Skip to main content
SpringerLink
Log in

Molecular Mechanisms of Early and Late LTP

  • Review Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

LTP is the most intensively studied cellular model of the memory and generally divided at least two distinct phases as early and late. E-LTP requires activation of CaMKII that initiates biochemical events and trafficking of proteins, which eventually potentiate synaptic transmission, and is independent of de novo protein synthesis. In contrast, L-LTP requires gene expression and local protein synthesis regulated via TrkB receptor- and functional prions CPEB2-3-mediated translation. Maintenance of LTP for longer periods depends on constitutively active PKMζ. Throughout this review, current knowledge about early and late phases of LTP will be reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Lomo T Frequency potentiation of excitatory synaptic activity in dentate area of hippocampal formation. Acta Physiol Scand 68: 277

  2. Bliss TV, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Nicoll RA, Schmitz D (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6(11):863

    Article  CAS  PubMed  Google Scholar 

  4. Grover LM, Teyler TJ (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347(6292):477

    Article  CAS  PubMed  Google Scholar 

  5. Wang H, Ardiles AO, Yang S, Tran T, Posada-Duque R, Valdivia G, Baek M, Chuang Y-A, Palacios AG, Gallagher M (2016) Metabotropic glutamate receptors induce a form of LTP controlled by translation and arc signaling in the hippocampus. J Neurosci 36(5):1723–1729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Frey U, Huang Y, Kandel E (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260(5114):1661–1664

    Article  CAS  PubMed  Google Scholar 

  7. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88(5):615–626

    Article  CAS  PubMed  Google Scholar 

  8. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294(5544):1030–1038

    Article  CAS  PubMed  Google Scholar 

  9. Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13(3):169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Herring BE, Nicoll RA (2016) Long-term potentiation: from CaMKII to AMPA receptor trafficking. Annu Rev Physiol 78:351–365

    Article  CAS  PubMed  Google Scholar 

  11. Nicoll RA (2017) A brief history of long-term potentiation. Neuron 93(2):281–290

    Article  CAS  PubMed  Google Scholar 

  12. Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

    Google Scholar 

  13. McNaughton BL, Douglas R, Goddard GV (1978) Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res 157(2):277–293

    Article  CAS  PubMed  Google Scholar 

  14. Levy WB, Steward O (1979) Synapses as associative memory elements in the hippocampal formation. Brain Res 175(2):233–245

    Article  CAS  PubMed  Google Scholar 

  15. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385(6616):533–536

    Article  CAS  PubMed  Google Scholar 

  16. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91(7):927–938

    Article  CAS  PubMed  Google Scholar 

  17. Nevian T, Sakmann B (2006) Spine Ca2+ signaling in spike-timing-dependent plasticity. J Neurosci 26(43):11001–11013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44(1):5–21

    Article  CAS  PubMed  Google Scholar 

  19. Manabe T, Nicoll RA (1994) Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265(5180):1888–1892

    Article  CAS  PubMed  Google Scholar 

  20. Diamond JS, Bergles DE, Jahr CE (1998) Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21(2):425–433

    Article  CAS  PubMed  Google Scholar 

  21. Lüscher C, Malenka RC, Nicoll RA (1998) Monitoring glutamate release during LTP with glial transporter currents. Neuron 21(2):435–441

    Article  PubMed  Google Scholar 

  22. Zakharenko SS, Zablow L, Siegelbaum SA (2001) Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4(7):711

    Article  CAS  PubMed  Google Scholar 

  23. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9(11):813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15(2):427–434

    Article  CAS  PubMed  Google Scholar 

  25. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375(6530):400

    Article  CAS  PubMed  Google Scholar 

  26. Lledo P-M, Zhang X, Südhof TC, Malenka RC, Nicoll RA (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279(5349):399–403

    Article  CAS  PubMed  Google Scholar 

  27. Lüscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24(3):649–658

    Article  PubMed  Google Scholar 

  28. Makino H, Malinow R (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64(3):381–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31

    Article  CAS  PubMed  Google Scholar 

  30. Malenka RC, Nicoll RA (1999) Long-term potentiation–a decade of progress? Science 285(5435):1870–1874

    Article  CAS  PubMed  Google Scholar 

  31. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14(3):311–317

    Article  CAS  PubMed  Google Scholar 

  32. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIα impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36(3):507–519

    Article  CAS  PubMed  Google Scholar 

  33. Chao LH, Pellicena P, Deindl S, Barclay LA, Schulman H, Kuriyan J (2010) Intersubunit capture of regulatory segments is a component of cooperative CaMKII activation. Nat Struct Mol Biol 17(3):264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. De Koninck P, Schulman H (1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279(5348):227–230

