Skip to main content
SpringerLink
Log in

PKA Anchoring and Synaptic Tagging and Capture

  • Chapter
  • First Online:
Synaptic Tagging and Capture

Abstract

Synaptic tagging and capture (STC) hypothesis has been receiving increasing attention because it reflects heterosynaptic association of information processing during memory formation in the brain. Indeed, electrophysiological and behavioral studies suggest that STC is a better cellular model for memory formation than the conventional homosynaptic experiment. In STC, a short-lasting potentiation in one pathway becomes persistent when it is paired with a long-lasting potentiation in the other independent pathway. It has been proposed that the setting of synapse-specific tag and capture of non-synapse-specific diffusible gene products by the tag determines the fate of each pathway. However, the mechanism of STC is still elusive and three major questions should be answered: (1) What is the tag and how does it modulate synapse-specific plasticity? (2) How does the tag capture gene products? (3) What are the gene products and how are they produced? Although several molecules and processes have been suggested to answer to these questions, they only provide partial explanations about the phenomenon. Here, this article will discuss how PKA modulates synapse-specific neuronal processing by coordinating signaling molecules and processes through PKA anchoring proteins, and how anchored PKA is involved in the generation and capture of plasticity-related gene products. Having PKA as a key molecule, the goal of this article is to provide a unified model of STC that addresses the key questions.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aakalu G, Smith WB, Nguyen N et al (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30:489–502

    PubMed  CAS  Google Scholar 

  • Abel T, Nguyen PV, Barad M et al (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615–626

    PubMed  CAS  Google Scholar 

  • Auer RN, Jensen ML, Whishaw IQ (1989) Neurobehavioral deficit due to ischemic brain damage limited to half of the CA1 sector of the hippocampus. J Neurosci 9:1641–1647

    PubMed  CAS  Google Scholar 

  • Baillie GS, Sood A, McPhee I et al (2003) Beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci U S A 100:940–945. doi:10.1073/pnas.262787199

  • Ballarini F, Moncada D, Martinez MC et al (2009) Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci U S A 106:14599–14604

    PubMed  CAS  PubMed Central  Google Scholar 

  • Banke TG, Bowie D, Lee H et al (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89–102

    PubMed  CAS  Google Scholar 

  • Barad M, Bourtchouladze R, Winder DG et al (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci U S A 95:15020–15025

    PubMed  CAS  PubMed Central  Google Scholar 

  • Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703

    PubMed  CAS  Google Scholar 

  • Barco A, Patterson SL, Patterson S et al (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 48:123–137

    PubMed  CAS  Google Scholar 

  • Barondes SH, Jarvik ME (1964) The influence of actinomycin-D on brain RNA synthesis and on memory. J Neurochem 11:187–195

    PubMed  CAS  Google Scholar 

  • Benarroch EE (2013) HCN channels: function and clinical implications. Neurology 80:304–310

    PubMed  Google Scholar 

  • Bernabeu R, Bevilaqua L, Ardenghi P et al (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc Natl Acad Sci U S A 94:7041–7046

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blitzer RD, Connor JH, Brown GP et al (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940–1942

    PubMed  CAS  Google Scholar 

  • Bolshakov VY, Golan H, Kandel ER, Siegelbaum S (1997) Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19:635–651

    PubMed  CAS  Google Scholar 

  • Brandon NJ, Jovanovic JN, Colledge M et al (2003) A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor beta subunits. Mol Cell Neurosci 22:87–97

    PubMed  CAS  Google Scholar 

  • Bregman DB, Bhattacharyya N, Rubin CS (1989) High affinity binding protein for the regulatory subunit of cAMP-dependent protein kinase II-B. Cloning, characterization, and expression of cDNAs for rat brain P150. J Biol Chem 264:4648–4656

    PubMed  CAS  Google Scholar 

  • Carr DW, Stofko-Hahn RE, Fraser ID et al (1992) Localization of the cAMP-dependent protein kinase to the postsynaptic densities by A-kinase anchoring proteins. Characterization of AKAP 79. J Biol Chem 267:16816–16823

    PubMed  CAS  Google Scholar 

  • Casadio A, Martin KC, Giustetto M et al (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237

    PubMed  CAS  Google Scholar 

  • Chavez-Noriega LE, Stevens CF (1994) Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14:310–317

