glutamate potency in recombinant NR1/NR2A NMDA receptors. J. Neurosci., 18, 581-589.
2. Anson, L.C., Schoepfer, R., Colquhoun, D. & Wyllie, D.J. (2000) Single-channel analysis of an NMDA receptor possessing a mutation in the region of the glutamate binding site. J. Physiol. (Lond), 527, 225-237.
3. Arvanian, V.L. & Mendell, L.M. (2001) Acute modulation of synaptic transmission to motorneurons by BDNF in the neonatal rat spinal cord. Eur. J. Neurosci., 14, 1800-1808.
4. Blum, R., Kafitz, K.W. & Konnerth, A. (2002) Neurotrophin-evoked depolarization requires the sodium channel Na (V), 1.9. Nature, 419, 683-684.
5. Brenner, G.J., Ji, R.R. & Woolf, C.J. (2002) Phosphorylation and trafficking of the NMDA receptor NR 1 subunit in dorsal horn neurons after noxious stimulation. Soc. Neurosci. Abstr., 2, 652.9.
6. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature, 356, 521-523.
7. Cho, H.J., Kim, S.Y., Park, M.J., Kim, D.S., Kim, J.K. & Chu, M.Y. (1997a) Expression of mRNA for brain-derived neurotrophic factor in the dorsal root ganglion following peripheral inflammation. Brain Res., 749, 358-362.
8. Cho, H.J., Kim, J.K., Zhou, X.F. & Rush, R.A. (1997b) Increased brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia and spinal cord following peripheral inflammation. Brain Res., 764, 269-272.
9. Cull-Candy, S., Brickley, S. & Farrant, M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327-335.
10. Dekker, L.V. & Parker, P.J. (1994) Protein kinase C: a question of specificity. Trends Biochem. Sci., 19, 73-77.
11. Di Luca, M., Gardoni, F., Finardi, A., Pagliardini, S., Cattabeni, F., Battaglia, G. & Missale, C. (2001) NMDA receptor subunits are phosphorylated by activation of neurotrophin receptors in PSD of rat spinal cord. Neuroreport, 12, 1301-1305.
12. Garraway, S.M., Petruska, J.C. & Mendell, L.M. (2003) BDNF sensitizes the response of lamina I1 neurons to high threshold primary afferent inputs. Eur. J. Neurosci., 18, 2467-2476.
13. 2+/calmodulin-dependent protein kinase I1 in long-term potentiation. J. Neurosci., 21, 7053-7062.
14. Gooney, M. & Lynch, M.A. (2001) Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB. J. Neurochem., 77, 1198-1207.
15. Groth, R. & Aanonsen, L. (2002) Spinal brain-derived neurotrophic factor (BDNF) produces hyperalgesia in normal mice while antisense directed against either BDNF or trkB, prevent inflammation-induced hyperalgesia. Pain, 100, 171-181.
16. Guo, W., Zou, S., Guan, Y, Ikeda, T., Tal, M., Dubner, R. & Ren, K. (2002) Tyrosine phosphorylation of the NR2B subunit of the NMDA receptor in the spinal cord during the development and maintenance of inflammatory hyperalgesia. J. Neurosci., 22, 6208-6217.
17. Heppenstall, P.A. & Lewin, G.R. (2001) BDNF but not NT-4 is required for normal flexion reflex plasticity and function. Proc. Nat Acad. Sci. USA, 98, 8107-8112.
18. Heumann, R. (1994) Neurotrophin signalling. Curr. Opin. Neurobiol., 4, 668-679.
19. Huang, E.J. & Reichardt, L.F. (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci., 24, 677-736.
20. Ji, R.R., Baba, H., Brenner, G.J. & Woolf, C. J. (1999) Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat. Neurosci., 2, 1114-1119.
21. Kerr, B.J., Bradbury, E.J., Bennett, D.L., Trivedi, P.M., Dassan, P., French, J., Shelton, D.B., McMahon, S.B. & Thompson, S.W. (1999) Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J. Neurosci., 19, 5138-5148.
22. Knusel, B., Rabin, S.J., Hefti, F. & Kaplan, D.R. (1994) Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J. Neurosci., 14, 1542-1554.
23. Kuryatov, A., Laube, B., Betz, H. & Kuhse, J. (1994) Mutational analysis of the glycine-binding site of the NMDA receptor, structural similarity with bacterial amino acid-binding proteins. Neuron, 12, 1291-1300.
24. Lan, J.Y., Skeberdis, V.A., Jover, T., Grooms, S.Y., Lin, Y., Araneda, R.C., Zheng, X., Bennett, M.V. & Zukin, R.S. (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci., 4, 382-390.
25. Lever, I.J., Bradbury, E.J., Cunningham, J.R., Adelson, D.W., Jones, M.G., McMahon, S.B., Marvizon, J.C. & Malcangio, M. (2001) Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J. Neurosci., 21, 4469-4477.
26. Lever, L.J., Pezet, S., McMahon, S.B. & Malcangio, M. (2003) The signalling components of sensory fiber transmission involved in the activation of ERK MAP kinase in the mouse dorsal horn. Mol. Cell Neurosci., 24, 259-270.
27. Li, Y.X., Zhang, Y., Lester, H.A., Schuman, E.M. & Davidson, N. (1998) Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci., 18, 10231-10240.
