Glutamate signaling to Ras-MAPK in striatal neurons: Mechanisms for inducible gene expression and plasticity

Molecular Neurobiology

Volumn 29, Issue 1, 2004, Pages 1-14

  Wang, John Q ^a   Tang, Qingsong ^a   Parelkar, Nikhil K ^a   Liu, Zhenguo ^a   Samdani, Shazia ^a   Eun, Sang Choe ^a   Yang, Lu ^a   Mao, Limin ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

ERK; fos; JNK; MAPK; mGluR; NMDA; Nucleus accumbens; p38; PI3 kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; AMPA RECEPTOR; AMPHETAMINE; CALCIUM; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 1 RECEPTOR; EGLUMETAD; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; GLUTAMIC ACID; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN FOS; PROTEIN KINASE (CALCIUM,CALMODULIN) II; RAS PROTEIN; SL 327; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ELK 1; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ASSOCIATIVE MEMORY; CALCIUM TRANSPORT; CORPUS STRIATUM; DRUG ABUSE; DRUG ANTAGONISM; DRUG DEPENDENCE; DRUG EXPOSURE; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HUMAN; LONG TERM POTENTIATION; MAMMAL; MEMORY DISORDER; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; ANIMAL; METABOLISM; NEOSTRIATUM; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOSTRIATUM; NEURONAL PLASTICITY; NEURONS; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 2542439782     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1385/mn:29:1:01     Document Type: Review

References (97)

1. Greenamyre J. T. and Porter R. H. (1994) Anatomy and physiology of glutamate in the CNS. Neurology 44, S7-S13.
2. Michaelis E. K. (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54, 369-415.
3. Schoepfer R., Monyer H., Sommer B., et al. (1994) Molecular biology of glutamate receptors. Prog. Neurobiol. 42, 353-357.
4. Ozawa S., Kamiya H., and Tsuzuki K. (1998) Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 54, 581-618.
5. Conn P. J. and Pin J. P. (1997) Pharmacology and function of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237.
6. Ascher P. and Nowak L. (1987) Electrophysiological studies of NMDA receptors. Trends Neurosci. 10, 284-287.
7. MacDermott A. B., Mayer M. L., Westbrook G. L., Smith S. J., and Barker J. L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature 321, 519-522.
8. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
9. Peyssonnaux C. and Eychene A. (2001) The Raf/MEK/ERK pathway: new concepts of activation. Biol. Cell. 93, 53-62.
10. Volmat V. and Pouyssegur J. (2001) Spatiotemporal regulation of the p42/p44 MAPK pathway. Biol. Cell. 93, 71-79.
11. Ray L. B. and Sturgill T. W. (1987) Rapid stimulation by insulin of a serine/threonine kinase in 3T3-L1 adipocytes that phosphorylates microtubule-associated protein 2 in vitro. Proc. Natl. Acad. Sci. USA 84, 1502-1506.
12. Lee J. D., Ulevitch R. J., and Han J. (1995) Primary structure of BMK1: a new mammalian map kinase. Biochem. Biophys. Res. Commun. 213, 715-724.
13. Thiels E. and Klann E. (2001) Extracellular signal-regulated kinase, synaptic plasticity, and memory. Rev. Neurosci. 12, 327-345.
14. Gallo K. A. and Johnson G. L. (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell. Biol. 3, 663-672.
15. Pearson G., Robinson F., Beers Gibson T., Xu B. E., Karandikar M., Berman K., and Cobb M. H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183.
16. Wang J. Q., Mao L., Parelkar N. K., Tang Q., and Choe E. S. (2003) Glutamate-regulated behavior, transmitter release, gene expression and addictive plasticity in the striatum: roles of metabotropic glutamate receptors. Curr. Neuropharmacol. 1, 1-20.
17. Mao L., Tang Q., Samdani S., Liu Z., and Wang J. Q. (2004) Regulation of MAPK/ERK phosphorylation via ionotropic glutamate receptors in cultured rat striatal neurons. Eur. J. Neurosci. (In press.)
