Redondo, Roger L., Okuno, Hiroyukki, Dr., Spooner, Patrick A., Frenguelli, Bruno G., Bito, Haruhiko and Morris, R. G. M. (Richard G. M.). (2010) Synaptic tagging and capture : differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. Journal of Neuroscience, Vol.30 (No.14). pp. 4981-4989. ISSN 0270-6474

PDF WRAP_Frenguelli_synoptic_tagging.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (2167Kb)

Abstract

Weakly tetanized synapses in area CA1 of the hippocampus that ordinarily display long-term potentiation lasting ~3 h (called early-LTP) will maintain a longer-lasting change in efficacy (late-LTP) if the weak tetanization occurs shortly before or after strong tetanization of an independent, but convergent, set of synapses in CA1. The synaptic tagging and capture hypothesis explains this heterosynaptic influence on persistence in terms of a distinction between local mechanisms of synaptic tagging and cell-wide mechanisms responsible for the synthesis, distribution, and capture of plasticity-related proteins (PRPs). We now present evidence that distinct CaM kinase (CaMK) pathways serve a dissociable role in these mechanisms. Using a hippocampal brain-slice preparation that permits stable long-term recordings in vitro for >10 h and using hippocampal cultures to validate the differential drug effects on distinct CaMK pathways, we show that tag setting is blocked by the CaMK inhibitor KN-93 (2-[N-(2-hydroxyethyl)]-N-(4-methoxybenzenesulfonyl)amino-N-(4-chlorocinnamyl)-N-methylbenzylamine) that, at low concentration, is more selective for CaMKII. In contrast, the CaMK kinase inhibitor STO-609 [7H-benzimidazo(2,1-a)benz(de)isoquinoline-7-one-3-carboxylic acid] specifically limits the synthesis and/or availability of PRPs. Analytically powerful three-pathway protocols using sequential strong and weak tetanization in varying orders and test stimulation over long periods of time after LTP induction enable a pharmacological dissociation of these distinct roles of the CaMK pathways in late-LTP and so provide a novel framework for the molecular mechanisms by which synaptic potentiation, and possibly memories, become stabilized.

