Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression

Neuron

Volumn 80, Issue 1, 2013, Pages 72-79

  Jakkamsetti, Vikram ^a   Tsai, Nien Pei ^a   Gross, Christina ^b   Molinaro, Gemma ^a,c   Collins, Katie A ^a   Nicoletti, Ferdinando ^c,d   Wang, KuanH ^e   Osten, Pavel ^f   Bassell, Gary J ^b   Gibson, Jay R ^a   Huber, KimberlyM ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c IRCCS NEUROMED   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^f Cold Spring Harbor ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; GLUTAMATE RECEPTOR; MESSENGER RNA; METABOTROPIC RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARC GENE; ARTICLE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPAL CA1 REGION; IMMEDIATE EARLY GENE; LONG TERM DEPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; RNA TRANSLATION; SYNAPTIC TRANSMISSION;

ANIMALS; CYTOSKELETAL PROTEINS; DENDRITES; GENES, REPORTER; HIPPOCAMPUS; LEARNING; LONG-TERM SYNAPTIC DEPRESSION; MICE; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION; TRANSCRIPTIONAL ACTIVATION;

EID: 84884756183     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.020     Document Type: Article

References (39)

1. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008, 9:387.
2. Auerbach B.D., Osterweil E.K., Bear M.F. Mutations causing syndromic autism define an axis of synaptic pathophysiology. Nature 2011, 480:63-68.
3. Besse F., Ephrussi A. Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat. Rev. Mol. Cell Biol. 2008, 9:971-980.
4. Bozdagi O., Sakurai T., Dorr N., Pilorge M., Takahashi N., Buxbaum J.D. Haploinsufficiency of Cyfip1 produces fragile X-like phenotypes in mice. PLoS ONE 2012, 7:e42422.
5. Bramham C.R., Alme M.N., Bittins M., Kuipers S.D., Nair R.R., Pai B., Panja D., Schubert M., Soule J., Tiron A., Wibrand K. The Arc of synaptic memory. Exp. Brain Res. 2010, 200:125-140.
6. Dong Z., Gong B., Li H., Bai Y., Wu X., Huang Y., He W., Li T., Wang Y.T. Mechanisms of hippocampal long-term depression are required for memory enhancement by novelty exploration. J.Neurosci. 2012, 32:11980-11990.
7. Fletcher B.R., Calhoun M.E., Rapp P.R., Shapiro M.L. Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity. J.Neurosci. 2006, 26:1507-1515.
8. Giorgi C., Yeo G.W., Stone M.E., Katz D.B., Burge C., Turrigiano G., Moore M.J. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 2007, 130:179-191.
9. Grinevich V., Kolleker A., Eliava M., Takada N., Takuma H., Fukazawa Y., Shigemoto R., Kuhl D., Waters J., Seeburg P.H., Osten P. Fluorescent Arc/Arg3.1 indicator mice: a versatile tool to study brain activity changes invitro and invivo. J.Neurosci. Methods 2009, 184:25-36.
10. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 1999, 2:1120-1124.
11. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., Barnes C.A. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J.Neurosci. 2000, 20:3993-4001.
12. Hagerman R., Kemper M., Hudson M. Learning disabilities and attentional problems in boys with the fragile X syndrome. Am. J. Dis. Child. 1985, 139:674-678.
13. Huber K.M., Kayser M.S., Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000, 288:1254-1257.
14. Huber K.M., Gallagher S.M., Warren S.T., Bear M.F. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA 2002, 99:7746-7750.
15. Karlsson M.P., Frank L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J.Neurosci. 2008, 28:14271-14281.
16. Kemp A., Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl. Acad. Sci. USA 2004, 101:8192-8197.
17. Krueger D.D., Bear M.F. Toward fulfilling the promise of molecular medicine in fragile X syndrome. Annu. Rev. Med. 2011, 62:411-429.