18. Vanhoutte P., Barnier J. V., Guibert B., Pages C., Besson M. J., Hipskind R. A., and Caboche J. (1999) Glutamate induces phosphorylation of Elk-1 and CREB, along with c-fos activation, via an extracellular signal-regulated kinase-dependent pathway in brain slices. Mol. Cell. Biol. 19, 136-146.
19. Schwarzschild M. A., Cole R. L., Meyers M. A., and Hyman S. E. (1999) Contrasting calcium dependencies of SAPK and ERK activation by glutamate in cultured striatal neurons. J. Neurochem. 72, 2248-2255.
20. Sgambato V., Vanhoutte P., Pages C., Rogard M., Hipskind R., Besson M. J., and Caboche J. (1998) In vivo expression and regulation of Elk-1, a target of the extracellular-regulated kinase signaling pathway, in the adult rat brain. J. Neurosci. 18, 214-226.
21. Sgambato V., Pages C., Rogard M., Besson M. J., and Caboche J. (1998) Extracellular signal-regulated kinase controls immediate early gene induction on corticostriatal stimulation. J. Neurosci. 18, 8814-8825.
22. Vincent S. R., Sebben M., Dumuis A., and Bockaert J. (1998) Neurotransmitter regulation of MAP kinase signaling in striatal neurons in primary culture. Synapse 29, 29-36.
23. English J. D. and Sweatt J. D. (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 272, 24,329-24,332.
24. English J. D. and Sweatt J. D. (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem. 272, 19,103-19,106.
25. Xia Z., Dudek H., Miranti C. K., and Greenberg M. E. (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16, 5425-5436.
26. Fuller G., Veitch K., Ho L. K., Cruise L., and Morris B. J. (2001) Activation of p44/p42 MAP kinase in striatal neurons via kainate receptors and P13 kinase. Mol. Brain Res. 89, 126-132.
27. Perkinton M. S., Ip J. K., Wood G. L., Crossthwaite A. J., and Williams R. J. (2002) Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurons. J. Neurochem. 80, 239-254.
28. Kurino M., Fukunaga K., Ushio Y., and Miyamoto E. (1995) Activation of mitogen-activated protein kinase in cultured rat hippocampal neurons by stimulation of glutamate receptors. J. Neurochem. 65, 1282-1289.
29. 2+-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J. Neurosci. 19, 5861-5874.
30. Williams R. J. and Glowinski J. (1996) Cyclothiazide unmasks an AMPA-evoked release of arachidonic acid from cultured striatal neurons. J. Neurochem. 67, 1551-1558.
31. Luttrell L. M. (2002) Activation and targeting of mitogen-activated protein kinases by G-protein-coupled receptors. Can. J. Physiol. Pharmacol. 80, 375-382.
32. Choe E. S. and Wang J. Q. (2001) Group I metabotropic glutamate receptor activation increases phosphorylation of cAMP response element-binding protein, Elk-1 and extracellular signal-regulated kinases in rat dorsal striatum. Mol. Brain Res. 94, 75-84.
33. Fiore R. S., Murphy T. H., Sanghera J. S., Pelech S. L., and Baraban J. M. (1993) Activation of p42 mitogen-activated protein kinase by glutamate receptor stimulation in rat primary cortical cultures. J. Neurochem. 61, 1626-1633.
34. Peavy R. D. and Conn P. J. (1998) Phosphorylation of mitogen-activated protein kinase in cultured rat cortical glia by stimulation of metabotropic glutamate receptors. J. Neurochem. 71, 603-612.
35. Iacovelli L., Bruno V., Salvatore L., et al. (2002) Native group-III metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/phosphatidylinositol-3-kinase pathways. J. Neurochem. 82, 216-223.
36. Calabresi P., Saulle E., Marfia G. A., et al. (2001) Activation of metabotropic glutamate receptor subtype 1/protein kinase C/mitogen-activated protein kinase pathway is required for postischemic long-term potentiation in the striatum. Mol. Pharmacol. 60, 808-815.
37. D'Onofrio M., Cuomo L., Battaglia G., et al. (2001) Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidylinositol-3-kinase pathways. J. Neurochem. 78, 435-445.