    Article  PubMed  Google Scholar 

  35. Pi HJ, Otmakhov N, Lemelin D, De Koninck P, Lisman J (2010) Autonomous CaMKII can promote either long-term potentiation or long-term depression, depending on the state of T305/T306 phosphorylation. J Neurosci 30(26):8704–8709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Incontro S, Díaz-Alonso J, Iafrati J, Vieira M, Asensio CS, Sohal VS, Roche KW, Bender KJ, Nicoll RA (2018) The CaMKII/NMDA receptor complex controls hippocampal synaptic transmission by kinase-dependent and independent mechanisms. Nat Commun 9(1):2069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lledo P-M, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci USA 92(24):11175–11179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pi HJ, Otmakhov N, El Gaamouch F, Lemelin D, De Koninck P, Lisman J (2010) CaMKII control of spine size and synaptic strength: role of phosphorylation states and nonenzymatic action. Proc Natl Acad Sci USA 107(32):14437–14442

    Article  PubMed  PubMed Central  Google Scholar 

  39. Leonard AS, Lim IA, Hemsworth DE, Horne MC, Hell JW (1999) Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. Proc Natl Acad Sci USA 96(6):3239–3244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Strack S, McNeill RB, Colbran RJ (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 275(31):23798–23806

    Article  CAS  PubMed  Google Scholar 

  41. Barria A, Malinow R (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48(2):289–301

    Article  CAS  PubMed  Google Scholar 

  42. Bayer K-U, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411(6839):801

    Article  CAS  PubMed  Google Scholar 

  43. Chen X, Levy JM, Hou A, Winters C, Azzam R, Sousa AA, Leapman RD, Nicoll RA, Reese TS (2015) PSD-95 family MAGUKs are essential for anchoring AMPA and NMDA receptor complexes at the postsynaptic density. Proc Natl Acad Sci USA 112(50):E6983–E6992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shi S-H, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284(5421):1811–1816

    Article  CAS  PubMed  Google Scholar 

  45. Penn A, Zhang C, Georges F, Royer L, Breillat C, Hosy E, Petersen J, Humeau Y, Choquet D (2017) Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors. Nature 549(7672):384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Barria A, Derkach V, Soderling T (1997) Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the α-amino-3-hydroxyl-5-methyl4-isoxazole-propionate-type glutamate receptor. J Biol Chem 272(52):32727–32730

    Article  CAS  PubMed  Google Scholar 

  47. Mammen AL, Kameyama K, Roche KW, Huganir RL (1997) Phosphorylation of the α-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem 272(51):32528–32533

    Article  CAS  PubMed  Google Scholar 

  48. Esteban JA, Shi S-H, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6(2):136

    Article  CAS  PubMed  Google Scholar 

  49. Boehm J, Kang M-G, Johnson RC, Esteban J, Huganir RL, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51(2):213–225

    Article  CAS  PubMed  Google Scholar 

  50. Lee H-K, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405(6789):955

    Article  CAS  PubMed  Google Scholar 

  51. Kristensen AS, Jenkins MA, Banke TG, Schousboe A, Makino Y, Johnson RC, Huganir R, Traynelis SF (2011) Mechanism of Ca 2+/calmodulin-dependent kinase II regulation of AMPA receptor gating. Nat Neurosci 14(6):727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lee H-K, Takamiya K, Han J-S, Man H, Kim C-H, Rumbaugh G, Yu S, Ding L, He C, Petralia RS (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112(5):631–643

    Article  CAS  PubMed  Google Scholar 

  53. Lee H-K, Takamiya K, He K, Song L, Huganir RL (2009) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103(1):479–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Opazo P, Choquet D (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46(1):1–8

    Article  CAS  PubMed  Google Scholar 

  55. Hayashi Y, Shi S-H, Esteban JA, Piccini A, Poncer J-C, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287(5461):2262–2267

    Article  CAS  PubMed  Google Scholar 

  56. Shi S-H, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105(3):331–343

    Article  CAS  PubMed  Google Scholar 

  57. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62(3):405–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zamanillo D, Sprengel R, Hvalby Ø, Jensen V, Burnashev N, Rozov A, Kaiser KM, Köster HJ, Borchardt T, Worley P (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284(5421):1805–1811

    Article  CAS  PubMed  Google Scholar 

  59. Meng Y, Zhang Y, Jia Z (2003) Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 39(1):163–176

    Article  CAS  PubMed  Google Scholar 

  60. Jackson AC, Nicoll RA (2011) The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70(2):178–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Sumioka A, Brown TE, Kato AS, Bredt DS, Kauer JA, Tomita S (2011) PDZ binding of TARPγ-8 controls synaptic transmission but not synaptic plasticity. Nat Neurosci 14(11):1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Sumioka A, Yan D, Tomita S (2010) TARP phosphorylation regulates synaptic AMPA receptors through lipid bilayers. Neuron 66(5):755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67(2):239–252

