The role of extracellular regulated kinases I/II in late-phase long-term potentiation

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5432-5441

  Rosenblum, Kobi ^a,b   Futter, Marie ^a,c   Voss, Karen ^a   Erent, Muriel ^a,d   Skehel, Paul A ^a,e   French, Pim ^a,f   Obosi, Louis ^a   Jones, Matt W ^a,g   Bliss, Tim V P ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF HAIFA   (Israel)

^c ROCKEFELLER UNIVERSITY   (United States)

^d MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^g MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Brain derived neurotrophic factor; Enhanced green fluorescent protein; Hippocampus; Immediate early genes; Long term potentiation; Mitogen activated protein kinase; Zif268

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUROTROPHIC FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL NUCLEUS; CELL STRAIN; CELLULAR DISTRIBUTION; CYTOPLASM; DENTATE GYRUS; ENZYME ACTIVITY; HIPPOCAMPUS; IMMEDIATE EARLY GENE; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; TRANSCRIPTION INITIATION; UPREGULATION;

EID: 0036662773     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05432.2002     Document Type: Article

References (61)

1. Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD (2000) The A-type potassium channel kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem 75:2277-2287.
2. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
3. Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol (Lond) 492:479-493.
4. Bailey CH, Kaang BK, Chen M, Martin KC, Lim CS, Casadio A, Kandel ER (1997) Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18:913-924.
5. Berman DE, Hazvi S, Rosenblum K, Seger R, Dudai Y (1998) Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J Neurosci 18:10037-10044.
6. Bliss TV, Collingridge GL (1993) A synaptic model of memory: Longterm potentiation in the hippocampus. Nature 361:31-39.
7. Blum S, Moore AN, Adams F, Dash PK (1999) A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J Neurosci 19:3535-3544.
8. Boglari G, Erhardt P, Cooper GM, Szeberenyi J (1998) Intact Ras function is required for sustained activation and nuclear translocation of extracellular signal-regulated kinases in nerve growth factor-stimulated PC12 cells. Eur J Cell Biol 75:54-58.
9. Brunet A, Roux D, Lenormand P, Dowd S, Keyse S, Pouyssegur J (1999) Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J 18:664-674.
10. Burnette WN (1981) "Western blotting": Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112:195-203.
11. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
12. Crow T, Xue-Bian JJ, Siddiqi V, Kang Y, Neary JT (1998) Phosphorylation of mitogen-activated protein kinase by one-trial and multi-trial classical conditioning. J Neurosci 18:3480-3487.
13. Davis HP, Squire LR (1984) Protein synthesis and memory: A review. Psychol Bull 96:518-559.
14. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20:4563-4572.
15. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
16. Fanger GR (1999) Regulation of the MAPK family members: Role of subcellular localization and architectural organization. Histol Histopathol 14:887-894.
17. Ferrell JE (1998) How regulated protein translation can produce switch-like responses. Trends Biochem Sci 23:461-465.
18. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
19. Frey U, Morris RG (1998) Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181-188.
20. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
21. Frodin M, Gammeltoft S (1999) Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol 151:65-77.
22. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA (2000) Inhibition of activity-dependent are protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20:3993-4001.
23. Hanse E, Gustafsson B (1994) TEA elicits two distinct potentiations of synaptic transmission in the CA1 region of the hippocampal slice. J Neurosci 8:5028-5034.
24. Hodge C, Liao J, Stofega M, Guan K, Carter-Su C, Schwartz J (1998) Growth hormone stimulates phosphorylation and activation of elk-1 and expression of c-fos, egr-1, and junB through activation of extracellular signal-regulated kinases 1 and 2. J Biol Chem 273:31327-31336.
25. Houpt TA, Berlin R (1999) Rapid, labile, and protein synthesis-independent short-term memory in conditioned taste aversion. Learn Mem 6:37-46.
26. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
27. Jankowsky JL, Patterson PH (1999) Cytokine and growth factor involvement in long-term potentiation. Mol Cell Neurosci 14:273-286.
28. Jones PG, Curtis CA, Hulme EC (1995) The function of a highly-conserved arginine residue in activation of the muscarinic M1 receptor. Eur J Pharmacol 288:251-257.
