Rapamycin-sensitive signalling in long-term consolidation of auditory cortex-dependent memory

European Journal of Neuroscience

Volumn 18, Issue 4, 2003, Pages 942-950

  Tischmeyer, Wolfgang ^a   Schicknick, Horst ^a,b   Kraus, Michaela ^a   Seidenbecher, Constanze I ^a   Staak, Sabine ^a   Scheich, Henning ^a   Gundelfinger, Eckart D ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b FAN GmbH   (Germany)

Author keywords

Brain; Gerbil; Learning; Mammalian target of rapamycin (mTOR); Translation

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; PROTEIN SYNTHESIS INHIBITOR; RAPAMYCIN; TACROLIMUS; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY DISCRIMINATION; BRAIN; BRAIN CORTEX; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; DRUG SENSITIVITY; FREQUENCY DISCRIMINATION; FREQUENCY MODULATION; GERBIL; LEARNING; LONG TERM MEMORY; MALE; MAMMAL CELL; MEMORY CONSOLIDATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRAINING;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; CONDITIONING, CLASSICAL; DISCRIMINATION LEARNING; GERBILLINAE; IMMUNOSUPPRESSIVE AGENTS; INJECTIONS, INTRAVENTRICULAR; MALE; MEMORY; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TACROLIMUS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 0041817635     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02820.x     Document Type: Article

References (57)