    Article  CAS  PubMed  Google Scholar 

  64. Hafner A-S, Penn AC, Grillo-Bosch D, Retailleau N, Poujol C, Philippat A, Coussen F, Sainlos M, Opazo P, Choquet D (2015) Lengthening of the stargazin cytoplasmic tail increases synaptic transmission by promoting interaction to deeper domains of PSD-95. Neuron 86(2):475–489

    Article  CAS  PubMed  Google Scholar 

  65. Park J, Chávez AE, Mineur YS, Morimoto-Tomita M, Lutzu S, Kim KS, Picciotto MR, Castillo PE, Tomita S (2016) CaMKII phosphorylation of TARPγ-8 is a mediator of LTP and learning and memory. Neuron 92(1):75–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Granger AJ, Shi Y, Lu W, Cerpas M, Nicoll RA (2013) LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493(7433):495

    Article  CAS  PubMed  Google Scholar 

  67. Walkup IVWG, Mastro TL, Schenker LT, Vielmetter J, Hu R, Iancu A, Reghunathan M, Bannon BD, Kennedy MB (2016) A model for regulation by SynGAP-α1 of binding of synaptic proteins to PDZ-domain’Slots’ in the postsynaptic density. Elife 5:e16813

    Article  PubMed  PubMed Central  Google Scholar 

  68. Sheng N, Bemben MA, Díaz-Alonso J, Tao W, Shi YS, Nicoll RA (2018) LTP requires postsynaptic PDZ-domain interactions with glutamate receptor/auxiliary protein complexes. Proc Natl Acad Sci USA 115(15):3948–3953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82(2):444–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Patriarchi T, Buonarati OR, Hell JW (2018) Postsynaptic localization and regulation of AMPA receptors and Cav1. 2 by β2 adrenergic receptor/PKA and Ca2+/CaMKII signaling. EMBO J 37(20):e99771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Araki Y, Zeng M, Zhang M, Huganir RL (2015) Rapid dispersion of SynGAP from synaptic spines triggers AMPA receptor insertion and spine enlargement during LTP. Neuron 85(1):173–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R (2002) Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110(4):443–455

    Article  CAS  PubMed  Google Scholar 

  73. Walkup IVWG, Sweredoski MJ, Graham RL, Hess S, Kennedy MB (2018) Phosphorylation of synaptic GTPase-activating protein (synGAP) by polo-like kinase (Plk2) alters the ratio of its GAP activity toward HRas, Rap1 and Rap2 GTPases. Biochem Biophys Res Commun 503(3):1599–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Herring BE, Nicoll RA (2016) Kalirin and Trio proteins serve critical roles in excitatory synaptic transmission and LTP. Proc Natl Acad Sci USA 113(8):2264–2269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Penzes P, Cahill ME, Jones KA, Srivastava DP (2008) Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol 18(9):405–413

    Article  CAS  PubMed  Google Scholar 

  76. Murakoshi H, Wang H, Yasuda R (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472(7341):100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kim IH, Wang H, Soderling SH, Yasuda R (2014) Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall. Elife 3:e02839

    Article  PubMed Central  Google Scholar 

  78. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63(1):92–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Correia SS, Bassani S, Brown TC, Lisé M-F, Backos DS, El-Husseini A, Passafaro M, Esteban JA (2008) Motor protein–dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 11(4):457

    Article  CAS  PubMed  Google Scholar 

  80. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li X-d, Davison IG, Ikebe M, Mercer JA, Kauer JA (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135(3):535–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. da Silva ME, Adrian M, Schätzle P, Lipka J, Watanabe T, Cho S, Futai K, Wierenga CJ, Kapitein LC, Hoogenraad CC (2015) Positioning of AMPA receptor-containing endosomes regulates synapse architecture. Cell Rep 13(5):933–943

    Article  CAS  Google Scholar 

  82. Wu D, Bacaj T, Morishita W, Goswami D, Arendt KL, Xu W, Chen L, Malenka RC, Südhof TC (2017) Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP. Nature 544(7650):316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Maximov A, Tang J, Yang X, Pang ZP, Südhof TC (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323(5913):516–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ahmad M, Polepalli JS, Goswami D, Yang X, Kaeser-Woo YJ, Südhof TC, Malenka RC (2012) Postsynaptic complexin controls AMPA receptor exocytosis during LTP. Neuron 73(2):260–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Jurado S, Goswami D, Zhang Y, Molina AJM, Südhof TC, Malenka RC (2013) LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77(3):542–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Dong H, O’brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386(6622):279