    PubMed  CAS  Google Scholar 

  • Chen LY, Rex CS, Casale MS et al (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363–5372

    PubMed  CAS  Google Scholar 

  • Coghlan VM, Perrino BA, Howard M et al (1995) Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267:108–111

    PubMed  CAS  Google Scholar 

  • Colledge M, Scott JD (1999) AKAPs: from structure to function. Trends Cell Biol 9:216–221

    PubMed  CAS  Google Scholar 

  • Colledge M, Dean RA, Scott GK et al (2000) Targeting of PKA to glutamate receptors through a MAGUK–AKAP complex. Neuron 27:107–119

    PubMed  CAS  Google Scholar 

  • Connor SA, Wang YT, Nguyen PV (2011) Activation of {beta}-adrenergic receptors facilitates heterosynaptic translation-dependent long-term potentiation. J Physiol 589:4321–4340

    PubMed  CAS  PubMed Central  Google Scholar 

  • Daaka Y, Luttrell LM, Lefkowitz RJ (1997) Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390:88–91

    PubMed  CAS  Google Scholar 

  • Esteban JA, Shi S-H, Wilson C et al (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136–143

    PubMed  CAS  Google Scholar 

  • Feliciello A, Giuliano P, Porcellini A et al (1996) The v-Ki-Ras oncogene alters cAMP nuclear signaling by regulating the location and the expression of cAMP-dependent protein kinase IIbeta. J Biol Chem 271:25350–25359

    PubMed  CAS  Google Scholar 

  • Feliciello A, Li Y, Avvedimento EV et al (1997) A-kinase anchor protein 75 increases the rate and magnitude of cAMP signaling to the nucleus. Curr Biol 7:1011–1014

    PubMed  CAS  Google Scholar 

  • Fraser ID, Cong M, Kim J et al (2000) Assembly of an A kinase-anchoring protein-beta(2)-adrenergic receptor complex facilitates receptor phosphorylation and signaling. Curr Biol 10:409–412

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frey U, Morris RG (1998) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545–552

    PubMed  CAS  Google Scholar 

  • Frey U, Krug M, Reymann KG, Matthies H (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  CAS  Google Scholar 

  • Frey U, Matthies H, Reymann KG (1991) The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129:111–114

    PubMed  CAS  Google Scholar 

  • Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664

    PubMed  CAS  Google Scholar 

  • Frey U, Frey S, Schollmeier F, Krug M (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol 490(Pt 3):703–711

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gao T, Yatani A, Dell’Acqua ML et al (1997) cAMP-dependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19:185–196

    PubMed  CAS  Google Scholar 

  • Garner CC, Tucker RP, Matus A (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336:674–677. doi:10.1038/336674a0

  • Gelinas JN, Nguyen PV (2005) Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 25:3294–3303

    PubMed  CAS  Google Scholar 

  • Gelinas JN, Tenorio G, Lemon N et al (2008) Beta-adrenergic receptor activation during distinct patterns of stimulation critically modulates the PKA-dependence of LTP in the mouse hippocampus. Learn Mem 15:281–289

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gelman IH, Lee K, Tombler E et al (1998) Control of cytoskeletal architecture by the src-suppressed C kinase substrate, SSeCKS. Cell Motil Cytoskeleton 41:1–17

    PubMed  CAS  Google Scholar 

  • Gerits N, Kostenko S, Shiryaev A et al (2008) Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell Signal 20:1592–1607

    PubMed  CAS  Google Scholar 

  • Gomez LL, Alam S, Smith KE et al (2002) Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J Neurosci 22:7027–7044

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gu J, Lee CW, Fan Y et al (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208–1215

    PubMed  CAS  PubMed Central  Google Scholar 

  • Harada A, Teng J, Takei Y et al (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541–549

    PubMed  CAS  PubMed Central  Google Scholar 

  • Havekes R, Canton D, Park AJ et al (2012) Gravin orchestrates protein kinase A and β2-adrenergic receptor signaling critical for synaptic plasticity and memory. J Neurosci 32:18137–18149

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hoshi N, Zhang J-S, Omaki M et al (2003) AKAP150 signaling complex promotes suppression of the M-current by muscarinic agonists. Nat Neurosci 6:564–571

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hou Y-Y, Lu B, Li M et al (2009) Involvement of actin rearrangements within the amygdala and the dorsal hippocampus in aversive memories of drug withdrawal in acute morphine-dependent rats. J Neurosci 29:12244–12254

