Neuralized1 Activates CPEB3: A Function for Nonproteolytic Ubiquitin in Synaptic Plasticity and Memory Storage

Artola, 2006, Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment, Eur. J. Neurosci., 23, 261, 10.1111/j.1460-9568.2005.04552.x Bassani, 2009, The GLUR2 subunit of AMPA receptors: synaptic role, Neuroscience, 158, 55, 10.1016/j.neuroscience.2008.10.007 Brigman, 2010, Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning, J. Neurosci., 30, 4590, 10.1523/JNEUROSCI.0640-10.2010 Carter, 2008, p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53, Cell Cycle, 7, 2519, 10.4161/cc.7.16.6422 Chen, 2009, Nonproteolytic functions of ubiquitin in cell signaling, Mol. Cell, 33, 275, 10.1016/j.molcel.2009.01.014 DiAntonio, 2004, Ubiquitin-dependent regulation of the synapse, Annu. Rev. Neurosci., 27, 223, 10.1146/annurev.neuro.27.070203.144317 Fischer, 2005, Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory, Neuron, 48, 825, 10.1016/j.neuron.2005.10.033 Glickman, 2002, The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction, Physiol. Rev., 82, 373, 10.1152/physrev.00027.2001 Guan, 2009, HDAC2 negatively regulates memory formation and synaptic plasticity, Nature, 459, 55, 10.1038/nature07925 Hicke, 2001, Protein regulation by monoubiquitin, Nat. Rev. Mol. Cell Biol., 2, 195, 10.1038/35056583 Hitchcock, 2003, A subset of membrane-associated proteins is ubiquitinated in response to mutations in the endoplasmic reticulum degradation machinery, Proc. Natl. Acad. Sci. USA, 100, 12735, 10.1073/pnas.2135500100 Hou, 2006, Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression, Neuron, 51, 441, 10.1016/j.neuron.2006.07.005 Huang, 2006, CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA, EMBO J., 25, 4865, 10.1038/sj.emboj.7601322 Kauderer, 2000, Capture of a protein synthesis-dependent component of long-term depression, Proc. Natl. Acad. Sci. USA, 97, 13342, 10.1073/pnas.97.24.13342 Keleman, 2007, Function of the Drosophila CPEB protein Orb2 in long-term courtship memory, Nat. Neurosci., 10, 1587, 10.1038/nn1996 Kopec, 2007, GluR1 links structural and functional plasticity at excitatory synapses, J. Neurosci., 27, 13706, 10.1523/JNEUROSCI.3503-07.2007 Koutelou, 2008, Neuralized-like 1 (Neurl1) targeted to the plasma membrane by N-myristoylation regulates the Notch ligand Jagged1, J. Biol. Chem., 283, 3846, 10.1074/jbc.M706974200 Li, 2003, Mono- versus polyubiquitination: differential control of p53 fate by Mdm2, Science, 302, 1972, 10.1126/science.1091362 Mabb, 2010, Ubiquitination in postsynaptic function and plasticity, Annu. Rev. Cell Dev. Biol., 26, 179, 10.1146/annurev-cellbio-100109-104129 Malleret, 2010, Bidirectional regulation of hippocampal long-term synaptic plasticity and its influence on opposing forms of memory, J. Neurosci., 30, 3813, 10.1523/JNEUROSCI.1330-09.2010 Manahan-Vaughan, 2000, Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats, J. Neurosci., 20, 8572, 10.1523/JNEUROSCI.20-22-08572.2000 Mayford, 1996, Control of memory formation through regulated expression of a CaMKII transgene, Science, 274, 1678, 10.1126/science.274.5293.1678 Miniaci, 2008, Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia, Neuron, 59, 1024, 10.1016/j.neuron.2008.07.036 Morris, 1982, Place navigation impaired in rats with hippocampal lesions, Nature, 297, 681, 10.1038/297681a0 Mukai, 2007, Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons, J. Neurochem., 100, 950, 10.1111/j.1471-4159.2006.04264.x Nayak, 1998, Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis, Nature, 394, 680, 10.1038/29305 Nicholls, 2008, Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility, Neuron, 58, 104, 10.1016/j.neuron.2008.01.039 Nicoll, 2003, Expression mechanisms underlying long-term potentiation: a postsynaptic view, Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, 721, 10.1098/rstb.2002.1228 Passafaro, 2003, Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2, Nature, 424, 677, 10.1038/nature01781 Pavlopoulos, 2008, Neuralized is expressed in the α/β lobes of adult Drosophila mushroom bodies and facilitates olfactory long-term memory formation, Proc. Natl. Acad. Sci. USA, 105, 14674, 10.1073/pnas.0801605105 Peng, 2003, A proteomics approach to understanding protein ubiquitination, Nat. Biotechnol., 21, 921, 10.1038/nbt849 Qian, 2002, Fusion proteins with COOH-terminal ubiquitin are stable and maintain dual functionality in vivo, J. Biol. Chem., 277, 38818, 10.1074/jbc.M205547200 Richter, 2007, CPEB: a life in translation, Trends