mGluR-Dependent Long-Term Depression Is Associated with Increased Phosphorylation of S6 and Synthesis of Elongation Factor 1A but Remains Expressed in S6K-Deficient Mice

REFERENCES

• Antar, L. N., R. Afroz, J. B. Dictenberg, R. C. Carroll, and G. J. Bassell. 2004. Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 24:2648–2655.
   PubMed Web of Science ®Google Scholar
• Antion, M. D., M. Merhav, C. A. Hoeffer, G. Reis, S. C. Kozma, G. Thomas, E. M. Schuman, K. Rosenblum, and E. Klann. 2008. Removal of S6K1 and S6K2 leads to divergent alterations in learning, memory, and synaptic plasticity. Learn. Mem. 15:29–38.
   PubMedGoogle Scholar
• Aschrafi, A., B. A. Cunningham, G. M. Edelman, and P. W. Vanderklish. 2005. The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain. Proc. Natl. Acad. Sci. USA 102:2180–2185.
   PubMedGoogle Scholar
• Banko, J. L., L. Hou, F. Poulin, N. Sonenberg, and E. Klann. 2006. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26:2167–2173.
   PubMedGoogle Scholar
• Bardoni, B., and J. L. Mandel. 2002. Advances in understanding of fragile X pathogenesis and FMRP function, and in identification of X linked mental retardation genes. Curr. Opin. Genet. Dev. 12:284–293.
   PubMed Web of Science ®Google Scholar
• Cammalleri, M., R. Lutjens, F. Berton, A. R. King, C. Simpson, W. Francesconi, and P. P. Sanna. 2003. 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. USA 100:14368–14373.
   PubMedGoogle Scholar
• Costa-Mattioli, M., D. Gobert, H. Harding, B. Herdy, M. Azzi, M. Bruno, M. Bidinosti, C. Ben Mamou, E. Marcinkiewicz, M. Yoshida, H. Imataka, A. C. Cuello, N. Seidah, W. Sossin, J. C. Lacaille, D. Ron, K. Nader, and N. Sonenberg. 2005. Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436:1166–1173.
   PubMed Web of Science ®Google Scholar
• Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253:100–109.
   PubMed Web of Science ®Google Scholar
• Gallagher, S. M., C. A. Daly, M. F. Bear, and K. M. Huber. 2004. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J. Neurosci. 24:4859–4864.
   PubMed Web of Science ®Google Scholar
• Giustetto, M., A. N. Hegde, K. Si, A. Casadio, K. Inokuchi, W. Pei, E. R. Kandel, and J. H. Schwartz. 2003. Axonal transport of eukaryotic translation elongation factor 1alpha mRNA couples transcription in the nucleus to long-term facilitation at the synapse. Proc. Natl. Acad. Sci. USA 100:13680–13685.
   PubMedGoogle Scholar
• Gout, I., T. Minami, K. Hara, Y. Tsujishita, V. Filonenko, M. D. Waterfield, and K. Yonezawa. 1998. Molecular cloning and characterization of a novel p70 S6 kinase, p70 S6 kinase beta containing a proline-rich region. J. Biol. Chem. 273:30061–30064.
   PubMedGoogle Scholar
• Greenough, W. T., A. Y. Klintsova, S. A. Irwin, R. Galvez, K. E. Bates, and I. J. Weiler. 2001. Synaptic regulation of protein synthesis and the fragile X protein. Proc. Natl. Acad. Sci. USA 98:7101–7106.
   PubMed Web of Science ®Google Scholar
• Gressner, A. M., and I. G. Wool. 1974. The phosphorylation of liver ribosomal proteins in vivo. Evidence that only a single small subunit protein (S6) is phosphorylated. J. Biol. Chem. 249:6917–6925.
   PubMedGoogle Scholar
• Holz, M. K., B. A. Ballif, S. P. Gygi, and J. Blenis. 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569–580.
   PubMed Web of Science ®Google Scholar
• Hou, L., M. D. Antion, D. Hu, C. M. Spencer, R. Paylor, and E. Klann. 2006. Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51:441–454.
   PubMed Web of Science ®Google Scholar
• Hou, L., and E. Klann. 2004. 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. 24:6352–6361.
   PubMed Web of Science ®Google Scholar
• Huang, F., J. K. Chotiner, and O. Steward. 2005. The mRNA for elongation factor 1alpha is localized in dendrites and translated in response to treatments that induce long-term depression. J. Neurosci. 25:7199–7209.