18. Lee H.K., Min S.S., Gallagher M., Kirkwood A. NMDA receptor-independent long-term depression correlates with successful aging in rats. Nat. Neurosci. 2005, 8:1657-1659.
19. Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62:788-801.
20. Manahan-Vaughan D., Braunewell K.H. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl. Acad. Sci. USA 1999, 96:8739-8744.
21. Miyashita T., Kubik S., Lewandowski G., Guzowski J.F. Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol. Learn. Mem. 2008, 89:269-284.
22. Miyashita T., Kubik S., Haghighi N., Steward O., Guzowski J.F. Rapid activation of plasticity-associated gene transcription in hippocampal neurons provides a mechanism for encoding of one-trial experience. J.Neurosci. 2009, 29:898-906.
23. Moult P.R., Gladding C.M., Sanderson T.M., Fitzjohn S.M., Bashir Z.I., Molnar E., Collingridge G.L. Tyrosine phosphatases regulate AMPA receptor trafficking during metabotropic glutamate receptor-mediated long-term depression. J.Neurosci. 2006, 26:2544-2554.
24. Napoli I., Mercaldo V., Boyl P.P., Eleuteri B., Zalfa F., De Rubeis S., Di Marino D., Mohr E., Massimi M., Falconi M., et al. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 2008, 134:1042-1054.
25. Narayanan U., Nalavadi V., Nakamoto M., Pallas D.C., Ceman S., Bassell G.J., Warren S.T. FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J.Neurosci. 2007, 27:14349-14357.
26. Niere F., Wilkerson J.R., Huber K.M. Evidence for a fragile X mental retardation protein-mediated translational switch in metabotropic glutamate receptor-triggered Arc translation and long-term depression. J.Neurosci. 2012, 32:5924-5936.
27. Park S., Park J.M., Kim S., Kim J.A., Shepherd J.D., Smith-Hicks C.L., Chowdhury S., Kaufmann W., Kuhl D., Ryazanov A.G., et al. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 2008, 59:70-83.
28. Plath N., Ohana O., Dammermann B., Errington M.L., Schmitz D., Gross C., Mao X., Engelsberg A., Mahlke C., Welzl H., et al. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 2006, 52:437-444.
29. Popkirov S.G., Manahan-Vaughan D. Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor-dependent, learning-facilitated long-term depression in CA1 synapses. Cereb. Cortex 2011, 21:501-509.
30. Qi Y., Hu N.W., Rowan M.J. Switching off LTP: mGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus. Cereb. Cortex 2013, 23:932-939.
31. Restivo L., Ferrari F., Passino E., Sgobio C., Bock J., Oostra B.A., Bagni C., Ammassari-Teule M. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl. Acad. Sci. USA 2005, 102:11557-11562.
32. Shepherd J.D., Bear M.F. New views of Arc, a master regulator of synaptic plasticity. Nat. Neurosci. 2011, 14:279-284.
33. Steward O., Wallace C.S., Lyford G.L., Worley P.F. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 1998, 21:741-751.
34. Thompson L.T., Best P.J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 1990, 509:299-308.
35. Vazdarjanova A., McNaughton B.L., Barnes C.A., Worley P.F., Guzowski J.F. Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J.Neurosci. 2002, 22:10067-10071.
36. Vazdarjanova A., Ramirez-Amaya V., Insel N., Plummer T.K., Rosi S., Chowdhury S., Mikhael D., Worley P.F., Guzowski J.F., Barnes C.A. Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J.Comp. Neurol. 2006, 498:317-329.
37. Wang K.H., Majewska A., Schummers J., Farley B., Hu C., Sur M., Tonegawa S. Invivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell 2006, 126:389-402.
38. Waung M.W., Huber K.M. Protein translation in synaptic plasticity: mGluR-LTD, Fragile X. Curr. Opin. Neurobiol. 2009, 19:319-326.
39. Waung M.W., Pfeiffer B.E., Nosyreva E.D., Ronesi J.A., Huber K.M. Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 2008, 59:84-97.