38. Ferraguti F., Baldani-Guerra B., Corsi M., Nakanishi S., and Corti C. (1999) Activation of the extracellular signal-regulated kinase 2 by metabotropic glutamate receptors. Eur. J. Neurosci. 11, 2073-2082.
39. Phillips T., Barnes A., Scott S., Emson P., and Rees S. (1998) Human metabotropic glutamate receptor 2 couples to the MAP kinase cascade in chinese hamster ovary cells. Neuroreport 13, 2335-2339.
40. Mukherjee P. K., DeCoster M. A., Campbell F. Z., Davis R. J., and Bazan N. G. (1999) Glutamate receptor signaling interplay modulates stress-sensitive mitogen-activated protein kinases and neuronal cell death. J. Biol. Chem. 274, 6493-6498.
41. Kawasaki H., Morooka T., Shimohama S., Kimura J., Hirano T., Gotoh Y., and Nishida E. (1997) Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J. Biol. Chem. 272, 18,518-18,521.
42. Chen R. W., Qin Z. H., Ren M., Kanai H., Chalecka-Franaszek E., Leeds P., and Chuang D. M. (2003) Regulation of c-Jun N-terminal kinase, p38 kinase and AP-1 DNA binding in cultured brain neurons: roles in glutamate excitotoxicity and lithium neuroprotection. J. Neurochem. 84, 566-575.
43. Jeon S. H., Kim Y. S., Bae C. D., and Park J. B. (2000) Activation of JNK and p38 in rat hippocampus after kainic acid induced seizure. Exp. Mol. Med. 32, 227-230.
44. Ferrer I., Blanco R., and Carmona M. (2001) Differential expression of active, phosphorylation-dependent MAP kinases, MAPK/ERK, SAPK/JNK and p38, and specific transcription factor substrates following quinolinic acid excitotoxicity in the rat. Mol. Brain Res. 94, 48-58.
45. Schwarzschild M. A., Cole R. L., and Hyman S. E. (1997) Glutamate, but not dopamine, stimulates stress-activated protein kinase and AP-1-mediated transcription in striatal neurons. J. Neurosci. 17, 3455-3466.
46. Tang Q., Mao L., Samdani S., and Wang J. Q. (2004) NMDA receptor signaling to extracellular signal-regulated protein kinase phosphorylation in cultured rat striatal neurons. submitted.
47. Wymann M. P. and Pirola L. (1998) Structure and function of phosphoinositide 3-kinase. Biochem. Biophys. Acta 1436, 127-150.
48. Shin B. C., Suzuki M., Inukai K., Anai M., Asano T., and Takata K. (1998) Multiple isoforms of the regulatory subunit for phosphatidylinositol 3-kinase (PI3-kinase) are expressed in neurons in the rat brain. Biochem. Biophys. Res. Comm. 246, 313-319.
49. Bernstein H. G., Keilhoff C., Reiser M., Freese S., and Wetzker R. (1998) Tissue distribution and subcellular localization of a G-protein activated phosphoinositide 3-kinase, An immunohistochemical study. Cell. Mol. Biol. 44, 973-983.
50. Joyal J. L., Burks D. J., Pons S., Matter W. F., Vlahos C. J., White M. F., and Sacks D. B. (1997) Calmodulin activates phosphatidylinositol 3-kinase. J. Biol. Chem. 272, 28,183-28,186.
51. Fischer R., Julsgart J., and Berchtold M. W. (1998) High affinity calmodulin target sequence in the signaling molecule PI 3-kinase. FEBS Lett. 425, 175-177.
52. Chan T. O., Rittenhouse S. E., and Tsichlis P. N. (1999) AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Ann. Rev. Biochem. 68, 965-1014.
53. Datta S. R., Brunet A., and Greenberg M. E. (1999) Cellular survival: a paly in three Akts. Genes Dev. 13, 2905-2927.
54. Yart A., Roche S., Wetzker R., Laffargue M., Tonks N., Mayeux P., Chap H., and Raynal P. (2002) A function for phosphoinositide 3-kinase beta lipid products in coupling beta gamma to Ras activation in response to lysophosphatidic acid. J. Biol. Chem. 277, 21,167-21,178.