    PubMed  CAS  Google Scholar 

  • Huang YY, 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 1:74–82. doi:10.1101/lm.1.1.74

  • Huang T, McDonough CB, Abel T (2006) Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. Eur J Cell Biol 85:635–642

    PubMed  CAS  PubMed Central  Google Scholar 

  • Impey S, Mark M, Villacres EC et al (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973–982

    PubMed  CAS  Google Scholar 

  • Impey S, Obrietan K, Wong ST et al (1998a) Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869–883

    PubMed  CAS  Google Scholar 

  • Impey S, Smith DM, Obrietan K et al (1998b) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595–601

    PubMed  CAS  Google Scholar 

  • Ji Y, Pang PT, Feng L, Lu B (2005) Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci 8:164–172

    PubMed  CAS  Google Scholar 

  • Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406

    PubMed  CAS  Google Scholar 

  • Kang H, Jia LZ, Suh KY et al (1996) Determinants of BDNF-induced hippocampal synaptic plasticity: role of the Trk B receptor and the kinetics of neurotrophin delivery. Learn Mem 3:188–196

    PubMed  CAS  Google Scholar 

  • Kelleher RJ, Govindarajan A, Jung H-Y et al (2004a) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467–479

    PubMed  CAS  Google Scholar 

  • Kelleher RJ, Govindarajan A, Tonegawa S (2004b) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44:59–73

    PubMed  CAS  Google Scholar 

  • Khuchua Z, Wozniak DF, Bardgett ME et al (2003) Deletion of the N-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory. Neuroscience 119:101–111

    PubMed  CAS  Google Scholar 

  • Kim M, Park AJ, Havekes R et al (2011) Colocalization of protein kinase A with adenylyl cyclase enhances protein kinase A activity during induction of long-lasting long-term-potentiation. PLoS Comput Biol 7:e1002084

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kramár EA, Lin B, Rex CS et al (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci U S A 103:5579–5584

    PubMed  PubMed Central  Google Scholar 

  • Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683–696

    PubMed  CAS  Google Scholar 

  • Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci U S A 97:6856–6861

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kuczewski N, Porcher C, Gaiarsa J-L (2010) Activity-dependent dendritic secretion of brain-derived neurotrophic factor modulates synaptic plasticity. Eur J Neurosci 32:1239–1244

    PubMed  Google Scholar 

  • Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5:45–54

    PubMed  CAS  Google Scholar 

  • Laurent A-C, Breckler M, Berthouze M, Lezoualc’h F (2012) Role of Epac in brain and heart. Biochem Soc Trans 40:51–57

    PubMed  CAS  Google Scholar 

  • Liao L, Pilotte J, Xu T et al (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics. J Proteome Res 6:1059–1071

    PubMed  CAS  Google Scholar 

  • Lin X, Gelman IH (2002) Calmodulin and cyclin D anchoring sites on the Src-suppressed C kinase substrate, SSeCKS. Biochem Biophys Res Commun 290:1368–1375

    PubMed  CAS  Google Scholar 

  • Lin X, Tombler E, Nelson PJ et al (1996) A novel src- and ras-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 271:28430–28438

    PubMed  CAS  Google Scholar 

  • Lin B, Kramár EA, Bi X et al (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062–2069

    PubMed  CAS  Google Scholar 

  • Lisman J (2003) Actin’s actions in LTP-induced synapse growth. Neuron 38:361–362

    PubMed  CAS  Google Scholar 

  • Lu Y, Ji Y, Ganesan S et al (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31:11762–11771

    PubMed  CAS  PubMed Central  Google Scholar 

  • Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352–357

    PubMed  CAS  Google Scholar 

  • Martin KC, Kosik KS (2002) Synaptic tagging—who’s it? Nat Rev Neurosci 3:813–820

    PubMed  CAS  Google Scholar 

  • Martin KC, Casadio A, Zhu H et al (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927–938

    PubMed  CAS  Google Scholar 

  • Matsushita M, Tomizawa K, Moriwaki A et al (2001) A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting long-term potentiation. J Neurosci 21:6000–6007

    PubMed  CAS  Google Scholar 

  • Matthies H, Reymann KG (1993) Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. Neuroreport 4:712–714