    Article  CAS  PubMed  Google Scholar 

  87. Chung HJ, Xia J, Scannevin RH, Zhang X, Huganir RL (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci 20(19):7258–7267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Hayashi T, Huganir RL (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J Neurosci 24(27):6152–6160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Shin H, Wyszynski M, Huh K-H, Valtschanoff JG, Lee J-R, Ko J, Streuli M, Weinberg RJ, Sheng M, Kim E (2003) Association of the kinesin motor KIF1A with the multimodular protein liprin-α. J Biol Chem 278(13):11393–11401

    Article  CAS  PubMed  Google Scholar 

  90. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22(3):461–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Pfennig S, Foss F, Bissen D, Harde E, Treeck JC, Segarra M, Acker-Palmer A (2017) GRIP1 Binds to ApoER2 and EphrinB2 to induce activity-dependent AMPA receptor insertion at the synapse. Cell Rep 21(1):84–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Ye B, Liao D, Zhang X, Zhang P, Dong H, Huganir RL (2000) GRASP-1: a neuronal RasGEF associated with the AMPA receptor/GRIP complex. Neuron 26(3):603–617

    Article  CAS  PubMed  Google Scholar 

  93. Hoogenraad CC, Popa I, Futai K, Sanchez-Martinez E, Wulf PS, Van Vlijmen T, Dortland BR, Oorschot V, Govers R, Monti M (2010) Neuron specific Rab4 effector GRASP-1 coordinates membrane specialization and maturation of recycling endosomes. PLoS Biol 8(1):e1000283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Chiu S-L, Diering GH, Ye B, Takamiya K, Chen C-M, Jiang Y, Niranjan T, Schwartz CE, Wang T, Huganir RL (2017) GRASP1 regulates synaptic plasticity and learning through endosomal recycling of AMPA receptors. Neuron 93(6):1405–1419. e1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Moretto E, Passafaro M (2018) Recent findings on AMPA receptor recycling. Front Cell Neurosci 12:286

    Article  PubMed  PubMed Central  Google Scholar 

  96. Fiuza M, Rostosky CM, Parkinson GT, Bygrave AM, Halemani N, Baptista M, Milosevic I, Hanley JG (2017) PICK1 regulates AMPA receptor endocytosis via direct interactions with AP2 α-appendage and dynamin. J Cell Biol 216(10):3323–3338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Abraham WC (2003) How long will long-term potentiation last? Philos Trans R Soc Lond B Biol Sci 358(1432):735–744

    Article  PubMed  PubMed Central  Google Scholar 

  98. Bosch M, Hayashi Y (2012) Structural plasticity of dendritic spines. Curr Opin Neurobiol 22(3):383–388

    Article  CAS  PubMed  Google Scholar 

  99. Bailey CH, Kandel ER, Harris KM (2015) Structural components of synaptic plasticity and memory consolidation. Cold Spring Harb Perspect Biol 7(7):a021758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Huang Y-Y, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1(1):74–82

    CAS  PubMed  Google Scholar 

  101. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265(5175):1104–1107

    Article  CAS  PubMed  Google Scholar 

  102. Eliot LS, Dudai Y, Kandel ER, Abrams TW (1989) Ca2+/calmodulin sensitivity may be common to all forms of neural adenylate cyclase. Proc Natl Acad Sci USA 86(23):9564–9568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Tang W-J, Gilman AG (1991) Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. Science 254(5037):1500–1503

    Article  CAS  PubMed  Google Scholar 

  104. Nguyen P, Woo N (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71(6):401–437

    Article  CAS  PubMed  Google Scholar 

  105. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79(1):59–68

    Article  CAS  PubMed  Google Scholar 

  106. Greengard P, Jen J, Nairn AC, Stevens CF (1991) Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253(5024):1135–1138

    Article  CAS  PubMed  Google Scholar 

  107. Yeckel MF, Kapur A, Johnston D (1999) Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2(7):625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272(31):19103–19106

    Article  CAS  PubMed  Google Scholar 

  109. Vossler MR, Yao H, York RD, Pan M-G, Rim CS, Stork PJ (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf-and Rap1-dependent pathway. Cell 89(1):73–82

    Article  CAS  PubMed  Google Scholar 

  110. Morozov A, Muzzio IA, Bourtchouladze R, Van-Strien N, Lapidus K, Yin D, Winder DG, Adams JP, Sweatt JD, Kandel ER (2003) Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39(2):309–325

    Article  CAS  PubMed  Google Scholar 

  111. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32(1):123–140

    Article  CAS  PubMed  Google Scholar 

  112. Boglári G, Erhardt P, Cooper GM, Szeberényi J (1998) Intact Ras function is required for sustained activation and nuclear translocation of extracellular signal-regulated kinases in nerve growth factor-stimulated PC12 cells. Eur J Cell Biol 75(1):54–58

