Dysregulated Src upregulation of NMDA receptor activity: A common link in chronic pain and schizophrenia

FEBS Journal

Volumn 279, Issue 1, 2012, Pages 2-11

  Salter, Michael W ^a,b   Pitcher, Graham M ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

glutamate receptors; hippocampus; prefrontal cortex; spinal cord dorsal horn; synaptic plasticity; tyrosine kinase; tyrosine phosphatase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 4; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEU DIFFERENTIATION FACTOR; PHENCYCLIDINE; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; STRIATAL ENRICHED TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

CHANNEL GATING; CHRONIC INFLAMMATION; CHRONIC PAIN; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HUMAN; HYPERSENSITIVITY; INTRACELLULAR SIGNALING; LONG TERM POTENTIATION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECEPTOR BLOCKING; RECEPTOR UPREGULATION; REVIEW; SCHIZOPHRENIA; SPINAL CORD DORSAL HORN;

ANIMALS; CHRONIC PAIN; HUMANS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SRC-FAMILY KINASES; UP-REGULATION;

EID: 83655167390     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08390.x     Document Type: Review

References (69)

1. Kalia LV, Kalia SK, &, Salter MW, (2008) NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol 7, 742-755. (Pubitemid 351957932)
2. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, &, Dingledine R, (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
3. MacDonald JF, Porietis AV, &, Wojtowicz JM, (1982) L-Aspartic acid induces a region of negative slope conductance in the current-voltage relationship of cultured spinal cord neurons. Brain Res 237, 248-253. (Pubitemid 12115709)
4. Husi H, Ward MA, Choudhary JS, Blackstock WP, &, Grant SG, (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3, 661-669. (Pubitemid 30437200)
5. Ng D, Pitcher GM, Szilard RK, Sertie A, Kanisek M, Clapcote SJ, Lipina T, Kalia LV, Joo D, McKerlie C, et al. (2009) Neto1 is a novel CUB-domain NMDA receptor-interacting protein required for synaptic plasticity and learning. PLoS Biol 7, e41.
6. MacDonald JF, Mody I, &, Salter MW, (1989) Regulation of N-methyl-D-aspartate receptors revealed by intracellular dialysis of murine neurones in culture. J Physiol (Lond) 414, 17-34. (Pubitemid 19177289)
7. 2+-dependent phosphatase. Nature 369, 235-239. (Pubitemid 24154801)
8. Wang LY, Orser BA, Brautigan DL, &, MacDonald JF, (1994) Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A. Nature 369, 230-232. (Pubitemid 24154799)
9. Wang YT, &, Salter MW, (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369, 233-235. (Pubitemid 24154800)
10. Yu X-M, Groveman BR, Feng S, Fang XQ, Pflueger M, Lin SX, &, Bienkiewicz E, (2011) Src family kinases in the nervous system-current knowledge of src kinase activity regulation. FEBS J 279, 20-28.
11. Wang YT, Yu XM, &, Salter MW, (1996) Ca(2+)-independent reduction of N-methyl-D-aspartate channel activity by protein tyrosine phosphatase. Proc Natl Acad Sci USA 93, 1721-1725.
12. Kohr G, &, Seeburg PH, (1996) Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J Physiol (Lond) 492 (Pt 2), 445-452. (Pubitemid 26137754)
13. MacDonald JF, Trepanier C, &, Jackson M, (2011) Regulation of NMDA receptors by the tyrosine kinase Fyn. FEBS J 279, 12-19.
14. Yu XM, Askalan R, Keil GJ, &, Salter MW, (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275, 674-678. (Pubitemid 27061336)