    PubMed  CAS  Google Scholar 

  • Mayford M, Baranes D, Podsypanina K, Kandel ER (1996) The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci U S A 93:13250–13255

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mayford M, Siegelbaum S, Kandel ER (2012) Synapses and memory storage. Cold Spring Harb Perspect Biol 4(6)

    Google Scholar 

  • Meiri N, Rosenblum K (1998) Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task. Brain Res 789:48–55

    PubMed  CAS  Google Scholar 

  • Messaoudi E, Ying S-W, Kanhema T et al (2002) Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22:7453–7461

    PubMed  CAS  Google Scholar 

  • Michel JJC, Scott JD (2002) AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol 42:235–257

    PubMed  CAS  Google Scholar 

  • Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27:7476–7481

    PubMed  CAS  Google Scholar 

  • Morris RGMG, Anderson E, Lynch GSS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 319:774–776. doi:10.1038/319774a0

  • Nadella KS, Saji M, Jacob NK et al (2009) Regulation of actin function by protein kinase A-mediated phosphorylation of Limk1. EMBO Rep 10:599–605

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nauert JB, Klauck TM, Langeberg LK, Scott JD (1997) Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffold protein. Curr Biol 7:52–62

    PubMed  CAS  Google Scholar 

  • Navakkode S, Sajikumar S, Frey JU (2004) The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 24:7740–7744

    PubMed  CAS  Google Scholar 

  • Nayak A, Zastrow DJ, Lickteig R et al (1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394:680–683. doi:10.1038/29305

  • Nguyen PV, Kandel ER (1997) Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4:230–243

    PubMed  CAS  Google Scholar 

  • Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71:401–437

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nie T, McDonough CB, Huang T et al (2007) Genetic disruption of protein kinase A anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory. J Neurosci 27:10278–10288

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535–545

    PubMed  CAS  Google Scholar 

  • Otmakhov N, Khibnik L, Otmakhova N et al (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91:1955–1962

    PubMed  CAS  Google Scholar 

  • Ouyang Y, Rosenstein A, Kreiman G et al (1999) Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J Neurosci 19:7823–7833

    PubMed  CAS  Google Scholar 

  • Patterson SL, Pittenger C, Morozov A et al (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123–140

    PubMed  CAS  Google Scholar 

  • Pittenger C, Kandel E (1998) A genetic switch for long-term memory. C R Acad Sci III 321:91–96

    PubMed  CAS  Google Scholar 

  • Ramachandran B, Frey JU (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J Neurosci 29:12167–12173

    PubMed  CAS  Google Scholar 

  • Redondo RL, Morris RGM (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12:17–30

    PubMed  CAS  Google Scholar 

  • Redondo RL, Okuno H, Spooner PA et al (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981–4989

    PubMed  CAS  Google Scholar 

  • Rex CS, Lin C-Y, Kramár EA et al (2007) Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27:3017–3029

    PubMed  CAS  Google Scholar 

  • Richter-Levin G, Akirav I (2003) Emotional tagging of memory formation—in the search for neural mechanisms. Brain Res Brain Res Rev 43:247–256

    PubMed  Google Scholar 

  • Roberson ED, English JD, Adams JP et al (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  CAS  Google Scholar 

  • Rosenmund C, Carr DW, Bergeson SE et al (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368:853–856

    PubMed  CAS  Google Scholar 

  • Sajikumar S, Frey JU (2004) Resetting of “synaptic tags” is time- and activity-dependent in rat hippocampal CA1 in vitro. Neuroscience 129:503–507

    PubMed  CAS  Google Scholar 

  • Sajikumar S, Li Q, Abraham WC, Xiao ZC (2009) Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn Mem 16:178–186

    PubMed  Google Scholar 

  • Sánchez C, Díaz-Nido J, Avila J (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 61:133–168

    PubMed  Google Scholar 

  • Santos AR, Comprido D, Duarte CB (2010) Regulation of local translation at the synapse by BDNF. Prog Neurobiol 92:505–516

    PubMed  CAS  Google Scholar 

  • Selbach O, Brown RE, Haas HL (1998) Long-term increase of hippocampal excitability by histamine and cyclic AMP. Neuropharmacology 36:1539–1548

    Google Scholar 

  • Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162–166

    PubMed  CAS  Google Scholar 

  • Sheng M, Lee SH (2001) AMPA receptor trafficking and the control of synaptic transmission. Cell 105:825–828