   PubMedGoogle Scholar
• Huber, K. M., S. M. Gallagher, S. T. Warren, and M. F. Bear. 2002. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA 99:7746–7750.
   PubMed Web of Science ®Google Scholar
• Huber, K. M., M. S. Kayser, and M. F. Bear. 2000. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254–1257.
   PubMed Web of Science ®Google Scholar
• Kelleher, R. J., III, A. Govindarajan, H. Y. Jung, H. Kang, and S. Tonegawa. 2004. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467–479.
   PubMed Web of Science ®Google Scholar
• Khalyfa, A., D. Bourbeau, E. Chen, E. Petroulakis, J. Pan, S. Xu, and E. Wang. 2001. Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2/S1 protein expression in normal and wasted mice. J. Biol. Chem. 276:22915–22922.
   PubMedGoogle Scholar
• Khan, A., A. M. Pepio, and W. S. Sossin. 2001. Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci. 21:382–391.
   PubMedGoogle Scholar
• Klann, E., M. D. Antion, J. L. Banko, and L. Hou. 2004. Synaptic plasticity and translation initiation. Learn. Mem. 11:365–372.
   PubMed Web of Science ®Google Scholar
• Lee-Fruman, K. K., C. J. Kuo, J. Lippincott, N. Terada, and J. Blenis. 1999. Characterization of S6K2, a novel kinase homologous to S6K1. Oncogene 18:5108–5114.
   PubMedGoogle Scholar
• Liu, G., W. M. Grant, D. Persky, V. M. Latham, Jr., R. H. Singer, and J. Condeelis. 2002. Interactions of elongation factor 1alpha with F-actin and beta-actin mRNA: implications for anchoring mRNA in cell protrusions. Mol. Biol. Cell 13:579–592.
   PubMed Web of Science ®Google Scholar
• Martin, K. A., S. S. Schalm, C. Richardson, A. Romanelli, K. L. Keon, and J. Blenis. 2001. Regulation of ribosomal S6 kinase 2 by effectors of the phosphoinositide 3-kinase pathway. J. Biol. Chem. 276:7884–7891.
   PubMed Web of Science ®Google Scholar
• Martin, K. A., S. S. Schalm, A. Romanelli, K. L. Keon, and J. Blenis. 2001. Ribosomal S6 kinase 2 inhibition by a potent C-terminal repressor domain is relieved by mitogen-activated protein-extracellular signal-regulated kinase kinase-regulated phosphorylation. J. Biol. Chem. 276:7892–7898.
   PubMed Web of Science ®Google Scholar
• Meyuhas, O. 2000. Synthesis of the translational apparatus is regulated at the translational level. Eur. J. Biochem. 267:6321–6330.
   PubMedGoogle Scholar
• Nosyreva, E. D., and K. M. Huber. 2005. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 25:2992–3001.
   PubMedGoogle Scholar
• Nosyreva, E. D., and K. M. Huber. 2006. Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J. Neurophysiol. 95:3291–3295.
   PubMed Web of Science ®Google Scholar
• Nygard, O., and L. Nilsson. 1990. Translational dynamics. Interactions between the translational factors, tRNA and ribosomes during eukaryotic protein synthesis. Eur. J. Biochem. 191:1–17.
   PubMedGoogle Scholar
• Oliver, C. J., R. T. Terry-Lorenzo, E. Elliott, W. A. Bloomer, S. Li, D. L. Brautigan, R. J. Colbran, and S. Shenolikar. 2002. Targeting protein phosphatase 1 (PP1) to the actin cytoskeleton: the neurabin I/PP1 complex regulates cell morphology. Mol. Cell. Biol. 22:4690–4701.
   PubMedGoogle Scholar
• Page, G., F. A. Khidir, S. Pain, L. Barrier, B. Fauconneau, O. Guillard, A. Piriou, and J. Hugon. 2006. Group I metabotropic glutamate receptors activate the p70S6 kinase via both mammalian target of rapamycin (mTOR) and extracellular signal-regulated kinase (ERK 1/2) signaling pathways in rat striatal and hippocampal synaptoneurosomes. Neurochem. Int. 49:413–421.
   PubMedGoogle Scholar
• Park, I. H., R. Bachmann, H. Shirazi, and J. Chen. 2002. Regulation of ribosomal S6 kinase 2 by mammalian target of rapamycin. J. Biol. Chem. 277:31423–31429.
