The Persistence of Hippocampal-Based Memory Requires Protein Synthesis Mediated by the Prion-like Protein CPEB3

Neuron

Volumn 86, Issue 6, 2015, Pages 1433-1448

  Fioriti, Luana ^a   Myers, Cory ^a   Huang, Yan You ^a   Li, Xiang ^a   Stephan, Joseph S ^a,b   Trifilieff, Pierre ^a   Colnaghi, Luca ^a,b   Kosmidis, Stylianos ^a,b   Drisaldi, Bettina ^a   Pavlopoulos, Elias ^a   Kandel, Eric R ^a,b,c  

^a College of Physicians and Surgeons of Columbia University ^*  (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Kavli Institute for Brain Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN 3; UNCLASSIFIED DRUG; CPEB3 PROTEIN, MOUSE; ENOLASE; GLUTAMIC ACID; RNA BINDING PROTEIN;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CONDITIONING; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; FEAR; GENETIC PROCEDURES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOUSE; MOUSE MUTANT; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN SYNTHESIS; SPATIAL MEMORY; SYNAPSE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GENETICS; IN VITRO STUDY; MAZE TEST; MEMORY; METABOLISM; MUTATION; NERVE CELL; PHYSIOLOGY; REACTION TIME; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; ANXIETY; CONDITIONING (PSYCHOLOGY); EXPLORATORY BEHAVIOR; FEAR; GLUTAMIC ACID; HIPPOCAMPUS; IN VITRO TECHNIQUES; LOCOMOTION; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURONS; PHOSPHOPYRUVATE HYDRATASE; REACTION TIME; RNA-BINDING PROTEINS;

EID: 84931574130     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.05.021     Document Type: Article

References (51)