55. Bondeva T., Pirola L., Bulgarelli-Leva G., Rubio I., Wetzker R., and Wymann M. P. (1998) Bifurcation of lipid and protein kinase signals of PI3Kgamma to the protein kinases PKB and MAPK. Science 282, 293-296.
56. Hu Q. J., Klippel A., Muslin A. J., Fantl W. J., and Williams L. T. (1995) Ras-dependent induction of cellular-responses by constitutively active phosphatidylinositol-3 kinase. Science 268, 100-102.
57. Pandey S. K., Theberge J. F., Bernier M., and Srivastava A. K. (1999) Phosphatidylinositol 3-kinase requirement in activation of the ras/C-raf-1/MEK/ERK and p70(s6k) signaling cascade by the insulinomimetic agent vanadyl sulfate. Biochemistry 38, 14,667-14,675.
58. Rodrigues-Viciana P., Warne P. H., Dhand R., et al. (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370, 527-532.
59. Winkler D. G., Johnson J. C., Cooper J. A., and Vojtek A. B. (1997) Identification and characterization of mutations in Ha-Ras that selectively decrease binding to cRaf-1. J. Biol. Chem. 272, 24,402-24,409.
60. Osada M., Tolkacheva T., Li W., Chan T. O., Tsichlis P. N., Saez R., Kimmelman A. C., and Chan A. M. (1999) Differential roles of Akt, Rac, and Ral in R-Ras-mediated cellular transformation, adhesion, and survival. Mol. Cell. Biol. 19, 6333-6344.
61. Xue L., Murray J. H., and Tolkovsky A. M. (2000) The Ras/ phosphatidylinositol 3-kinase and Ras/ERK pathways function as independent survival modules each of which inhibits distinct apoptotic signaling pathway in sympathetic neurons. J. Biol. Chem. 275, 8817-8824.
62. Suga J., Yoshimasa Y., Yamada K., et al. (1997) Differential activation of mitogen-activated protein kinase by insulin and epidermal growth factor in 3T3-L1 adipocytes: a possible involvement of PI3-kinase in the activation of the MAP kinase by insulin. Diabetes 46, 735-741.
63. Li J., Yen C., Liaw D., et al. (1997) PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275, 1943-1947.
64. Steck P. A., Pershouse M. A., Jasser S. A., et al. (1997) Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 15, 356-362.
65. Myers M. P., Stolarov J. P., Eng C., Li J., Wang S. I., Wigler M. H., Parsons R., and Tonks N. K. (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. USA 94, 9052-9057.
66. Maehama T. and Dixon J. E. (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-triphosphate. J. Biol. Chem. 273, 13,375-13,378.
67. Lachyankar M. B., Sultana N., Schonhoff C. M., et al. (2000) A role for nuclear PTEN in neuronal differentiation. J. Neurosci. 20, 1404-1413.
68. Gu J., Tamura M., and Yamada K. M. (1998) Tumor suppressor PTEN inhibits integrin- and growth factor-mediated mitogen-activated protein (MAP) kinase signaling pathways. J. Cell. Biol. 143, 1375-1383.
69. 2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity. Neuron 16, 233-236.
70. 2+, and calmodulin. Cell. Signal. 14, 649-654.
71. Choe E. S. and Wang J. Q. (2001) Group I metabotropic glutamate receptors control phosphorylation of CREB, Elk-1 and ERK via a CaMKII-dependent pathway in rat striatum. Neurosci. Lett. 313, 129-132.
72. Peavy R. D., Chang M. S., Sanders-Bush E., and Conn P. J. (2001) Metabotropic glutamate receptor 5-induced phosphorylation of extracellular signal-regulated kinase in astrocytes depends on transactivation of the epidermal growth factor receptor. J. Neurosci. 21, 9619-9628.
73. Hazzalin C. A. and Mahadevan L. C. (2002) MAPK-regulated transcription: a continuously variable gene switch? Nat. Rev. Mol. Cell. Biol. 3, 30-40.
74. Valjent E., Caboche J., and Vanhoutte P. (2001) Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain: a molecular substrate for learning and memory? Mol. Neurobiol. 23, 83-99.