   PubMedGoogle Scholar
• Pearson, R. B., P. B. Dennis, J. W. Han, N. A. Williamson, S. C. Kozma, R. E. Wettenhall, and G. Thomas. 1995. The principal target of rapamycin-induced p70s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain. EMBO J. 14:5279–5287.
   PubMedGoogle Scholar
• Pende, M., S. H. Um, V. Mieulet, M. Sticker, V. L. Goss, J. Mestan, M. Mueller, S. Fumagalli, S. C. Kozma, and G. Thomas. 2004. S6K1−/−/S6K2−/− mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24:3112–3124.
   PubMed Web of Science ®Google Scholar
• Raymond, C. R., V. L. Thompson, W. P. Tate, and W. C. Abraham. 2000. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J. Neurosci. 20:969–976.
   PubMed Web of Science ®Google Scholar
• Richardson, C. J., M. Broenstrup, D. C. Fingar, K. Julich, B. A. Ballif, S. Gygi, and J. Blenis. 2004. SKAR is a specific target of S6 kinase 1 in cell growth control. Curr. Biol. 14:1540–1549.
   PubMed Web of Science ®Google Scholar
• Roberson, E. D., J. D. English, J. P. Adams, J. C. Selcher, C. Kondratick, and J. D. Sweatt. 1999. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 19:4337–4348.
   PubMed Web of Science ®Google Scholar
• Ronesi, J. A., and K. M. Huber. 2008. Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation. J. Neurosci. 28:543–547.
   PubMedGoogle Scholar
• Roux, P. P., D. Shahbazian, H. Vu, M. K. Holz, M. S. Cohen, J. Taunton, N. Sonenberg, and J. Blenis. 2007. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J. Biol. Chem. 282:14056–14064.
   PubMed Web of Science ®Google Scholar
• Ruvinsky, I., and O. Meyuhas. 2006. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 31:342–348.
   PubMed Web of Science ®Google Scholar
• Ruvinsky, I., N. Sharon, T. Lerer, H. Cohen, M. Stolovich-Rain, T. Nir, Y. Dor, P. Zisman, and O. Meyuhas. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19:2199–2211.
   PubMed Web of Science ®Google Scholar
• Sarbassov, D. D., S. M. Ali, and D. M. Sabatini. 2005. Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17:596–603.
   PubMed Web of Science ®Google Scholar
• Shima, H., M. Pende, Y. Chen, S. Fumagalli, G. Thomas, and S. C. Kozma. 1998. Disruption of the p70(s6k)/p85(s6k) gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 17:6649–6659.
   PubMed Web of Science ®Google Scholar
• Stolovich, M., T. Lerer, Y. Bolkier, H. Cohen, and O. Meyuhas. 2005. Lithium can relieve translational repression of TOP mRNAs elicited by various blocks along the cell cycle in a glycogen synthase kinase-3- and S6-kinase-independent manner. J. Biol. Chem. 280:5336–5342.
   PubMedGoogle Scholar
• Sung, Y. J., N. Dolzhanskaya, S. L. Nolin, T. Brown, J. R. Currie, and R. B. Denman. 2003. The fragile X mental retardation protein FMRP binds elongation factor 1A mRNA and negatively regulates its translation in vivo. J. Biol. Chem. 278:15669–15678.
   PubMed Web of Science ®Google Scholar
• Tang, H., E. Hornstein, M. Stolovich, G. Levy, M. Livingstone, D. Templeton, J. Avruch, and O. Meyuhas. 2001. Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol. Cell. Biol. 21:8671–8683.
   PubMed Web of Science ®Google Scholar
• Tsokas, P., E. A. Grace, P. Chan, T. Ma, S. C. Sealfon, R. Iyengar, E. M. Landau, and R. D. Blitzer. 2005. Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J. Neurosci. 25:5833–5843.
   PubMedGoogle Scholar
• Tsokas, P., T. Ma, R. Iyengar, E. M. Landau, and R. D. Blitzer. 2007. Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J. Neurosci. 27:5885–5894.
   PubMedGoogle Scholar
• Wang, L., I. Gout, and C. G. Proud. 2001. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J. Biol. Chem. 276:32670–32677.
   PubMedGoogle Scholar
• Weiler, I. J., and W. T. Greenough. 1993. Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc. Natl. Acad. Sci. USA 90:7168–7171.
   PubMed Web of Science ®Google Scholar
• Wool, I. G. 1996. Mammalian ribosome: the structure and evolution of the proteins, p. 685-718. In J. W. B. Hershey and N. Sonenburg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar