Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation

Journal of Neuroscience

Volumn 20, Issue 3, 2000, Pages 969-976

  Raymond, Clarke R ^a,c   Thompson, Vida L ^a   Tate, Warren P ^a   Abraham, Wickliffe C ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b Box 56 ^*  (New Zealand)

^c Biology and Environment   (Australia)

Author keywords

Hippocampus; LTP; Metaplasticity; mGluRs; Protein synthesis; Synaptic plasticity

Indexed keywords

GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST; MESSENGER RNA; METABOTROPIC RECEPTOR; PROTEIN SYNTHESIS INHIBITOR; RECEPTOR SUBTYPE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RAT; RECEPTOR BINDING; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

EID: 0034143238     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-03-00969.2000     Document Type: Article

References (57)

1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
2. Abraham WC, Otani S (1991) Macromolecules and the maintenance of long-term potentiation. In: Kindling and synaptic plasticity. The legacy of Graham Goddard (Morrell F, ed), pp 92-109. Boston: Birkhauser.
3. Abraham WC, Tate WP (1997) Metaplasticity: a new vista across the field of synaptic plasticity. Prog Neurobiol 52:303-323.
4. Abraham WC, Demmer J, Richardson C, Williams J, Lawlor P, Mason SE, Tate WP, Dragunow M (1993) Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 56:717-727.
5. Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving A, Seal AJ, Henley JM, Jane DE, Watkins JC, Collingridge GA (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363:347-350.
6. Behnisch T, Fjodorow K, Reymann KG (1991) L-2-Amino-3-phosphonopropionate blocks late synaptic long-term potentiation. NeuroReport 2:386-388.
7. Ben-Ari Y, Anikstejn I. (1995) Role of glutamate metabotropic receptors in long-term potentiation in the hippocampus. Semin Neurosci 7:127-135.
8. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
9. Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate gyrus of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
10. Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368:740-743.
11. Bruckenstein DA, Lein PJ, Higgins D, Fremeau Jr RT (1990) Distinct spatial localisation of specific mRNAs in cultured sympathetic neurons. Neuron 5:809-819.
12. Chinestra P, Aniksztejn L, Diabira D, Ben-Ari Y (1993) (RS)-Alpha-methyl-4-carboxyphenylglycine neither prevents induction of LTP nor antagonizes metabotropic glutamate receptors in CA1 hippocampal neurons. J Neurophysiol 70:2684-2689.
13. Cohen AS, Abraham WC (1996) Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors. J Neurophysiol 76:953-962.
14. Cohen AS, Raymond CR, Abraham WC (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8:160-170.
15. Cohen AS. Coussens CM, Raymond CR, Abraham WC (1999) A long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J Neurophysiol 82:31-39.
16. Frey U, Morris RGM (1997) Synaptic lagging and long-term potentiation. Nature 385:533-536.
17. Frey U, Morris RGM (1998) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545-552.
18. Frey U, Frey S, Schollmeier F, Krug M (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in the rat hippocampus in vivo and in vitro. J Physiol (Lond) 490:703-711.
19. Gao F-B (1998) Messenger RNAs in dendrites: localization, stability, and implications for neuronal function. BioEssays 20:70-78.
20. Gardiol A, Racca C, Triller A (1999) Dendritic and postsynaptic protein synthetic machinery. J Neurosci 19:168-179.
21. Ghirardi M, Montarolo PG, Kandel ER (1995) A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14:413-420.
22. Grover LM, Teyler TJ (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347:477-479.
23. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
24. Kleiman R, Banker G, Steward O (1993) Subcellular distribution of rRNA and poly(A) RNA in hippocampal neurons in culture. Mol Brain Res 20:305-312.
25. Krug M, Lössner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
26. Linden DJ (1996) A protein synthesis-dependent late phase of cerebellar long-term depression. Neuron 17:483-490.
27. Lovinger DM, Wong K, Murakami K, Routtenberg A (1987) Protein kinase C inhibitors eliminate hippocampal long-term potentiation (LTP). Brain Res 436:177-183.
