Staufen1 Regulation of Protein Synthesis-Dependent Long-Term Potentiation and Synaptic Function in Hippocampal Pyramidal Cells

REFERENCES

• Alvarez, V. A., D. A. Ridenour, and B. L. Sabatini. 2006. Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J. Neurosci. 26:7820–7825.
   PubMed Web of Science ®Google Scholar
• 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
• Banker, G., and K. Goslin. 1988. Developments in neuronal cell culture. Nature 336:185–186.
   PubMedGoogle Scholar
• Bourdeau, M. L., F. Morin, C. E. Laurent, M. Azzi, and J. C. Lacaille. 2007. Kv4.3-mediated A-type K+ currents underlie rhythmic activity in hippocampal interneurons. J. Neurosci. 27:1942–1953.
   PubMedGoogle Scholar
• Bradshaw, K. D., N. J. Emptage, and T. V. Bliss. 2003. A role for dendritic protein synthesis in hippocampal late LTP. Eur. J. Neurosci. 18:3150–3152.
   PubMed Web of Science ®Google Scholar
• Broadus, J., S. Fuerstenberg, and C. Q. Doe. 1998. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391:792–795.
   PubMed Web of Science ®Google Scholar
• Buchner, G., M. T. Bassi, G. Andolfi, A. Ballabio, and B. Franco. 1999. Identification of a novel homolog of the Drosophila staufen protein in the chromosome 8q13-q21.1 region. Genomics 62:113–118.
   PubMedGoogle Scholar
• Chavez-Noriega, L. E., and C. F. Stevens. 1992. Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin. Brain Res. 574:85–92.
   PubMedGoogle Scholar
• Comery, T. A., J. B. Harris, P. J. Willems, B. A. Oostra, S. A. Irwin, I. J. Weiler, and W. T. Greenough. 1997. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. USA 94:5401–5404.
   PubMedGoogle Scholar
• DesGroseillers, L., and N. Lemieux. 1996. Localization of a human double-stranded RNA-binding protein gene (STAU) to band 20q13.1 by fluorescence in situ hybridization. Genomics 36:527–529.
   PubMedGoogle Scholar
• Dubnau, J., A. S. Chiang, L. Grady, J. Barditch, S. Gossweiler, J. McNeil, P. Smith, F. Buldoc, R. Scott, U. Certa, C. Broger, and T. Tully. 2003. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13:286–296.
   PubMed Web of Science ®Google Scholar
• Duchaine, T. F., I. Hemraj, L. Furic, A. Deitinghoff, M. A. Kiebler, and L. DesGroseillers. 2002. Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. J. Cell Sci. 115:3285–3295.
   PubMedGoogle Scholar
• Dugre-Brisson, S., G. Elvira, K. Boulay, L. Chatel-Chaix, A. J. Mouland, and L. DesGroseillers. 2005. Interaction of Staufen1 with the 5′ end of mRNA facilitates translation of these RNAs. Nucleic Acids Res. 33:4797–4812.
   PubMedGoogle Scholar
• Elvira, G., B. Massie, and L. DesGroseillers. 2006. The zinc-finger protein ZFR is critical for Staufen 2 isoform specific nucleocytoplasmic shuttling in neurons. J. Neurochem. 96:105–117.
   PubMedGoogle Scholar
• Fitzjohn, S. M., A. E. Kingston, D. Lodge, and G. L. Collingridge. 1999. DHPG-induced LTD in area CA1 of juvenile rat hippocampus; characterisation and sensitivity to novel mGlu receptor antagonists. Neuropharmacology 38:1577–1583.
   PubMedGoogle Scholar
• Frey, U., M. Krug, K. G. Reymann, and H. Matthies. 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.
   PubMed Web of Science ®Google Scholar
• Gelinas, J. N., and P. V. Nguyen. 2005. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J. Neurosci. 25:3294–3303.
   PubMedGoogle Scholar
• Goetze, B., F. Tuebing, Y. Xie, M. M. Dorostkar, S. Thomas, U. Pehl, S. Boehm, P. Macchi, and M. A. Kiebler. 2006. The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J. Cell Biol. 172:221–231.