    Article  PubMed  Google Scholar 

  113. Thomson S, Mahadevan LC, Clayton AL (1999) MAP kinase-mediated signalling to nucleosomes and immediate-early gene induction. Semin Cell Dev Biol 10(2):205–214

    Article  CAS  PubMed  Google Scholar 

  114. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B 358(1432):805–814

    Article  CAS  Google Scholar 

  115. Veyrac A, Besnard A, Caboche J, Davis S, Laroche S (2014) The transcription factor Zif268/Egr1, brain plasticity, and memory. Prog Mol Biol Transl Sci 122:89–129

    Article  CAS  PubMed  Google Scholar 

  116. Christy B, Nathans D (1989) DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci USA 86(22):8737–8741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Worley PF, Christy BA, Nakabeppu Y, Bhat RV, Cole AJ, Baraban JM (1991) Constitutive expression of zif268 in neocortex is regulated by synaptic activity. Proc Natl Acad Sci USA 88(12):5106–5110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340(6233):474

    Article  CAS  PubMed  Google Scholar 

  119. Abraham WC, Dragunow M, Tate WP (1991) The role of immediate early genes in the stabilization of long-term potentiation. Mol Neurobiol 5(2–4):297

    Article  CAS  PubMed  Google Scholar 

  120. Richardson C, Tate W, Mason S, Lawlor P, Dragunow M, Abraham W (1992) Correlation between the induction of an immediate early gene, zif/268, and long-term potentiation in the dentate gyrus. Brain Res 580(1–2):147–154

    Article  CAS  PubMed  Google Scholar 

  121. Abraham W, Mason S, Demmer J, Williams J, Richardson C, Tate WEEA, Lawlor P, Dragunow M (1993) Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 56(3):717–727

    Article  CAS  PubMed  Google Scholar 

  122. Jones M, Errington M, French P, Fine A, Bliss T, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4(3):289

    Article  CAS  PubMed  Google Scholar 

  123. James AB, Conway A-M, Morris BJ (2005) Genomic profiling of the neuronal target genes of the plasticity-related transcription factor-Zif268. J Neurochem 95(3):796–810

    Article  CAS  PubMed  Google Scholar 

  124. Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21(4):741–751

    Article  CAS  PubMed  Google Scholar 

  125. Moga D, Calhoun M, Chowdhury A, Worley P, Morrison J, Shapiro M (2004) Activity-regulated cytoskeletal-associated protein is localized to recently activated excitatory synapses. Neuroscience 125(1):7–11

    Article  CAS  PubMed  Google Scholar 

  126. Rodriguez J, Davies H, Silva A, De Souza I, Peddie C, Colyer F, Lancashire C, Fine A, Errington M, Bliss T (2005) Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arg3. 1 protein expression in spines, dendrites and glia. European J Neurosci 21(9):2384–2396

    Article  CAS  Google Scholar 

  127. Panja D, Dagyte G, Bidinosti M, Wibrand K, Kristiansen Å-M, Sonenberg N, Bramham CR (2009) Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J Biol Chem 284(46):31498–31511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A (2010) The Arc of synaptic memory. Exp Brain Res 200(2):125–140

    Article  PubMed  Google Scholar 

  129. Waltereit R, Dammermann B, Wulff P, Scafidi J, Staubli U, Kauselmann G, Bundman M, Kuhl D (2001) Arg3. 1/Arc mRNA induction by Ca2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J Neurosci 21(15):5484–5493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Messaoudi E, Kanhema T, Soulé J, Tiron A, Dagyte G, da Silva B, Bramham CR (2007) Sustained Arc/Arg3. 1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27(39):10445–10455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Nikolaienko O, Patil S, Eriksen MS, Bramham CR (2017) Arc protein: a flexible hub for synaptic plasticity and cognition. Semin Cell Dev Biol 77:33–42

    Article  CAS  PubMed  Google Scholar 

  132. Nair RR, Patil S, Tiron A, Kanhema T, Panja D, Schiro L, Parobczak K, Wilczynski G, Bramham CR (2017) Dynamic Arc SUMOylation and selective interaction with F-actin-binding protein drebrin A in LTP consolidation in vivo. Front Synaptic Neurosci 9:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Newpher TM, Harris S, Pringle J, Hamilton C, Soderling S Regulation of spine structural plasticity by Arc/Arg3. 1. Semin Cell Dev Biol 77:25–32