29. Jones MW, French PJ, Bliss TV, Rosenblum K (1999) Molecular mechanisms of long-term potentiation in the insular cortex in vivo. J Neurosci 19:RC36(1-8).
30. Jones MW, Errington ML, French PJ, Fine A, Bliss TVP, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2000) A requirement for the immediate early gene Zif268 in the expression of late LTP, the consolidation of long-term memories. Nat Neurosci 4:289-296.
31. Jovanovic JN, Czernik AJ, Fienberg AA, Greengard P, Sihra TS (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 3:323-329.
32. Kang H, Schuman EM (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
33. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
34. Kato A, Ozawa F, Saitoh Y, Hirai K, Inokuchi K (1997) Vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis. FEBS Lett 412:183-189.
35. Kohrmann M, Haubensak W, Hemraj I, Kaether C, Lessmann VJ, Kiebler MA (1999) Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J Neurosci Res 58:831-835.
36. Korte M, Kang H, Bonhoeffer T, Schuman E (1998) A role for BDNF in the late phase of hippocampal long-term potentiation. Neuropharmacology 37:553-559.
37. Kumahara E, Ebihara T, Saffen D (1999) Nerve growth factor induces zif268 gene expression via MAPK-dependent and -independent pathways in PC12D cells. J Biochem 125:541-553.
38. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T. Nature 227:680-685.
39. Malgaroli A, Tsien RW (1992) Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357:134-139.
40. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
41. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
42. Messaoudi E, Bardsen K, Srebro B, Bramham CR (1998) Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J Neurophysiol 79:496-499.
43. Messaoudi E, Croll SD, Bramham CR (2000) Characterization of BDNF-induced long-term potentiation in the rat dentate gyrus. Soc Neurosci Abstr 26:247.
44. Minichiello L, Korte M, Wolfer D, Kuhn R, Unsicker K, Cestari V, Rossi-Arnaud C, Lipp HP, Bonhoeffer T, Klein R (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24:401-414.
45. Nakamura T, Sanokawa R, Sasaki Y, Ayusawa D, Oishi M, Mori N (1996) N-Shc: A neural-specific adapter molecule that mediates signaling from neurotrophin/Trk to Ras/MAPK pathway. Oncogene 13:111-119.
46. Ortiz J, Harris HW, Guitart X, Terwilliger RZ, Haycock JW, Nestler EJ (1995) Extracellular signal-regulated protein kinases (ERKs) and ERK kinase (MEK) in brain: Regional distribution and regulation by chronic morphine. J Neurosci 15:1285-1297.
47. Otani S, Abraham WC (1989) Inhibition of protein synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats. Neurosci Lett 106:175-180.
48. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140.
49. Pizzorusso T, Ratto GM, Putignano E, Maffei L (2000) Brain-derived neurotrophic factor causes cAMP response element-binding protein phosphorylation in absence of calcium increases in slices and cultured neurons from rat visual cortex. J Neurosci 20:2809-2816.
50. Roberts LA, Higgins MJ, O'Shaughnessy CT, Stone TW, Morris BJ (1996) Changes in hippocampal gene expression associated with the induction of long-term potentiation. Brain Res Mol Brain Res 42:123-127.
51. Robinson MJ, Harkins PC, Zhang J, Baer R, Haycock JW, Cobb MH, Goldsmith EJ (1996) Mutation of position 52 in ERK2 creates a non-productive binding mode for adenosine 5′-triphosphate. Biochemistry 35:5641-5646.
52. Rosenblum K, Meiri N, Dudai Y (1993) Taste memory: The role of protein synthesis in gustatory cortex. Behav Neural Biol 59:49-56.
53. Rosenblum K, Futter M, Jones M, Hulme EC, Bliss TVP (2000) ERKI/II regulation by the muscarinic acetylcholine receptors in neurons. J Neurosci 20:977-985.
54. Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368-379.
55. Schuman EM (1999) Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 9:105-109.
56. Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9:726-735.
57. Thomson S, Mahadevan LC, Clayton AL (1999) MAP kinase-mediated signalling to nucleosomes and immediate-early gene induction. Semin Cell Dev Biol 10:205-214.
58. Walz R, Roesler R, Quevedo J, Sant'Anna MK, Madruga M, Rodrigues C, Gottfried C, Medina JH, Izquierdo I (2000) Time-dependent impairment of inhibitory avoidance retention in rats by posttraining infusion of a mitogen-activated protein kinase kinase inhibitor into cortical and limbic structures. Neurobiol Learn Mem 73:11-20.
59. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
60. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TV, Hunt SP (1990) Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4:603-614.
61. Ying SW, Futter M, Rosenblum K, Webber M, Hunt SP, Bliss TVP, Bramham CR (2002) BDNF induces LTP in intact adult hippocampus: Requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532-1540.