15. Yu XM, &, Salter MW, (1998) Gain control of NMDA-receptor currents by intracellular sodium. Nature 396, 469-474. (Pubitemid 28553317)
16. Gingrich JR, Pelkey KA, Fam SR, Huang Y, Petralia RS, Wenthold RJ, &, Salter MW, (2004) Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc Natl Acad Sci USA 101, 6237-6242. (Pubitemid 38520558)
17. Lei G, Xue S, Chery N, Liu Q, Xu J, Kwan CL, Fu YP, Lu YM, Liu M, Harder KW, et al. (2002) Gain control of N-methyl-D-aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha. EMBO J 21, 2977-2989. (Pubitemid 34670382)
18. Xu J, Weerapura M, Ali MK, Jackson MF, Li H, Lei G, Xue S, Kwan CL, Manolson MF, Yang K, et al. (2008) Control of excitatory synaptic transmission by C-terminal Src kinase. J Biol Chem 283, 17503-17514.
19. Huang Y, Lu W, Ali DW, Pelkey KA, Pitcher GM, Lu YM, Aoto H, Roder JC, Sasaki T, Salter MW, et al. (2001) CAKß/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29, 485-496. (Pubitemid 32206485)
20. Yaka R, Thornton C, Vagts AJ, Phamluong K, Bonci A, &, Ron D, (2002) NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc Natl Acad Sci USA 99, 5710-5715. (Pubitemid 34411615)
21. Thornton C, Yaka R, Dinh S, &, Ron D, (2003) H-Ras modulates N-methyl-D-aspartate receptor function via inhibition of Src tyrosine kinase activity. J Biol Chem 278, 23823-23829. (Pubitemid 36830207)
22. Kalia LV, Pitcher GM, Pelkey KA, &, Salter MW, (2006) PSD-95 is a negative regulator of the tyrosine kinase Src in the NMDA receptor complex. EMBO J 25, 4971-4982. (Pubitemid 44607041)
23. Salter MW, &, Kalia LV, (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5, 317-328. (Pubitemid 38478658)
24. Ali DW, &, Salter MW, (2001) NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11, 336-342. (Pubitemid 32524099)
25. Oyama T, Goto S, Nishi T, Sato K, Yamada K, Yoshikawa M, &, Ushio Y, (1995) Immunocytochemical localization of the striatal enriched protein tyrosine phosphatase in the rat striatum: a light and electron microscopic study with a complementary DNA-generated polyclonal antibody. Neuroscience 69, 869-880.
26. Boulanger LM, Lombroso PJ, Raghunathan A, During MJ, Wahle P, &, Naegele JR, (1995) Cellular and molecular characterization of a brain-enriched protein tyrosine phosphatase. J Neurosci 15, 1532-1544.
27. Pelkey KA, Askalan R, Paul S, Kalia LV, Nguyen TH, Pitcher GM, Salter MW, &, Lombroso PJ, (2002) Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation. Neuron 34, 127-138. (Pubitemid 34270704)
28. Malenka RC, &, Nicoll RA, (1999) Long-term potentiation-a decade of progress? Science 285, 1870-1874.
29. Kalia LV, Gingrich JR, &, Salter MW, (2004) Src in synaptic transmission and plasticity. Oncogene 23, 8007-8016. (Pubitemid 39468858)
30. MacDonald JF, Jackson MF, &, Beazely MA, (2006) Hippocampal long-term synaptic plasticity and signal amplification of NMDA receptors. Crit Rev Neurobiol 18, 71-84. (Pubitemid 350194079)
31. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, &, Kandel ER, (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258, 1903-1910. (Pubitemid 23026728)
32. Lu YM, Roder JC, Davidow J, &, Salter MW, (1998) Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279, 1363-1368.
33. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, &, Yamamoto T, (2001) Characterization of Fyn-mediated tyrosine phosphorylation sites on GluRepsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem 276, 693-699. (Pubitemid 32050862)
34. Rostas JA, Brent VA, Voss K, Errington ML, Bliss TV, &, Gurd JW, (1996) Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation. Proc Natl Acad Sci USA 93, 10452-10456.