1. Abraham, R.T. & Wiederrecht, G.J. (1996) Immunopharmacology of rapamycin. Annu. Rev. Immunol., 14, 483-510.
2. Aitkin, L. (1990) The Auditory Cortex. Chapman & Hall, London.
3. Akirav, I. & Richter-Levin, G. (2002) Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci., 22, 9912-9921.
4. Bailey, C.H., Giustetto, M., Huang, Y.Y., Hawkins, R.D. & Kandel, E.R. (2000) Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nature Rev. Neurosci., 1, 11-20.
5. Beaumont, V., Zhong, N., Fletcher, R., Froemke, R.C. & Zucker, R.S. (2001) Phosphorylation and local presynaptic protein synthesis in calcium- and calcineurin-dependent induction of crayfish long-term facilitation. Neuron, 32, 489-501.
6. Bennett, P.C., Schmidt, L., Lawen, A., Moutsoulas, P. & Ng, K.T. (2002) Cyclosporin A, FK506 and rapamycin produce multiple, temporally distinct, effects on memory following single-trial, passive avoidance training in the chick. Brain Res., 927, 180-194.
7. Berke, J.D. & Hyman, S.E. (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron, 25, 515-532.
8. Brown, E.J., Albers, M.W., Shin, T.B., Ichikawa, K., Keith, C.T., Lane, W.S. & Schreiber, S.L. (1994) A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature, 369, 756-758.
9. Brown, E.J. & Schreiber, S.L. (1996) A signaling pathway to translational control. Cell, 86, 517-520.
10. Budinger E., Heil, P. & Scheich H. (2000a) Functional organization of auditory cortex in the Mongolian gerbil (Meriones ungulculatus). III. Anatomical subdivisions and corticocortical connections. Eur. J. Neurosci., 12, 2425-2451.
11. Budinger, E., Heil, P. & Scheich, H. (2000b) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur. J. Neurosci., 12, 2452-2474.
12. Burnett, P.E., Blackshaw, S., Lai, M.M., Qureshi, I.A., Burnett A.F., Sabatini, D.M. & Snyder, S.H. (1998) Neurabin is a synaptic protein linking p70 S6 kinase and the neuronal cytoskeleton. Proc. Natl Acad. Sci. USA, 95, 8351-8356.
13. Casadio, A., Martin, K.C., Giustetto, M., Zhu, H., Chen, M., Bartsch, D., Bailey, C.H. & Kandel, E.R. (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell, 99, 221-237.
14. Clardy, J. (1995) The chemistry of signal transduction. Proc. Natl Acad. Sci. USA, 92, 56-61.
15. Davis, H.P. & Squire, L.R. (1984) Protein synthesis and memory: a review. Psychol. Bull., 96, 518-559.
16. Edeline, J.M. (1999) Learning-induced physiological plasticity in the thalamocortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol., 57, 165-224.
17. Ehret, G. (1997) The auditory cortex. J. Comp. Physiol. [a], 181, 547-557.
18. Frankland, P.W., O'Brien, C., Ohno, M., Kirkwood, A. & Silva, A.J. (2001) Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature, 411, 309-313.
19. Galvan, V.V. & Weinberger, N.M. (2002) Long-term consolidation and retention of learning-induced tuning plasticity in the auditory cortex of the guinea pig. Neurobiol. Learn. Mem., 77, 78-108.
20. Greengard, P. (2001) The neurobiology of slow synaptic transmission. Science, 294, 1024-1030.
21. Grolleau, A., Bowman, J., Pradet-Balade, B., Puravs, E., Hanash, S., Garcia-Sanz, J.A. & Beretta, L. (2002) Global and specific translational control by rapamycin in T cells uncovered by microarrays and proteomics. J. Biol. Chem., 277, 22175-22184.
22. Hasuo, H., Matsuoka, T. & Akasu, T. (2002) Activation of presynaptic 5-hydroxytryptamine 2A receptors facilitates excitatory synaptic transmission via protein kinase C in the dorsolateral septal nucleus. J. Neurosci., 22, 7509-7517.
23. Ikegami, S. & Inokuchi, K. (2000) Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience, 98, 637-646.
24. Izquierdo, I. & McGaugh, J.L. (2000) Behavioural pharmacology and its contribution to the molecular basis of memory consolidation. Behav. Pharmacol., 11, 517-534.
25. Jacinto, E. & Hall, M.N. (2003) Tor signalling in bugs, brain and brawn. Nature Rev. Mol. Cell. Biol., 4, 117-126.
26. Jefferies, H.B., Fumagalli, S., Dennis, P.B., Reinhard, C., Pearson, R.B. & Thomas, G. (1997) Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J., 16, 3693-3704.
27. Jefferies, H.B., Reinhard, C., Kozma, S.C. & Thomas, G. (1994) Rapamycin selectively represses translation of the 'polypyrimidine tract' mRNA family. Proc. Natl Acad. Sci. USA, 91, 4441-4445.
28. Khan, A., Pepio, A.M. & Sossin, W.S. (2001) Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci., 21, 382-391.
29. Kraus, M., Schicknick, H., Wetzel, W., Ohl, F., Staak, S. & Tischmeyer, W. (2002) Memory consolidation for the discrimination of frequency-modulated tones in mongolian gerbils is sensitive to protein-synthesis inhibitors applied to the auditory cortex. Learn. Mem., 9, 293-303.