Biochem. Sci., 32, 279, 10.1016/j.tibs.2007.04.004 Saglietti, 2007, Extracellular interactions between GluR2 and N-cadherin in spine regulation, Neuron, 54, 461, 10.1016/j.neuron.2007.04.012 Sala, 2001, Regulation of dendritic spine morphology and synaptic function by Shank and Homer, Neuron, 31, 115, 10.1016/S0896-6273(01)00339-7 Segref, 2009, Think locally: control of ubiquitin-dependent protein degradation in neurons, EMBO Rep., 10, 44, 10.1038/embor.2008.229 Shimada, 2003, Age-related loss of synapses in the frontal cortex of SAMP10 mouse: a model of cerebral degeneration, Synapse, 48, 198, 10.1002/syn.10209 Si, 2003, A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia, Cell, 115, 893, 10.1016/S0092-8674(03)01021-3 Si, 2003, A neuronal isoform of the aplysia CPEB has prion-like properties, Cell, 115, 879, 10.1016/S0092-8674(03)01020-1 Si, 2010, Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation, Cell, 140, 421, 10.1016/j.cell.2010.01.008 Spence, 2000, Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain, Cell, 102, 67, 10.1016/S0092-8674(00)00011-8 Sutton, 2006, Dendritic protein synthesis, synaptic plasticity, and memory, Cell, 127, 49, 10.1016/j.cell.2006.09.014 Tanaka, 2008, Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines, Science, 319, 1683, 10.1126/science.1152864 Theis, 2003, Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus, Proc. Natl. Acad. Sci. USA, 100, 9602, 10.1073/pnas.1133424100 Bevins, R.A., and Besheer, J. (2006). Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat. Protoc. 1, 1306–1311. Bourtchouladze, R., Lidge, R., Catapano, R., Stanley, J., Gossweiler, S., Romashko, D., Scott, R., and Tully, T. (2003). A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc. Natl. Acad. Sci. USA 100, 10518–10522. Cho, K.O., Hunt, C.A., and Kennedy, M.B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929–942. Dittgen, T., Nimmerjahn, A., Komai, S., Licznerski, P., Waters, J., Margrie, T.W., Helmchen, F., Denk, W., Brecht, M., and Osten, P. (2004). Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc. Natl. Acad. Sci. USA 101, 18206–18211. Hake, L.E., Mendez, R., and Richter, J.D. (1998). Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol. Cell. Biol. 18, 685–693. Kellendonk, C., Simpson, E.H., Polan, H.J., Malleret, G., Vronskaya, S., Winiger, V., Moore, H., and Kandel, E.R. (2006). Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 49, 603–615. Köhler, M., Kornau, H.C., and Seeburg, P.H. (1994). The organization of the gene for the functionally dominant alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor subunit GluR-B. J. Biol. Chem. 269, 17367–17370. Lattal, K.M., and Abel, T. (2004). Behavioral impairments caused by injections of the protein synthesis inhibitor anisomycin after contextual retrieval reverse with time. Proc. Natl. Acad. Sci. USA 101, 4667–4672. Malleret, G., Hen, R., Guillou, J.L., Segu, L., and Buhot, M.C. (1999). 5-HT1B receptor knock-out mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze. J. Neurosci. 19, 6157–6168. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D., and Kandel, E.R. (1996). Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678–1683 Puthanveettil, S.V., Monje, F.J., Miniaci, M.C., Choi, Y.B., Karl, K.A., Khandros, E., Gawinowicz, M.A., Sheetz, M.P., and Kandel, E.R. (2008). A new component in synaptic plasticity: upregulation of kinesin in the neurons of the gill-withdrawal reflex. Cell 135, 960–973. Savonenko, A.V., Melnikova, T., Laird, F.M., Stewart, K.A., Price, D.L., and Wong, P.C. (2008). Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc. Natl. Acad. Sci. USA 105, 5585–5590. Silva, A.J. (1997). Mutant mice and neuroscience: recommendations concerning genetic background. Banbury Conference on genetic background in mice. Neuron 19, 755–759. Taubenfeld, S.M., Stevens, K.A., Pollonini, G., Ruggiero, J., and Alberini, C.M. (2002). Profound molecular changes following hippocampal slice preparation: loss of AMPA receptor subunits and uncoupled mRNA/protein expression. J. Neurochem. 81, 1348–1360. Villasana, L.E., Klann, E., and Tejada-Simon, M.V. (2006). Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J. Neurosci. Methods 158, 30–36. Walf, A.A., and Frye, C.A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2, 322–328. Wellman, C.L., Izquierdo, A., Garrett, J.E., Martin, K.P., Carroll, J., Millstein, R., Lesch, K.P., Murphy, D.L., and Holmes, A. (2007). Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J. Neurosci. 27, 684–691.