    PubMed  CAS  Google Scholar 

  • Shih M, Lin F, Scott JD et al (1999) Dynamic complexes of beta2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J Biol Chem 274:1588–1595

    PubMed  CAS  Google Scholar 

  • Skeberdis VA, Chevaleyre V, Lau CG et al (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9:501–510

    PubMed  CAS  Google Scholar 

  • Slack JR, Walsh C (1995) Effects of a cAMP analogue simulate the distinct components of long-term potentiation in CA1 region of rat hippocampus. Neurosci Lett 201:25–28

    PubMed  CAS  Google Scholar 

  • Snyder EM, Colledge M, Crozier RA et al (2005) Role for A kinase-anchoring proteins (AKAPS) in glutamate receptor trafficking and long term synaptic depression. J Biol Chem 280:16962–16968

    PubMed  CAS  PubMed Central  Google Scholar 

  • Steward O, Halpain S (1999) Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J Neurosci 19:7834–7845

    PubMed  CAS  Google Scholar 

  • Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325

    PubMed  CAS  Google Scholar 

  • Streb JW, Kitchen CM, Gelman IH, Miano JM (2004) Multiple promoters direct expression of three AKAP12 isoforms with distinct subcellular and tissue distribution profiles. J Biol Chem 279:56014–56023

    PubMed  CAS  Google Scholar 

  • Tao X, Finkbeiner S, Arnold DB et al (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726

    PubMed  CAS  Google Scholar 

  • Theurkauf WE, Vallee RB (1982) Molecular characterization of the cAMP-dependent protein kinase bound to microtubule-associated protein 2. J Biol Chem 257:3284–3290

    PubMed  CAS  Google Scholar 

  • Tongiorgi E, Righi M, Cattaneo A (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17:9492–9505

    PubMed  CAS  Google Scholar 

  • Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327–1338

    PubMed  CAS  Google Scholar 

  • Wang DO, Martin KC, Zukin RS (2010a) Spatially restricting gene expression by local translation at synapses. Trends Neurosci 33:173–182

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wang S-H, Redondo RL, Morris RGM (2010b) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci U S A 107:19537–19542

    PubMed  CAS  PubMed Central  Google Scholar 

  • Willoughby D, Wong W, Schaack J et al (2006) An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J 25:2051–2061

    PubMed  CAS  PubMed Central  Google Scholar 

  • Woo NH, Abel T, Nguyen PV (2002) Genetic and pharmacological demonstration of a role for cyclic AMP-dependent protein kinase-mediated suppression of protein phosphatases in gating the expression of late LTP. Eur J Neurosci 16:1871–1876

    PubMed  Google Scholar 

  • Yao Y, Kelly MT, Sajikumar S et al (2008) PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28:7820–7827

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yoshii A, Constantine-Paton M (2007) BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 10:702–711

    PubMed  CAS  Google Scholar 

  • Young JZ, Nguyen PV (2005) Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25:7221–7231

    PubMed  CAS  Google Scholar 

  • Young JZ, Isiegas C, Abel T, Nguyen PV (2006) Metaplasticity of the late-phase of long-term potentiation: a critical role for protein kinase A in synaptic tagging. Eur J Neurosci 23:1784–1794

    PubMed  PubMed Central  Google Scholar 

  • Zakharenko SS, Patterson SL, Dragatsis I et al (2003) Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39:975–990

    PubMed  CAS  Google Scholar 

  • Zhong H, Sia G-M, Sato TR et al (2009) Subcellular dynamics of type II PKA in neurons. Neuron 62:363–374

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950–2967

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We thank Ted Huang for the scheme in Fig. 5.1.

Author information

Authors and Affiliations

  1. Department of Biology, University of Pennsylvania, Philadelphia, PA, USA

    Alan Jung Park & Ted Abel

Authors
  1. Alan Jung Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ted Abel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ted Abel .

Editor information

Editors and Affiliations

  1. Yong Loo Lin School of Medicine Department of Physiology, National University of Singapore, Singapore, Singapore

    Sreedharan Sajikumar

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Park, A.J., Abel, T. (2015). PKA Anchoring and Synaptic Tagging and Capture. In: Sajikumar, S. (eds) Synaptic Tagging and Capture. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1761-7_5

Download citation

Publish with us

Policies and ethics

Search

Navigation