30. Lee, F.J.S., Xue, S., Pei, L., Vukusic, B., Chéry, N., Wang, Y., Wang, Y.T. & Niznik, H.B., Yu, X. & Liu, F. (2002) Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine D1 receptor. Cell, 111, 219-230.
31. Malleret, G., Haditsch, U., Genoux, D., Jones, M.W., Bliss, T.V., Vanhoose, A.M., Weitlauf, C., Kandel, E.R., Winder, D.G. & Mansuy, I.M. (2001) Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell, 104, 675-686.
32. Martin, S.J., Grimwood, P.D. & Morris, R.G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci., 23, 649-711.
33. Matthies, H. (1989) In search of cellular mechanisms of memory. Prog. Neurobiol., 32, 277-349.
34. McGaugh, J.L. (2000) Memory - a century of consolidation. Science, 287, 248-251.
35. Moser, P.C., Bergis, O.E., Jegham, S., Lochead, A., Duconseille, E., Terranova, J.P., Caille, D., Berque-Bestel, I., Lezoualc'h, F., Fischmeister, R., Dumuis, A., Bockaert, J., George, P., Soubrie, P. & Scatton, B. (2002) SL65.0155, a novel 5-hydroxytryptamine (4) receptor partial agonist with potent cognition-enhancing properties. J. Pharmacol. Exp. Ther., 302, 731-741.
36. Ohl, F.W., Scheich, H. & Freeman, W.J. (2001) Change in pattern of ongoing cortical activity with auditory category learning. Nature, 412, 733-736.
37. Ohl, F.W., Wetzel, W., Wagner, T., Rech, A. & Scheich, H. (1999) Bilateral ablation of auditory cortex in Mongolian gerbil affects discrimination of frequency modulated tones but not of pure tones. Learn. Mem., 6, 347-362.
38. Ostroff, L.E., Fiala, J.C., Allwardt, B. & Harris, K.M. (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron, 35, 535-545.
39. Perroy, J., El Far, O., Bertaso, F., Pin, J.P., Betz, H., Bockaert, J. & Fagni, L. (2002) PICK1 is required for the control of synaptic transmission by the metabotropic glutamate receptor 7. EMBO J., 21, 2990-2999.
40. Quevedo, C., Salinas, M. & Alcazar, A. (2002) Regulation of cap-dependent translation by insulin-like growth factor-1 in neuronal cells. Biochem. Biophys. Res. Commun., 291, 560-566.
41. Raught, B., Gingras, A.C. & Sonenberg, N. (2001) The target of rapamycin (TOR) proteins. Proc. Natl Acad. Sci. USA, 98, 7037-7044.
42. Raymond, C.R., Redman, S.J. & Crouch, M.F. (2002) The phosphoinositide 3-kinase and p70 S6 kinase regulate long-term potentiation in hippocampal neurons. Neuroscience, 109, 531-536.
43. Rose, S.P. (2000) God's organism? The chick as a model system for memory studies. Learn Mem, 7, 1-17.
44. Rosenblum, K., Futter, M., Jones, M., Hulme, E.C. & Bliss, T.V. (2000) ERKI/II regulation by the muscarinic acetylcholine receptors in neurons. J. Neurosci., 20, 977-985.
45. Sabatini, D.M., Erdjument-Bromage, H., Lui, M., Tempst, P. & Snyder, S.H. (1994) RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell, 78, 35-43.
46. Sabatini, D.M., Lai, M.M. & Snyder, S.H. (1997) Neural roles of immunophilins and their ligands. Mol. Neurobiol., 15, 223-239.
47. Scheich, H. (1991) Auditory cortex: comparative aspects of maps and plasticity. Curr. Opin. Neurobiol., 1, 236-247.
48. Scheich, H., Stark, H., Zuschratter, W., Ohl, F.W. & Simonis, C.E. (1997) Some functions of primary auditory cortex in learning and memory formation. Adv. Neurol., 73, 179-193.
49. Stark, H., Bischof, A., Wagner, T. & Scheich, H. (2001) Activation of the dopaminergic system of medial prefrontal cortex of gerbils during formation of relevant associations for the avoidance strategy in the shuttle-box. Prog. Neuropsychopharmacol. Biol. Psychiatry, 25, 409-426.
50. Stark, H. & Scheich, H. (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J. Neurochem., 68, 691-697.
51. Steward, O. & Schuman, E.M. (2001) Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci., 24, 299-325.
52. Stork, O. & Welzl, H. (1999) Memory formation and the regulation of gene expression. Cell. Mol. Life Sci., 55, 575-592.
53. Takei, N., Kawamura, M., Hara, K., Yonezawa, K. & Nawa, H. (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J. Biol. Chem., 276, 42818-42825.
54. Tang, S.J., Reis, G., Kang, H., Gingras, A.C., Sonenberg, N. & Schuman, E.M. (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl Acad. Sci. USA, 99, 467-472.
55. Weinberger, N.M. (1995) Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annu. Rev. Neurosci., 18, 129-158.
56. Yanow, S.K., Manseau, F., Hislop, J., Castellucci, V.F. & Sossin, W.S. (1998) Biochemical pathways by which serotonin regulates translation in the nervous system of Aplysia. J. Neurochem., 70, 572-583.
57. Zeng, H., Chattarji, S., Barbarosie, M., Rondi-Reig, L., Philpot, B.D., Miyakawa, T., Bear, M.F. & Tonegawa, S. (2001) Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell, 107, 617-629.