75. Li R., Pei H., and Watson D. K. (2000) Regulation of Ets function by protein-protein interactions. Oncogene 19, 6514-6523.
76. Sharrocks A. D. (2001) The ETS-domain transcription factor family. Nat. Rev. Mol. Cell. Biol. 2, 827-837.
77. Yordy J. S. and Muise-Helmericks R. C. (2000) Signal transduction and the Ets family of transcription factors. Oncogene 19, 6503-6513.
78. Hipskind R. A., Rao V. N., Mueller C. G. F., Reddy E. S. P., and Nordheim A. (1991) Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF. Nature 354, 531-534.
79. Dalton S. and Treisman R. (1992) Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum element. Cell 68, 597-612.
80. Giovane A., Pintzas A., Maira S. M., Sobieszczuk P., and Wasylyk B. (1994) Net, a new ets transcription factor that is activated by ras. Genes. Dev. 8, 1502-1513.
81. Lopez M., Oettgen P., Akbarali Y., Dendorfer U., and Liberman T. A. (1994) ERP, a new member of the ets transcription factor/oncoprotein family: cloning, characterization and differential expression during B-cell development. Mol. Cell. Biol. 14, 3292-3309.
82. Gille H., Sharrocks A. D., and Shaw P. E. (1992) Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promotor. Nature 358, 414-417.
83. Gille H., Kortenjann M., Thoma O., Moomaw C., Slaughter C., Cobb M., and Shaw P. E. (1995) ERK phosphorylation potentiates Elk-1-mediated ternary complex formation and transactivation. EMBO J. 14, 951-962.
84. Mao L. and Wang J. Q. (2003) Metabotropic glutamate receptor subtype 5-regulated Elk-1 phosphorylation and immediate early gene expression in striatal neurons, J. Neurochem. 85, 1006-1017.
85. Valjent E., Corvol J. C., Pages C., Besson M. J., Maldonado R., and Caboche J. (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J. Neurosci. 20, 8701-8709.
86. Choe E. S., Chung K. T., Mao L., and Wang J. Q. (2002) Amphetamine increases phosphorylation of extracellular signal-regulated kinase and transcription factors in the rat striatum via group I metabotropic glutamate receptors. Neuropsychopharmacology 27, 565-575.
87. Berhow M. T., Hiroi N., and Nestler E. J. (1996) Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J. Neurosci. 16, 4707-4715.
88. Freeman W. M., Nader M. A., Nader S. H., et al. (2001) Chronic cocaine-mediated changes in non-human primate nucleus accumbens gene expression. J. Neurochem. 77, 542-549.
89. Choe E. S. and Wang J. Q. (2002) CaMKII regulates amphetamine-induced ERK1/2 phosphorylation in striatal neurons. NeuroReport 13, 1013-1016.
90. Pierce R. C., Pierce-Bancroft A. F., and Prasad B. M. (1999) Neurotrophin-3 contributes to the initiation of behavioral sensitization to cocaine by activating the Ras/Mitogen-activated protein kinase signal transduction cascade. J. Neurosci. 19, 8685-8695.
91. Berke J. D. and Hyman S. E. (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25, 515-532.
92. Berke J. D. (2003) Learning and memory mechanisms involved in compulsive drug use and relapse. Methods Mol. Med. 79, 75-101.
93. Boening J. A. (2001) Neurobiology of an addiction memory. J. Neural. Transm. 108, 755-765.
94. Calabresi P., Saulle E., Centonze D., Pisani A., Marfia G. A., and Bernardi G. (2002) Post-ischaemic long-term synaptic potentiation in the striatum: a putative mechanism for cell type-specific vulnerability. Brain 125, 844-860.
95. Kahn L., Alonso G., Robbe D., Bockaert J., and Manzoni O. J. (2001) Group 2 metabotropic glutamate receptors induced long term depression in mouse striatal slices. Neurosci. Lett. 316, 178-182.
96. Mazzucchelli C., Vantaggiato C., Ciamei A., et al. (2002) Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34, 807-820.
97. English J. M. and Cobb M. H. (2002) Pharmacological inhibitors of MARK pathways. Trends in Pharmacol. Sci. 23, 40-45.