35. Petrone A, Battaglia F, Wang C, Dusa A, Su J, Zagzag D, Bianchi R, Casaccia-Bonnefil P, Arancio O, &, Sap J, (2003) Receptor protein tyrosine phosphatase alpha is essential for hippocampal neuronal migration and long-term potentiation. EMBO J 22, 4121-4131. (Pubitemid 37021741)
36. Lauri SE, Taira T, &, Rauvala H, (2000) High-frequency synaptic stimulation induces association of fyn and c-src to distinct phosphorylated components. NeuroReport 11, 997-1000. (Pubitemid 30235444)
37. Manabe T, Aiba A, Yamada A, Ichise T, Sakagami H, Kondo H, &, Katsuki M, (2000) Regulation of long-term potentiation by H-Ras through NMDA receptor phosphorylation. J Neurosci 20, 2504-2511. (Pubitemid 30220337)
38. Pitcher GM, Kalia LV, Ng D, Goodfellow NM, Yee KT, Lambe EK, &, Salter MW, (2011) Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors. Nat Med 17, 470-478.
39. Breivik H, Collett B, Ventafridda V, Cohen R, &, Gallacher D, (2006) Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur J Pain 10, 287-333.
40. Woolf CJ, &, Salter MW, (2000) Neuronal plasticity: increasing the gain in pain. Science 288, 1765-1769.
41. Salter MW, (2005) Cellular signalling pathways of spinal pain neuroplasticity as targets for analgesic development. Curr Top Med Chem 5, 557-567. (Pubitemid 41052328)
42. Liu XJ, &, Salter MW, (2010) Glutamate receptor phosphorylation and trafficking in pain plasticity in spinal cord dorsal horn. Eur J Neurosci 32, 278-289.
43. Beggs S, &, Salter MW, (2010) Microglia-neuronal signalling in neuropathic pain hypersensitivity 2.0. Curr Opin Neurobiol 20, 474-480.
44. Guo H, &, Huang LY, (2001) Alteration in the voltage dependence of NMDA receptor channels in rat dorsal horn neurones following peripheral inflammation. J Physiol 537, 115-123. (Pubitemid 33076959)
45. Isaev D, Gerber G, Park SK, Chung JM, &, Randik M, (2000) Facilitation of NMDA-induced currents and Ca2+ transients in the rat substantia gelatinosa neurons after ligation of L5-L6 spinal nerves. NeuroReport 11, 4055-4061. (Pubitemid 32038803)
46. Iwata H, Takasusuki T, Yamaguchi S, &, Hori Y, (2007) NMDA receptor 2B subunit-mediated synaptic transmission in the superficial dorsal horn of peripheral nerve-injured neuropathic mice. Brain Res 1135, 92-101. (Pubitemid 46176831)
47. Woolf CJ, &, Salter MW, (2006) Plasticity and pain: role of the dorsal horn. In Melzack and Wall's Textbook of Pain, 5th edn (, McMahon SB, &, Koltzenburg M, eds), pp. 91-106. Elsevier, London.
48. Guo W, Wei F, Zou S, Robbins MT, Sugiyo S, Ikeda T, Tu JC, Worley PF, Dubner R, &, Ren K, (2004) Group I metabotropic glutamate receptor NMDA receptor coupling and signaling cascade mediate spinal dorsal horn NMDA receptor 2B tyrosine phosphorylation associated with inflammatory hyperalgesia. J Neurosci 24, 9161-9173. (Pubitemid 39372260)
49. Abe T, Matsumura S, Katano T, Mabuchi T, Takagi K, Xu L, Yamamoto A, Hattori K, Yagi T, Watanabe M, et al. (2005) Fyn kinase-mediated phosphorylation of NMDA receptor NR2B subunit at Tyr1472 is essential for maintenance of neuropathic pain. Eur J Neurosci 22, 1445-1454. (Pubitemid 41442416)
50. Katsura H, Obata K, Mizushima T, Sakurai J, Kobayashi K, Yamanaka H, Dai Y, Fukuoka T, Sakagami M, &, Noguchi K, (2006) Activation of Src-family kinases in spinal microglia contributes to mechanical hypersensitivity after nerve injury. J Neurosci 26, 8680-8690. (Pubitemid 44319403)
