Activation of mammalian target of rapamycin signaling in spatial learning

Neuroscience Research

Volumn 68, Issue 2, 2010, Pages 88-93

  Qi, Sihua ^a   Mizuno, Makoto ^a   Yonezawa, Kazuyoshi ^b   Nawa, Hiroyuki ^a   Takei, Nobuyuki ^a,c  

^a NIIGATA UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

4EBP; MTOR; P70S6K; Protein synthesis; Rapamycin; Translation

Indexed keywords

INITIATION FACTOR 4E BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; P70S6 KINASE; PHOSPHOTRANSFERASE; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ASSAY; GENE ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; RNA TRANSLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; CARRIER PROTEINS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMUNOSUPPRESSIVE AGENTS; LEARNING; MALE; MAZE LEARNING; PHOSPHOPROTEINS; RATS; RATS, WISTAR; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SIROLIMUS; SPACE PERCEPTION; TOR SERINE-THREONINE KINASES;

EID: 77956275001     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2010.06.008     Document Type: Article

References (45)

1. Banko J.L., Poulin F., Hou L., DeMaria C.T., Sonenberg N., Klann E. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J. Neurosci. 2005, 25:9581-9590.
2. Bekinschtein P., Katche C., Slipczuk L.N., Igaz L.M., Cammarota M., Izquierdo I., Medina J.H. mTOR signaling in the hippocampus is necessary for memory formation. Neurobiol. Learn. Mem. 2007, 87:303-307.
3. Belelovsky K., Kaphzan H., Elkobi A., Rosenblum K. Biphasic activation of the mTOR pathway in the gustatory cortex is correlated with and necessary for taste learning. J. Neurosci. 2009, 29:7424-7431.
4. Blundell J., Kouser M., Powell C.M. Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation. Neurobiol. Learn. Mem. 2008, 90:28-35.
5. Cammalleri M., Lutjens R., Berton F., King A.R., Simpson C., Francesconi W., Sanna P.P. Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14368-14373.
6. Casadio A., Martin K.C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C.H., Kandel E.R. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 1999, 99:221-237.
7. Costa-Mattioli M., Gobert D., Harding H., Herdy B., Azzi M., Bruno M., Bidinosti M., Ben Mamou C., Marcinkiewicz E., Yoshida M., Imataka H., Cuello A.C., Seidah N., Sossin W., Lacaille J.C., Ron D., Nader K., Sonenberg N. Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 2005, 436:1166-1173.
8. Costa-Mattioli M., Gobert D., Stern E., Gamache K., Colina R., Cuello C., Sossin W., Kaufman R., Pelletier J., Rosenblum K., Krnjević K., Lacaille J.C., Nader K., Sonenberg N. eIF2alpha phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory. Cell 2007, 129:195-206.
9. Costa-Mattioli M., Sossin W.S., Klann E., Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61:10-26.
10. Dash P.K., Orsi S.A., Moore A.N. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-mammalian target of rapamycin pathway. J. Neurosci. 2006, 26:8048-8056.
11. Fumagalli S., Thomas G. S6 phosphorylation and signal transduction. Translational Control in Gene Expression 2000, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp. 695-717. N. Sonenberg, J.W.B. Hershey, M.B. Mathews (Eds.).
12. Hara K., Yonezawa K., Kozlowski M.T., Sugimoto T., Andrabi K., Weng Q.P., Kasuga M., Nishimoto I., Avruch J. Regulation of eIF-4E BP1 phosphorylation by mTOR. J. Biol. Chem. 1997, 272:26457-26463.
13. Hara K., Maruki Y., Long X., Yoshino K., Oshiro N., Hidayat S., Tokunaga C., Avruch J., Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002, 110:177-189.
14. Hay N., Sonenberg N. Upstream and downstream of Mtor. Genes Dev. 2004, 18:1926-1945.
15. Helmstetter F.J., Parsons R.G., Gafford G.M. Macromolecular synthesis, distributed synaptic plasticity, and fear conditioning. Neurobiol. Learn. Mem. 2008, 89(3):324-337.
16. Hoeffer C.A., Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 2009.
17. Hou L., Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 2004, 24:6352-6361.
18. Inamura N., Hoshino S., Uchiumi T., Nawa H., Takei N. Cellular and subcellular distributions of translation initiation, elongation and release factors in rat hippocampus. Mol. Brain. Res. 2003, 111:165-174.