   PubMed Web of Science ®Google 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
• Harris, K. M., and J. K. Stevens. 1989. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9:2982–2997.
   PubMed Web of Science ®Google Scholar
• Huang, Y. Y., X. C. Li, and E. R. Kandel. 1994. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69–79.
   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
• Huber, K. M., N. B. Sawtell, and M. F. Bear. 1998. Effects of the metabotropic glutamate receptor antagonist MCPG on phosphoinositide turnover and synaptic plasticity in visual cortex. J. Neurosci. 18:1–9.
   PubMedGoogle Scholar
• Judge, A. D., V. Sood, J. R. Shaw, D. Fang, K. McClintock, and I. MacLachlan. 2005. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23:457–462.
   PubMed Web of Science ®Google Scholar
• Kanai, Y., N. Dohmae, and N. Hirokawa. 2004. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43:513–525.
   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
• Kiebler, M. A., and L. DesGroseillers. 2000. Molecular insights into mRNA transport and local translation in the mammalian nervous system. Neuron 25:19–28.
   PubMed Web of Science ®Google Scholar
• Kiebler, M. A., I. Hemraj, P. Verkade, M. Kohrmann, P. Fortes, R. M. Marion, J. Ortin, and C. G. Dotti. 1999. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J. Neurosci. 19:288–297.
   PubMed Web of Science ®Google Scholar
• Kim, K. C., and H. K. Kim. 2006. Role of Staufen in dendritic mRNA transport and its modulation. Neurosci. Lett. 397:48–52.
   PubMedGoogle Scholar
• Kim, Y. K., L. Furic, L. Desgroseillers, and L. E. Maquat. 2005. Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay. Cell 120:195–208.
   PubMed Web of Science ®Google Scholar
• Kohrmann, M., M. Luo, C. Kaether, L. DesGroseillers, C. G. Dotti, and M. A. Kiebler. 1999. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10:2945–2953.
   PubMed Web of Science ®Google Scholar
• Kopec, C. D., B. Li, W. Wei, J. Boehm, and R. Malinow. 2006. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26:2000–2009.
   PubMed Web of Science ®Google Scholar
• Krichevsky, A. M., and K. S. Kosik. 2001. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683–696.
   PubMedGoogle Scholar
• Luo, M., T. F. Duchaine, and L. DesGroseillers. 2002. Molecular mapping of the determinants involved in human Staufen-ribosome association. Biochem. J. 365:817–824.
   PubMedGoogle Scholar
• Manabe, T., P. Renner, and R. A. Nicoll. 1992. Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355:50–55.
   PubMedGoogle Scholar
• Marion, R. M., P. Fortes, A. Beloso, C. Dotti, and J. Ortin. 1999. A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:2212–2219.
   PubMedGoogle Scholar
• Matsuzaki, F., T. Ohshiro, H. Ikeshima-Kataoka, and H. Izumi. 1998. miranda localizes staufen and prospero asymmetrically in mitotic neuroblasts and epithelial cells in early Drosophila embryogenesis. Development 125:4089–4098.
   PubMed Web of Science ®Google Scholar
• Matsuzaki, M., G. C. Ellis-Davies, T. Nemoto, Y. Miyashita, M. Iino, and H. Kasai. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4:1086–1092.
   PubMed Web of Science ®Google Scholar
• McKinney, R. A. 2005. Physiological roles of spine motility: development, plasticity and disorders. Biochem. Soc. Trans. 33:1299–1302.
   PubMedGoogle Scholar
• Miller, S., M. Yasuda, J. K. Coats, Y. Jones, M. E. Martone, and M. Mayford. 2002. Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36:507–519.
   PubMed Web of Science ®Google Scholar
• Nguyen, P. V., T. Abel, and E. R. Kandel. 1994. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104–1107.
   PubMed Web of Science ®Google Scholar
• Nusser, Z., R. Lujan, G. Laube, J. D. Roberts, E. Molnar, and P. Somogyi. 1998. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545–559.