28. Liao, G.Y., Wagner, D.A., Hsu, M.H. & Leonard, J.P. (2001) Evidence for direct protein kinase-C mediated modulation of N-methyl-D-aspartate receptor current. Mol. Pharmacol., 59, 960-964.
29. Logan, S.M., Rivera, F.E. & Leonard, J.P. (1999) Protein kinase C modulation of recombinant NMDA receptor currents: roles for the C-terminal C1 exon and calcium ions. J. Neurosci., 19, 974-986.
30. MacDonald, J.F., Kotecha, S.A., Lu, W.Y. & Jackson, M.F. (2001) Convergence of PKC-dependent kinase signal cascades on NMDA receptors. Curr. Drug Targets, 2, 299-312.
31. Malcangio, M. & Bowery, N.G. (1994) Effect of the tachykinin NK1 receptor antagonists, RP 67580 and SR 140333, on electrically-evoked substance P release from rat spinal cord. Br. J. Pharmacol., 113, 635-641.
32. Malcangio, M. & Lessmann, V. (2003) A common thread for pain and memory synapses? Brain-derived neurotrophic factor and trkB receptors. Trends Pharmacol. Sci., 24, 116-121.
33. Martin, W.J., Malmberg, A.B. & Basbaum, A.I. (2001) PKCgamma contributes to a subset of the NMDA-dependent spinal circuits that underlie injury-induced persistent pain. J. Neurosci., 21, 5321-5327.
34. Michael, G.J., Averill, S., Nitkunan, A., Rattray, M., Bennett, D.L., Yan, Q. & Priestley, J.V. (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci., 17, 8476-8490.
35. Pascual, M., Climent, E. & Guerri, C. (2001) BDNF induces glutamate release in cerebrocortical nerve terminals and in cortical astrocytes. Neuroreport, 12, 2673-2677.
36. Pezet, S., Cunningham, J., Patel, J., Grist, J., Gavazzi, I., Lever, I.J. & Malcangio, M. (2002a) BDNF modulates sensory neuron synaptic activity by a facilitation of GABA transmission in the dorsal horn. Mol. Cell Neurosci., 21, 51-62.
37. Pezet, S., Malcangio, M., Lever, I.J., Perkinton, M.S., Thompson, S.W., Williams, R.J. & McMahon, S.B. (2002b) Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn. Mol. Cell Neurosci., 21, 684-695.
38. Pezet, S., Malcangio, M. & McMahon, S.B. (2002c) BDNF: a neuromodulator in nociceptive pathways? Brain Res. Brain Res. Rev., 40, 240-249.
39. Raymond, L.A., Tingley, W.G., Blackstone, C.D., Roche, K.W. & Huganir, R.L. (1994) Glutamate receptor modulation by protein phosphorylation. J. Physiol. Paris, 88, 181-192.
40. Scarisbrick, I.A., Isackson, P.J. & Windebank, A.J. (1999) Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 in the adult rat spinal cord: regulation by the glutamate receptor agonist kainic acid. J. Neurosci., 19, 7757-7769.
41. Sheng, M., Cummings, J., Roldan, L.A., Jan, Y.N. & Jan, L.Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature, 368, 144-147.
42. Slack, S.E. & Thompson, S.W. (2002) Brain-derived neurotrophic factor induces NMDA receptor 1 phosphorylation in rat spinal cord. Neuroreport, 13, 1967-1970.
43. Suen, P.C., Wu, K., Levine, E.S., Mount, H.T., Xu, J.L., Lin, S.Y & Black, I.B. (1997) Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-D-aspartate receptor subunit 1. Proc. Natl Acad. Sci. USA, 94, 8191-8195.
44. Tingley, W.G., Ehlers, M.D., Kameyama, K., Doherty, C., Ptak, J.B., Riley, C.T. & Huganir, R.L. (1997) Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem., 272, 5157-5166.
45. Tingley, W.G., Roche, K.W., Thompson, A.K. & Huganir, R.L. (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature, 364, 70-73.
46. Xiong, Z.G., Raouf, R., Lu, W.Y., Wang, L.Y., Orser, B.A., Dudek, E.M., Browning, M.D. & MacDonald, J.F. (1998) Regulation of N-methyl-D-aspartate receptor function by constitutively active protein kinase C. Mol. Pharmacol., 54, 1055-1063.
47. Zheng, X., Zhang, L., Wang, A.P., Bennett, M.V. & Zukin, R.S. (1999) Protein kinase C potentiation of N-methyl-D-aspartate receptor activity is not mediated by phosphorylation of N-methyl-D-aspartate receptor subunits. Proc. Natl Acad. Sci. USA, 96, 15262-15267.
48. Zhou, X.F., Parada, L.F., Soppet, D. & Rush, R.A. (1993) Distribution of trkB tyrosine kinase immunoreactivity in the rat central nervous system. Brain Res., 622, 63-70.
49. Zhou, X.F. & Rush, R.A. (1996) Endogenous brain-derived neurotrophic factor is anterogradely transported in primary sensory neurons. Neuroscience, 74, 945-953.
50. Zou, X., Lin, Q. & Willis, W.D. (2000) Enhanced phosphorylation of NMDA receptor 1 subunits in spinal cord dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats. J. Neurosci., 20, 6989-6997.
51. Zou, X., Lin, Q. & Willis, W.D. (2002) Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal hom and spinothalamic tract neurons after intradermal injection of capsaicin in rats. Neuroscience, 115, 775-786.