1. Alarcon J.M., Hodgman R., Theis M., Huang Y.S., Kandel E.R., Richter J.D. Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn. Mem. 2004, 11:318-327.
2. Alberti S., Halfmann R., King O., Kapila A., Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009, 137:146-158.
3. Bailey C.H., Kandel E.R., Si K. The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 2004, 44:49-57.
4. Bannerman D.M., Rawlins J.N., Good M.A. The drugs don't work-or do they? Pharmacological and transgenic studies of the contribution of NMDA and GluR-A-containing AMPA receptors to hippocampal-dependent memory. Psychopharmacology (Berl.) 2006, 188:552-566.
5. Bast T., da Silva B.M., Morris R.G.M. Distinct contributions of hippocampal NMDA and AMPA receptors to encoding and retrieval of one-trial place memory. J. Neurosci. 2005, 25:5845-5856.
6. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat. Protoc. 2006, 1:1306-1311.
7. Chao H.-W., Tsai L.-Y., Lu Y.-L., Lin P.-Y., Huang W.-H., Chou H.-J., Lu W.-H., Lin H.-C., Lee P.-T., Huang Y.-S. Deletion of CPEB3 enhances hippocampus-dependent memory via increasing expressions of PSD95 and NMDA receptors. J. Neurosci. 2013, 33:17008-17022.
8. Chiesa R., Fioriti L., Tagliavini F., Salmona M., Forloni G. Citotoxicity of PrP peptides. Techniques in Prion Research 2004, 176-197. Birkhäuser Basel. S. Lehmann, J. Grassi (Eds.).
9. Drisaldi D., Colnaghi L., Fioriti L., Rao N., Myers C., Snyder A.M., Metzger D.J., Tarasoff J., Konstantinov E., Fraser P., et al. SUMOylation is an inhibitory constraint that regulates the prion-like aggregation and Activity of CPEB3. Cell Rep. 2015, 11. Published online June 11, 2015. 10.1016/j.celrep.2015.04.061.
10. Du L., Richter J.D. Activity-dependent polyadenylation in neurons. RNA 2005, 11:1340-1347.
11. Dudai Y. Molecular bases of long-term memories: a question of persistence. Curr. Opin. Neurobiol. 2002, 12:211-216.
12. Fanselow M.S., Poulos A.M. The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 2005, 56:207-234.
13. Fiumara F., Fioriti L., Kandel E.R., Hendrickson W.A. Essential role of coiled coils for aggregation and activity of Q/N-rich prions and PolyQ proteins. Cell 2010, 143:1121-1135.
14. Gerlai R., Henderson J.T., Roder J.C., Jia Z. Multiple behavioral anomalies in GluR2 mutant mice exhibiting enhanced LTP. Behav. Brain Res. 1998, 95:37-45.
15. Groc L., Choquet D. AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res. 2006, 326:423-438.
16. Hake L.E., Richter J.D. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 1994, 79:617-627.
17. Hosoda N., Funakoshi Y., Hirasawa M., Yamagishi R., Asano Y., Miyagawa R., Ogami K., Tsujimoto M., Hoshino S. Anti-proliferative protein Tob negatively regulates CPEB3 target by recruiting Caf1 deadenylase. EMBO J. 2011, 30:1311-1323.
18. Huang Y.-S., Kan M.-C., Lin C.-L., Richter J.D. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 2006, 25:4865-4876.
19. Izquierdo I., Bevilaqua L.R.M., Rossato J.I., da Silva W.C., Bonini J., Medina J.H., Cammarota M. The molecular cascades of long-term potentiation underlie memory consolidation of one-trial avoidance in the CA1 region of the dorsal hippocampus, but not in the basolateral amygdala or the neocortex. Neurotox. Res. 2008, 14:273-294.
20. Jaafari N., Konopacki F.A., Owen T.F., Kantamneni S., Rubin P., Craig T.J., Wilkinson K.A., Henley J.M. SUMOylation is required for glycine-induced increases in AMPA receptor surface expression (ChemLTP) in hippocampal neurons. PLoS ONE 2013, 8:e52345.
21. Kandel E.R. The molecular biology of memory storage: a dialog between genes and synapses. Biosci. Rep. 2001, 21:565-611.
22. Keleman K., Krüttner S., Alenius M., Dickson B.J. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 2007, 10:1587-1593.
23. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
24. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
25. Lee H.-K., Takamiya K., He K., Song L., Huganir R.L. Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J. Neurophysiol. 2010, 103:479-489.
26. Liang K.C., Hon W., Tyan Y.M., Liao W.L. Involvement of hippocampal NMDA and AMPA receptors in acquisition, formation and retrieval of spatial memory in the Morris water maze. Chin. J. Physiol. 1994, 37:201-212.
27. Majumdar A., Cesario W.C., White-Grindley E., Jiang H., Ren F., Khan M.R., Li L., Choi E.M.-L., Kannan K., Guo F., et al. Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 2012, 148:515-529.
28. Martin K.C., Barad M., Kandel E.R. Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 2000, 10:587-592.
29. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248-251.
30. Mead A.N., Stephens D.N. Involvement of AMPA receptor GluR2 subunits in stimulus-reward learning: evidence from glutamate receptor gria2 knock-out mice. J. Neurosci. 2003, 23:9500-9507.
31. Michelitsch M.D., Weissman J.S. A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc. Natl. Acad. Sci. USA 2000, 97:11910-11915.
32. Morris R.G.M. Spatial localization does not require the presence of local cues. Learn. Motiv. 1981, 12:239-260.
33. Morris R.G.M., Inglis J., Ainge J.A., Olverman H.J., Tulloch J., Dudai Y., Kelly P.A.T. Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 2006, 50:479-489.
34. Muller D., Toni N., Buchs P.A. Spine changes associated with long-term potentiation. Hippocampus 2000, 10:596-604.
35. Nayak A., Zastrow D.J., Lickteig R., Zahniser N.R., Browning M.D. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 1998, 394:680-683.
36. Nolan M.F., Malleret G., Dudman J.T., Buhl D.L., Santoro B., Gibbs E., Vronskaya S., Buzsáki G., Siegelbaum S.A., Kandel E.R., Morozov A. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 2004, 119:719-732.
37. Oe S., Yoneda Y. Cytoplasmic polyadenylation element-like sequences are involved in dendritic targeting of BDNF mRNA in hippocampal neurons. FEBS Lett. 2010, 584:3424-3430.
38. Pavlopoulos E., Trifilieff P., Chevaleyre V., Fioriti L., Zairis S., Pagano A., Malleret G., Kandel E.R. Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 2011, 147:1369-1383.
39. Raveendra B.L., Siemer A.B., Puthanveettil S.V., Hendrickson W.A., Kandel E.R., McDermott A.E. Characterization of prion-like conformational changes of the neuronal isoform of Aplysia CPEB. Nat. Struct. Mol. Biol. 2012, 20:495-501.
40. Reisel D., Bannerman D.M., Schmitt W.B., Deacon R.M.J., Flint J., Borchardt T., Seeburg P.H., Rawlins J.N.P. Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci. 2002, 5:868-873.
41. Si K., Giustetto M., Etkin A., Hsu R., Janisiewicz A.M., Miniaci M.C., Kim J.-H., Zhu H., Kandel E.R. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 2003, 115:893-904.
42. Si K., Choi Y.-B., White-Grindley E., Majumdar A., Kandel E.R. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 2010, 140:421-435.
43. Skibinska A., Lech M., Kossut M. PSD95 protein level rises in murine somatosensory cortex after sensory training. Neuroreport 2001, 12:2907-2910.
44. Slipczuk L., Bekinschtein P., Katche C., Cammarota M., Izquierdo I., Medina J.H. BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS ONE 2009, 4:e6007.
45. Smith W.B., Starck S.R., Roberts R.W., Schuman E.M. Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 2005, 45:765-779.
46. Stephan J.S., Fioriti L., Lamba N., Colnaghi L., Karl K., Derkatch I., Kandel E.R. The CPEB3 protein is a functional prion that interacts with the actin cytoskeleton. Cell Rep. 2015, 11. Published online June 11, 2015. 10.1016/j.celrep.2015.04.060.
47. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127:49-58.
48. Theis M., Si K., Kandel E.R. 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 2003, 100:9602-9607.
49. Vnek N., Rothblat L.A. The hippocampus and long-term object memory in the rat. J. Neurosci. 1996, 16:2780-2787.
50. Wu L., Wells D., Tay J., Mendis D., Abbott M.-A., Barnitt A., Quinlan E., Heynen A., Fallon J.R., Richter J.D. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses. Neuron 1998, 21:1129-1139.
51. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., Kaiser K.M., Köster H.J., Borchardt T., Worley P., et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 1999, 284:1805-1811.