  134. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3. 1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52(3):445–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. DaSilva LL, Wall MJ, de Almeida LP, Wauters SC, Januário YC, Müller J, Corrêa SA (2016) Activity-regulated cytoskeleton-associated protein controls AMPAR endocytosis through a direct interaction with clathrin-adaptor protein 2. eNeuro. https://doi.org/10.1523/ENEURO.0144-15.2016

    Article  PubMed  PubMed Central  Google Scholar 

  136. Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3. 1 with CaMKIIβ. Cell 149(4):886–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Fiete IR, Senn W, Wang CZ, Hahnloser RH (2010) Spike-time-dependent plasticity and heterosynaptic competition organize networks to produce long scale-free sequences of neural activity. Neuron 65(4):563–576

    Article  CAS  PubMed  Google Scholar 

  138. Okuno H, Minatohara K, Bito H (2017) Inverse synaptic tagging: an inactive synapse-specific mechanism to capture activity-induced Arc/arg3. 1 and to locally regulate spatial distribution of synaptic weights. Semin Cell Dev Biol 77:43–50

    Article  CAS  PubMed  Google Scholar 

  139. Korb E, Wilkinson CL, Delgado RN, Lovero KL, Finkbeiner S (2013) Arc in the nucleus regulates PML-dependent GluA1 transcription and homeostatic plasticity. Nat Neurosci 16(7):874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Nikolaienko O, Eriksen MS, Patil S, Bito H, Bramham CR (2017) Stimulus-evoked ERK-dependent phosphorylation of activity-regulated cytoskeleton-associated protein (Arc) regulates its neuronal subcellular localization. Neuroscience 360:68–80

    Article  CAS  PubMed  Google Scholar 

  141. Wee CL, Teo S, Oey NE, Wright GD, VanDongen HM, VanDongen AM (2014) Nuclear arc interacts with the histone acetyltransferase tip60 to modify H4K12 acetylation. eNeuro:ENEURO. 0019-0014.2014

  142. Martin KC, Kosik KS (2002) Synaptic tagging—who’s it? Nat Rev Neurosci 3(10):813

    Article  CAS  PubMed  Google Scholar 

  143. Steward O, Levy WB (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2(3):284–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Leßmann V, Brigadski T (2009) Mechanisms, locations, and kinetics of synaptic BDNF secretion: an update. Neurosci Res 65(1):11–22

    Article  CAS  PubMed  Google Scholar 

  145. Dieni S, Matsumoto T, Dekkers M, Rauskolb S, Ionescu MS, Deogracias R, Gundelfinger ED, Kojima M, Nestel S, Frotscher M (2012) BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol 196:775–788

    Article  CAS  Google Scholar 

  146. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20(21):5887–5897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Lin P-Y, Kavalali ET, Monteggia LM (2018) Genetic Dissection of Presynaptic and Postsynaptic BDNF-TrkB Signaling in Synaptic Efficacy of CA3-CA1 Synapses. Cell Rep 24(6):1550–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Tanaka J-i, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GC, Kasai H (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319(5870):1683–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Harward SC, Hedrick NG, Hall CE, Parra-Bueno P, Milner TA, Pan E, Laviv T, Hempstead BL, Yasuda R, McNamara JO (2016) Autocrine BDNF–TrkB signalling within a single dendritic spine. Nature 538(7623):99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Park H, Poo M-m (2013) Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14(1):7

    Article  CAS  PubMed  Google Scholar 

  151. Kang H, Welcher AA, Shelton D, Schuman EM (1997) Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19(3):653–664

    Article  CAS  PubMed  Google Scholar 

  152. Lu Y, Ji Y, Ganesan S, Schloesser R, Martinowich K, Sun M, Mei F, Chao MV, Lu B (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31(33):11762–11771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10(3):381–391

    Article  CAS  PubMed  Google Scholar 

  154. Troca-Marín JA, Alves-Sampaio A, Montesinos ML (2011) An increase in basal BDNF provokes hyperactivation of the Akt-mammalian target of rapamycin pathway and deregulation of local dendritic translation in a mouse model of Down’s syndrome. J Neurosci 31(26):9445–9455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Panja D, Bramham CR (2014) BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76:664–676

    Article  CAS  PubMed  Google Scholar 

  156. Sossin WS, Costa-Mattioli M (2018) Translational control in the brain in health and disease. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a032912

    Article  Google Scholar 

  157. Briz V, Hsu Y-T, Li Y, Lee E, Bi X, Baudry M (2013) Calpain-2-mediated PTEN degradation contributes to BDNF-induced stimulation of dendritic protein synthesis. J Neurosci 33(10):4317–4328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Wang Y, Zhu G, Briz V, Hsu Y-T, Bi X, Baudry M (2014) A molecular brake controls the magnitude of long-term potentiation. Nat Commun 5:3051