19. Inamura N., Nawa H., Takei N. Enhancement of translation elongation in neurons by brain-derived neurotrophic factor: implications for mammalian target of rapamycin signaling. J. Neurochem. 2005, 95:1438-1445.
20. Ishizuka Y., Kakiya N., Nawa H., Takei N. Leucine induces phosphorylation and activation of p70S6K in cortical neurons through the system l amino acid transporter. J. Neurochem. 2008, 106:934-942.
21. Isotani S., Hara K., Tokunaga C., Inoue H., Avruch J., Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J. Biol. Chem. 1999, 274:34493-34498.
22. Jacinto E., Hall M.N. Tor signalling in bugs, brain and brawn. Nat. Rev. Mol. Cell Biol. 2003, 4:117-126.
23. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
24. Kanhema T., Dagestad G., Panja D., Tiron A., Messaoudi E., Håvik B., Ying S.W., Nairn A.C., Sonenberg N., Bramham C.R. Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control. J. Neurochem. 2006, 99:1328-1337.
25. Kelleher R.J., Govindarajan A., Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 2004, 44:59-73.
26. Klann E., Dever T.E. Biochemical mechanisms for translational regulation in synaptic plasticity. Nat. Rev. Neurosci. 2004, 5:931-942.
27. Lu B. BDNF and activity-dependent synaptic modulation. Learn. Mem. 2003, 10:86-98.
28. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248-251.
29. Mizuno M., Yamada K., Olariu A., Nawa H., Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 2000, 20:7116-7121.
30. Mizuno M., Yamada K., Takei N., Tran M.H., He J., Nakajima A., Nawa H., Nabeshima T. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol. Psychiatry 2003, 8:217-224.
31. Mothe-Satney I., Gautier N., Hinault C., Lawrence J.C., Van Obberghen E. In rat hepatocytes glucagon increases mammalian target of rapamycin phosphorylation on serine 2448 but antagonizes the phosphorylation of its downstream targets induced by insulin and amino acids. J. Biol. Chem. 2004, 279:42628-42637.
32. Nawa H., Takei N. BDNF as an anterophin; a novel neurotrophic relationship between brain neurons. Trends Neurosci. 2001, 24:683-684.
33. Nishiuma T., Hara K., Tsujishita Y., Kaneko K., Shii K., Yonezawa K. Characterization of the phosphoproteins and protein kinase activity in mTOR immunoprecipitates. Biochem. Biophys. Res. Commun. 1998, 252:440-444.
34. Parsons R.G., Gafford G.M., Helmstetter F.J. Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J. Neurosci. 2006, 26:12977-12983.
35. Paxions G., Watson C. The Rat Brain in Stereotaxic Coordinates 1982, Academic Press, New York.
36. Poo M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2001, 2:24-32.
37. Richter J.D., Klann E. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 2009, 23:1-11.
38. Takei N., Kawamura M., Hara K., Yonezawa K., Nawa H. Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J. Biol. Chem. 2001, 276:42818-42825.
39. Takei N., Inamura N., Kawamura M., Namba H., Hara K., Yonezawa K., Nawa H. Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J. Neurosci. 2004, 24:9760-9769.
40. Takei N., Kawamura M., Ishizuka Y., Kakiya N., Inamura N., Namba H., Nawa H. Brain-derived neurotrophic factor enhances the basal protein synthesis by increasing active eukaryotic elongation factor 2 levels and promoting translation elongation in cortical neurons. J. Biol. Chem. 2009, 284:26340-26348.
41. Tang S.J., Reis G., Kang H., Gingras A.C., Sonenberg N., Schuman E.M. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:467-472.
42. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995, 270:593-598.
43. Tischmeyer W., Schicknick H., Kraus M., Seidenbecher C.I., Staak S., Scheich H., Gundelfinger E.D. Rapamycin-sensitive signalling in long-term consolidation of auditory cortex-dependent memory. Eur. J. Neurosci. 2003, 18:942-950.
44. Tsokas P., Grace E.A., Chan P., Ma T., Sealfon S.C., Iyengar R., Landau E.M., Blitzer R.D. Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J. Neurosci. 2005, 25:5833-5843.
45. Yamada K., Mizuno M., Nabeshima T. Role for brain-derived neurotrophic factor in learning and memory. Life Sci. 2002, 70:735-744.