28. Lujan R, Nusser N, Roberts JDB, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488-1500.
29. Malinow R, Madison DV, Tsien RW (1988) Persistent protein kinase activity underlying long-term potentiation. Nature 335:820-824.
30. Manahan-Vaughan D, Reymann KG (1996) Metabotropic glutamate receptor subtype agonists facilitate long-term potentiation within a distinct time window in dentate gyrus in vivo. Neuroscience 74:723-731.
31. Martone WE, Pollock JA, Jones YZ, Ellisman MH (1996) Ultrastructural localization of dendritic messenger RNA in adult rat hippocampus. J Neurosci 16:7437-7446.
32. Matthies H (1989) In search of cellular mechanisms of memory. Prog Neurobiol 32:277-349.
33. Merlin LR, Bergold PJ, Wong RKS (1998) Requirement of protein synthesis for group I mGluR-mediated induction of epileptiform discharges. J Neurophysiol 80:989-993.
34. Moroni F, Lombardi G, Thomsen C, Leonardi P, Atucci S, Peruginelli F, Torregrossa SA, Pellegrini-Giampietro DE, Luniea R, Pellicciari R (1997) Pharmacological characterization of 1-aminoindan-1,5-dicarboxylic acid, a potent mGluR1 antagonist. J Pharmacol Exp Ther 281:721-729.
35. Nguyen PV, Kandel ER (1997) Brief θ-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4:230-243.
36. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
37. Otani S, Marshall CJ, Tate WP, Goddard GV, Abraham WC (1989) Maintenance of long-term potentiation in the rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization. Neuroscience 28:519-526.
38. Palmer MJ, Irving AJ, Seabrook GR, Jane DE, Collingridge GL (1997) The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 36:1517-1532.
39. Racine RJ, Milgram NW, Hafner S (1983) Long-term potentiation phenomena in the rat limbic forebrain. Brain Res 260:217-231.
40. Raymond CR, Abraham WC (1998) Priming of LTP by group I metabotropic glutamate receptors involves de novo protein synthesis. Soc Neurosci Abstr 24:1321.
41. Rowlands AG, Panniers R, Henshaw EC (1988) The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J Biol Chem 263:5526-5533.
42. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630-634.
43. Schuman EM (1997) Synapse specificity and long-term information storage. Neuron 18:339-342.
44. Selig DK, Lee H-K, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075-1082.
45. Sonenburg N (1996) mRNA 5′ cap-binding protein eIF4E and control of cell growth. In: Translational control (Hershey JWB, Mathews MB, Sonenburg N, eds), pp 245-269. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
46. Steward O (1994) Dendrites as compartments for macromolecular synthesis. Proc Natl Acad Sci USA 91:10766-10768.
47. Steward O (1997) mRNA localisation in neurons: a multipurpose mechanism? Neuron 18:9-12.
48. Steward O, Levy WB (1982) Preferential localisation of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2:284-291.
49. Thomas MJ, O'Dell TJ (1995) The molecular switch hypothesis fails to explain the inconsistent effects of the metabotropic glutamate receptor antagonist MCPG on long-term potentiation. Brain Res 695:45-52.
50. Tiedge H, Brosius J (1996) Translational machinery in dendrites of hippocampal neurons in culture. J Neurosci 16:7171-7181.
51. Tongiorgi E, Righi M, Cattaneo A (1997) Activity-dependent targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17:9492-9505.
52. Torre ER, Steward O (1996) Protein synthesis within dendrites: glycosylation of newly synthesized proteins in dendrites of hippocampal neurons in culture. J Neurosci 16:5967-5978.
53. Weiler IJ, Greenough WT (1993) Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc Natl Acad Sci USA 90:7168-7171.
54. Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, Miyashiro K, Comery TA, Patel B, Eberwine J, Greenough WT (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Natl Acad Sci USA 94:5395-5400.
55. Wilsch VW, Behnisch T, Jäger T, Reymann KG, Balschun D (1998) When are class I metabotropic glutamate receptors necessary for long-term potentiation? J Neurosci 18:6071-6080.
56. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER (1998) Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92:25-37.
57. Wu L, Wells D, Tay J, Mendis D, Abbott M-A, Barnitt A, Quinlan E, Heynen A, Fallon JR, Richter JD (1998) CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21:1129-1139.