    Article  CAS  PubMed  Google Scholar 

  159. Baudry M, Zhu G, Liu Y, Wang Y, Briz V, Bi X (2015) Multiple cellular cascades participate in long-term potentiation and in hippocampus-dependent learning. Brain Res 1621:73–81

    Article  CAS  PubMed  Google Scholar 

  160. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E, Wu D, Saule E, Bouschet T (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53(5):703–717

    Article  CAS  PubMed  Google Scholar 

  161. Huang Y-WA, Ruiz CR, Eyler EC, Lin K, Meffert MK (2012) Dual regulation of miRNA biogenesis generates target specificity in neurotrophin-induced protein synthesis. Cell 148(5):933–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Amen AM, Ruiz-Garzon CR, Shi J, Subramanian M, Pham DL, Meffert MK (2017) A rapid induction mechanism for Lin28a in trophic responses. Mol Cell 65(3):490–503. e497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung W-H, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306(5695):487–491

    Article  CAS  PubMed  Google Scholar 

  164. Barco A, Patterson S, Alarcon JM, Gromova P, Mata-Roig M, Morozov A, Kandel ER (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48(1):123–137

    Article  CAS  PubMed  Google Scholar 

  165. Si K, Lindquist S, Kandel ER (2003) A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115(7):879–891

    Article  CAS  PubMed  Google Scholar 

  166. Si K, Choi Y-B, White-Grindley E, Majumdar A, Kandel ER (2010) Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140(3):421–435

    Article  CAS  PubMed  Google Scholar 

  167. Keleman K, Krüttner S, Alenius M, Dickson BJ (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 10(12):1587

    Article  CAS  PubMed  Google Scholar 

  168. Krüttner S, Stepien B, Noordermeer JN, Mommaas MA, Mechtler K, Dickson BJ, Keleman K (2012) Drosophila CPEB Orb2A mediates memory independent of Its RNA-binding domain. Neuron 76(2):383–395

    Article  CAS  PubMed  Google Scholar 

  169. Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F, Li L, Choi EM-L, Kannan K, Guo F, Unruh J (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148(3):515–529

    Article  CAS  PubMed  Google Scholar 

  170. Fiumara F, Rajasethupathy P, Antonov I, Kosmidis S, Sossin WS, Kandel ER (2015) MicroRNA-22 gates long-term heterosynaptic plasticity in Aplysia through presynaptic regulation of CPEB and downstream targets. Cell Rep 11(12):1866–1875

    Article  CAS  PubMed  Google Scholar 

  171. Krüttner S, Traunmüller L, Dag U, Jandrasits K, Stepien B, Iyer N, Fradkin LG, Noordermeer JN, Mensh BD, Keleman K (2015) Synaptic Orb2A bridges memory acquisition and late memory consolidation in Drosophila. Cell Rep 11(12):1953–1965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Theis M, Si K, Kandel ER (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(16):9602–9607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Lu W-H, Yeh N-H, Huang Y-S (2017) CPEB2 Activates GRASP1 mRNA Translation and Promotes AMPA Receptor Surface Expression, Long-Term Potentiation, and Memory. Cell Rep 21(7):1783–1794

    Article  CAS  PubMed  Google Scholar 

  174. Huang YS, Kan MC, Lin CL, Richter JD (2006) CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J 25(20):4865–4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Fioriti L, Myers C, Huang Y-Y, Li X, Stephan JS, Trifilieff P, Colnaghi L, Kosmidis S, Drisaldi B, Pavlopoulos E (2015) The persistence of hippocampal-based memory requires protein synthesis mediated by the prion-like protein CPEB3. Neuron 86(6):1433–1448

    Article  CAS  PubMed  Google Scholar 

  176. Si K, Kandel ER (2016) The role of functional prion-like proteins in the persistence of memory. Cold Spring Harb Perspect Biol 8(4):a021774

    Article  PubMed  PubMed Central  Google Scholar 

  177. Pavlopoulos E, Trifilieff P, Chevaleyre V, Fioriti L, Zairis S, Pagano A, Malleret G, Kandel ER (2011) Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147(6):1369–1383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Drisaldi B, Colnaghi L, Fioriti L, Rao N, Myers C, Snyder AM, Metzger DJ, Tarasoff J, Konstantinov E, Fraser PE (2015) SUMOylation is an inhibitory constraint that regulates the prion-like aggregation and activity of CPEB3. Cell Rep 11(11):1694–1702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Gebauer F, Richter JD (1996) Mouse cytoplasmic polyadenylylation element binding protein: an evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc Natl Acad Sci USA 93(25):14602–14607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, Miniaci MC, Kim J-H, Zhu H, Kandel ER (2003) A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115(7):893–904