Item Type:	Journal Article
Subjects:	R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Synapses -- Research, Hippocampus (Brain), Neuroplasticity -- Research, Adaptation (Physiology)
Journal or Publication Title:	Journal of Neuroscience
Publisher:	Society for Neuroscience
ISSN:	0270-6474
Date:	7 April 2010
Volume:	Vol.30
Number:	No.14
Number of Pages:	9
Page Range:	pp. 4981-4989
Identification Number:	10.1523/JNEUROSCI.3140-09.2010
Status:	Peer Reviewed
Access rights to Published version:	Restricted or Subscription Access
Funder:	Human Frontiers Science Program (HFSP), Volkswagenstiftung (VWS), Medical Research Council (Great Britain) (MRC), Japan. Monbu Kagakushō [Japan. Ministry of Education, Culture, Sports, Science and Technology] (MK), Japan. Kōsei Rōdōshō (KR), Takeda Kagaku Shinkō Zaidan [Science Foundation], Yamada Kagaku Shinkō Zaidan (YKSZ)
References:	Andersen P, Sundberg SH, Sveen O, Wigstro¨m H (1977) Specific longlasting potentiation of synaptic transmission in hippocampal slices. Nature 266:736 –737. Bito H, Deisseroth K, TsienRW (1996) CREB phosphorylation and dephosphorylation: a Ca 2- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203–1214. 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. Braun AP, Schulman H (1995) The multifunctional calcium/calmodulindependent protein kinase: from form to function. Annu Rev Physiol 57:417– 445. Erondu NE, Kennedy MB (1985) Regional distribution of type II Ca2/ calmodulin-dependent protein kinase in rat brain. J Neurosci 5:3270– 3277. Fonseca R, Na¨gerl UV, Morris RG, Bonhoeffer T (2004) Competing for memory: hippocampal LTP under regimes of reduced protein synthesis. Neuron 44:1011–1020. Fonseca R, Na¨gerl UV, Bonhoeffer T (2006) Neuronal activity determines the protein synthesis dependence of long-term potentiation. Nat Neurosci 9:478–480. Frey U, Morris RGM (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536. Frey U, MorrisRGM (1998a) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545–552. Frey U, Morris RGM (1998b) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181–188. Frey U, Krug M, Reymann KG, MatthiesH (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. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870–873. Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, Andreev D, De Zeeuw CI, Elgersma Y (2006) alphaCaMKII Is essential for cerebellar LTD and motor learning. Neuron 51:835– 843. Hanson PI, Meyer T, Stryer L, Schulman H (1994) Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron 12:943–956. Ho N, Liauw JA, Blaeser F, Wei F, Hanissian S, Muglia LM, Wozniak DF, Nardi A, Arvin KL, Holtzman DM, Linden DJ, Zhuo M, Muglia LJ, Chatila TA (2000) Impaired synaptic plasticity and cAMP response element-binding protein activation in Ca2/calmodulin-dependent protein kinase type IV/Gr-deficient mice. J Neurosci 20:6459–6472. Ho OH, Delgado JY, O’Dell TJ (2004) Phosphorylation of proteins involved in activity-dependent forms of synaptic plasticity is altered in hippocampal slices maintained in vitro. J Neurochem 91:1344 –1357. Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H (1995) A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 212:806–812. Kang H, Sun LD, Atkins CM, Soderling TR, Wilson MA, Tonegawa S (2001) An important role of neural activity-dependent CaMKIV signaling in the consolidation of long-term memory. Cell 106:771–783. Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activityresponsive element in the Arc/Arg3.1 promoter essential for synapse-tonucleus signaling in activated neurons. Proc Natl Acad Sci U S A 106:316 –321. Krug M, Lo¨ssner B, Ott T (1984) Anisomycin blocks the late phase of longterm potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39–42. Leutgeb JK, Frey JU, Behnisch T (2003) LTP in cultured hippocampalentorhinal cortex slices from young adult (P25-30) rats. J Neurosci Methods 130:19 –32. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175–190. Lisman JE, Goldring MA (1988) Feasibility of long-term storage of graded information by the Ca2/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc Natl Acad SciU S A 85:5320 –5324. Lisman JE, Zhabotinsky AM (2001) A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31:191–201. Malenka RC, Kauer JA, Perkel DJ, Mauk MD, Kelly PT, Nicoll RA, Waxham MN (1989) An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340:554 –557. Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862– 866. 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 91:927–938. Meyer T, Hanson PI, Stryer L, Schulman H (1992) Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256:1199 –1202. Miller P, Zhabotinsky AM, Lisman JE, Wang XJ (2005) The stability of a stochastic CaMKII switch: dependence on the number of enzyme molecules and protein turnover. PLoS Biol 3:e107. Miller SG, Kennedy MB (1986) Regulation of brain type II Ca2/ calmodulin-dependent protein kinase by autophosphorylation: a Ca 2- triggered molecular switch. Cell 44:861– 870. Moncada D, ViolaH (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27:7476 –7481. Navakkode S, Sajikumar S, Frey JU (2007) Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology 52:1547–1554. O’Carroll CM, Morris RGM (2004) Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47:324 –332. Ouyang Y, Kantor D, Harris KM, Schuman EM, Kennedy MB (1997) Visualization of the distribution of autophosphorylated calcium/calmodulindependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus. J Neurosci 17:5416 –5427. Reymann KG, Frey JU (2007) The late maintenance of hippocampal LTP: requirements, phases, “synaptic tagging”, “late-associativity” and implications. Neuropharmacology 52:24–40. Rose J, Jin SX, CraigAM (2009) Heterosynaptic molecular dynamics: locally induced propagating synaptic accumulation of CaM kinase II. Neuron 61:351–358. Sajikumar S, Navakkode S, Frey JU (2005) Protein synthesis-dependent long-term functional plasticity: methods and techniques. Curr Opin Neurobiol 15:607– 613. Sajikumar S, Navakkode S, Frey JU (2007) Identification of compartmentand process-specific molecules required for “synaptic tagging” during long-term potentiation and long-term depression in hippocampal CA1. J Neurosci 27:5068 –5080. Sajikumar S, Navakkode S, Frey JU (2008) Distinct single but not necessarily repeated tetanization is required to induce hippocampal late-LTP in the rat CA1. Learn Mem 15:46–49. Sanhueza M, McIntyre CC, Lisman JE (2007) Reversal of synaptic memory by Ca2/calmodulin-dependent protein kinase II inhibitor. J Neurosci 27:5190 –5199. Schurr A, Reid KH, Tseng MT, Edmonds HL Jr, West CA, Rigor BM (1986) Effect of electrical stimulation on the viability of the hippocampal slice preparation. Brain Res Bull 16:299 –301. Schwartzkroin PA, Wester K (1975) Long-lasting facilitation of a synaptic potential following tetanization in the in vitro hippocampal slice. Brain Res 89:107–119. Sumi M, Kiuchi K, Ishikawa T, Ishii A, Hagiwara M, Nagatsu T, Hidaka H (1991) The newly synthesized selective Ca2/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181:968 –975. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R (2002) STO-609, a specific inhibitor of the Ca2�/calmodulin-dependent protein kinase kinase. J Biol Chem 277:15813–15818. Yamauchi T (2005) Neuronal Ca2/calmodulin-dependent protein kinase II—discovery, progress in a quarter of a century, and perspective: implication for learning and memory. Biol Pharm Bull 28:1342–1354. Zhang YP, Holbro N, Oertner TG (2008) Optical induction of plasticity at single synapses reveals input-specific accumulation of CaMKII. Proc Natl Acad Sci U S A 105:12039 –12044.
URI:	http://wrap.warwick.ac.uk/id/eprint/2389

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item