51. Salter MW, Dong Y, Kalia LV, Liu XJ, &, Pitcher G, (2009) Regulation of NMDA receptors by kinases and phosphatases. In Source Biology of the NMDA Receptor (, Van Dongen AM, ed), pp. 123-148 CRC Press, Boca Raton, USA.
52. Tsuda M, Tozaki-Saitoh H, Masuda T, Toyomitsu E, Tezuka T, Yamamoto T, &, Inoue K, (2008) Lyn tyrosine kinase is required for P2X(4) receptor upregulation and neuropathic pain after peripheral nerve injury. Glia 56, 50-58. (Pubitemid 350172730)
53. Battaglia AA, Sehayek K, Grist J, McMahon SB, &, Gavazzi I, (2003) EphB receptors and ephrin-B ligands regulate spinal sensory connectivity and modulate pain processing. Nat Neurosci 6, 339-340. (Pubitemid 36373976)
54. Kobayashi H, Kitamura T, Sekiguchi M, Homma MK, Kabuyama Y, Konno S, Kikuchi S, &, Homma Y, (2007) Involvement of EphB1 receptor/EphrinB2 ligand in neuropathic pain. Spine 32, 1592-1598. (Pubitemid 47051841)
55. Liu XJ, Gingrich JR, Vargas-Caballero M, Dong YN, Sengar A, Beggs S, Wang SH, Ding HK, Frankland PW, &, Salter MW, (2008) Treatment of inflammatory and neuropathic pain by uncoupling Src from the NMDA receptor complex. Nat Med 14, 1325-1332.
56. Gogos JA, &, Gerber DJ, (2006) Schizophrenia susceptibility genes: emergence of positional candidates and future directions. Trends Pharmacol Sci 27, 226-233.
57. Cardno AG, Sham PC, Murray RM, &, McGuffin P, (2001) Twin study of symptom dimensions in psychoses. Br J Psychiatry 179, 39-45.
58. Balu DT, &, Coyle JT, (2011) Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Rev 35, 848-870.
59. Lindsley CW, Shipe WD, Wolkenberg SE, Theberge CR, Williams DL Jr, Sur C, &, Kinney GG, (2006) Progress towards validating the NMDA receptor hypofunction hypothesis of schizophrenia. Curr Top Med Chem 6, 771-785.
60. Hahn CG, Wang HY, Cho DS, Talbot K, Gur RE, Berrettini WH, Bakshi K, Kamins J, Borgmann-Winter KE, Siegel SJ, et al. (2006) Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nat Med 12, 824-828. (Pubitemid 44050073)
61. Banerjee A, Macdonald ML, Borgmann-Winter KE, &, Hahn CG, (2010) Neuregulin 1-erbB4 pathway in schizophrenia: from genes to an interactome. Brain Res Bull 83, 132-139.
62. Chong VZ, Thompson M, Beltaifa S, Webster MJ, Law AJ, &, Weickert CS, (2008) Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr Res 100, 270-280.
63. Law AJ, Lipska BK, Weickert CS, Hyde TM, Straub RE, Hashimoto R, Harrison PJ, Kleinman JE, &, Weinberger DR, (2006) Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPs associated with the disease. Proc Natl Acad Sci USA 103, 6747-6752.
64. Deakin IH, Law AJ, Oliver PL, Schwab MH, Nave KA, Harrison PJ, &, Bannerman DM, (2009) Behavioural characterization of neuregulin 1 type I overexpressing transgenic mice. NeuroReport 20, 1523-1528.
65. Huang YZ, Won S, Ali DW, Wang Q, Tanowitz M, Du QS, Pelkey KA, Yang DJ, Xiong WC, Salter MW, et al. (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26, 443-455.
66. Pitcher GM, Beggs S, Woo RS, Mei L, &, Salter MW, (2008) ErbB4 is a suppressor of long-term potentiation in the adult hippocampus. NeuroReport 19, 139-143.
67. Kwon OB, Paredes D, Gonzalez CM, Neddens J, Hernandez L, Vullhorst D, &, Buonanno A, (2008) Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proc Natl Acad Sci USA 105, 15587-15592.
68. Eilam R, Pinkas-Kramarski R, Ratzkin BJ, Segal M, &, Yarden Y, (1998) Activity-dependent regulation of Neu differentiation factor/neuregulin expression in rat brain. Proc Natl Acad Sci USA 95, 1888-1893. (Pubitemid 28103489)
69. Uhlhaas PJ, Haenschel C, Nikolic D, &, Singer W, (2008) The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr Bull 34, 927-943.