    Article  CAS  PubMed  Google Scholar 

  181. Sacktor TC (2011) How does PKMζ maintain long-term memory? Nat Rev Neurosci 12(1):9

    Article  CAS  PubMed  Google Scholar 

  182. Sacktor TC (2008) PKMζ, LTP maintenance, and the dynamic molecular biology of memory storage. Prog Brain Res 169:27–40

    Article  CAS  PubMed  Google Scholar 

  183. Yu N-K, Uhm H, Shim J, Choi J-H, Bae S, Sacktor TC, Hohng S, Kaang B-K (2017) Increased PKMζ activity impedes lateral movement of GluA2-containing AMPA receptors. Mol Brain 10(1):56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Muslimov IA, Nimmrich V, Hernandez AI, Tcherepanov A, Sacktor TC, Tiedge H (2004) Dendritic transport and localization of protein kinase mζ mrna implications for molecular memory consolidation. J Biol Chem 279(50):52613–52622

    Article  CAS  PubMed  Google Scholar 

  185. Westmark PR, Westmark CJ, Wang S, Levenson J, O’Riordan KJ, Burger C, Malter JS (2010) Pin1 and PKMζ sequentially control dendritic protein synthesis. Sci Signal 3(112):ra18–ra18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Kelly MT, Crary JF, Sacktor TC (2007) Regulation of protein kinase Mζ synthesis by multiple kinases in long-term potentiation. J Neurosci 27(13):3439–3444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Hsieh C, Tsokas P, Serrano P, Hernández AI, Tian D, Cottrell JE, Shouval HZ, Fenton AA, Sacktor TC (2017) Persistent increased PKMζ in long-term and remote spatial memory. Neurobiol Learn Mem 138:135–144

    Article  CAS  PubMed  Google Scholar 

  188. Mastushita-Sakai T, White-Grindley E, Samuelson J, Seidel C, Si K (2010) Drosophila Orb2 targets genes involved in neuronal growth, synapse formation, and protein turnover. Proc Natl Acad Sci USA 107(26):11987–11992

    Article  PubMed  PubMed Central  Google Scholar 

  189. Araki Y, Lin D-T, Huganir RL (2010) Plasma membrane insertion of the AMPA receptor GluA2 subunit is regulated by NSF binding and Q/R editing of the ion pore. Proc Natl Acad Sci USA 107(24):11080–11085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Hanley JG, Khatri L, Hanson PI, Ziff EB (2002) NSF ATPase and α-/β-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34(1):53–67

    Article  CAS  PubMed  Google Scholar 

  191. Yao Y, Kelly MT, Sajikumar S, Serrano P, Tian D, Bergold PJ, Frey JU, Sacktor TC (2008) PKMζ maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28(31):7820–7827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Lee AM, Kanter BR, Wang D, Lim JP, Zou ME, Qiu C, McMahon T, Dadgar J, Fischbach-Weiss SC, Messing RO (2013) Prkcz null mice show normal learning and memory. Nature 493(7432):416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Volk LJ, Bachman JL, Johnson R, Yu Y, Huganir RL (2013) PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory. Nature 493(7432):420

    Article  CAS  PubMed  Google Scholar 

  194. Tsokas P, Hsieh C, Yao Y, Lesburgueres E, Wallace EJC, Tcherepanov A, Jothianandan D, Hartley BR, Pan L, Rivard B (2016) Compensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice. Elife 5:e14846

    Article  PubMed  PubMed Central  Google Scholar 

  195. Wang S, Sheng T, Ren S, Tian T, Lu W (2016) Distinct roles of PKCι/λ and PKMζ in the initiation and maintenance of hippocampal long-term potentiation and memory. Cell Rep 16(7):1954–1961

    Article  CAS  PubMed  Google Scholar 

  196. Matt L, Hell JW (2013) PKCλ: a new player in LTP coming to the rescue of PKCζ’s faltering role in LTP? EMBO J 32(10):1348–1349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Ren SQ, Yan JZ, Zhang XY, Bu YF, Pan WW, Yao W, Tian T, Lu W (2013) PKCλ is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP. EMBO J 32(10):1365–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Medicine, Department of Physiology, Selcuk University, 42031, Konya, Turkey

    Saltuk Bugra Baltaci, Rasim Mogulkoc & Abdulkerim Kasim Baltaci

Authors
  1. Saltuk Bugra Baltaci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rasim Mogulkoc
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdulkerim Kasim Baltaci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdulkerim Kasim Baltaci.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baltaci, S.B., Mogulkoc, R. & Baltaci, A.K. Molecular Mechanisms of Early and Late LTP. Neurochem Res 44, 281–296 (2019). https://doi.org/10.1007/s11064-018-2695-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-018-2695-4

Keywords

Search

Navigation