   PubMedGoogle Scholar
• Ostroff, L. E., J. C. Fiala, B. Allwardt, and K. M. Harris. 2002. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535–545.
   PubMed Web of Science ®Google Scholar
• Otmakhov, N., L. Khibnik, N. Otmakhova, S. Carpenter, S. Riahi, B. Asrican, and J. Lisman. 2004. Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J. Neurophysiol. 91:1955–1962.
   PubMed Web of Science ®Google Scholar
• Pierce, J. P., K. van Leyen, and J. B. McCarthy. 2000. Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat. Neurosci. 3:311–313.
   PubMedGoogle Scholar
• Sabatini, B. L., M. Maravall, and K. Svoboda. 2001. Ca(2+) signaling in dendritic spines. Curr. Opin. Neurobiol. 11:349–356.
   PubMedGoogle Scholar
• Scanziani, M., M. Capogna, B. H. Gahwiler, and S. M. Thompson. 1992. Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus. Neuron 9:919–927.
   PubMedGoogle Scholar
• Shi, S. H., Y. Hayashi, R. S. Petralia, S. H. Zaman, R. J. Wenthold, K. Svoboda, and R. Malinow. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811–1816.
   PubMed Web of Science ®Google Scholar
• Sledz, C. A., M. Holko, M. J. de Veer, R. H. Silverman, and B. R. Williams. 2003. Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5:834–839.
   PubMed Web of Science ®Google Scholar
• Sossin, W. S., and L. DesGroseillers. 2006. Intracellular trafficking of RNA in neurons. Traffic 7:1581–1589.
   PubMed Web of Science ®Google Scholar
• Steward, O., and E. M. Schuman. 2001. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24:299–325.
   PubMed Web of Science ®Google Scholar
• St Johnston, D. 1995. The intracellular localization of messenger RNAs. Cell 81:161–170.
   PubMed Web of Science ®Google Scholar
• Stoppini, L., P. A. Buchs, and D. Muller. 1991. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37:173–182.
   PubMed Web of Science ®Google Scholar
• Sutton, M. A., and E. M. Schuman. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49–58.
   PubMed Web of Science ®Google Scholar
• Tang, S. J., D. Meulemans, L. Vazquez, N. Colaco, and E. Schuman. 2001. A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32:463–475.
   PubMedGoogle Scholar
• Tang, S. J., and E. M. Schuman. 2002. Protein synthesis in the dendrite. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:521–529.
   PubMed Web of Science ®Google Scholar
• Thomas, M. G., L. J. Martinez Tosar, M. Loschi, J. M. Pasquini, J. Correale, S. Kindler, and G. L. Boccaccio. 2005. Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol. Biol. Cell 16:405–420.
   PubMedGoogle Scholar
• Tiedge, H., and J. Brosius. 1996. Translational machinery in dendrites of hippocampal neurons in culture. J. Neurosci. 16:7171–7181.
   PubMedGoogle Scholar
• Turrigiano, G. G. 2000. AMPA receptors unbound: membrane cycling and synaptic plasticity. Neuron 26:5–8.
   PubMedGoogle Scholar
• Volk, L. J., C. A. Daly, and K. M. Huber. 2006. Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression. J. Neurophysiol. 95:2427–2438.
   PubMedGoogle Scholar
• Wickham, L., T. Duchaine, M. Luo, I. R. Nabi, and L. DesGroseillers. 1999. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:2220–2230.
   PubMed Web of Science ®Google Scholar
• Wong, S. T., J. Athos, X. A. Figueroa, V. V. Pineda, M. L. Schaefer, C. C. Chavkin, L. J. Muglia, and D. R. Storm. 1999. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787–798.
   PubMed Web of Science ®Google Scholar
• Yuste, R., and W. Denk. 1995. Dendritic spines as basic functional units of neuronal integration. Nature 375:682–684.
   PubMedGoogle Scholar
• Zalfa, F., T. Achsel, and C. Bagni. 2006. mRNPs, polysomes or granules: FMRP in neuronal protein synthesis. Curr. Opin. Neurobiol. 16:265–269.
   PubMed Web of Science ®Google Scholar