Arc mRNA docks precisely at the base of individual dendritic spines indicating the existence of a specialized microdomain for synapse-specific mRNA translation

Journal of Comparative Neurology

Volumn 520, Issue 14, 2012, Pages 3105-3119

  Dynes, Joseph L ^a,b   Steward, Oswald ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arc mRNA; Dendritic spines; Microdomain

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARC GENE; ARTICLE; BRAIN TISSUE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; DNA TRANSFECTION; EMBRYO; GENE; GENE EXPRESSION REGULATION; GENE LOCATION; MALE; MOLECULAR DOCKING; MS2 GENE; NERVE CELL CULTURE; NONHUMAN; POLYSOME; PRIORITY JOURNAL; RAT; REPORTER GENE; SYNAPTIC MEMBRANE; TRANSLATION REGULATION;

ADAM PROTEINS; ANIMALS; ANTIGENS, CD; CELL COMPARTMENTATION; CELLS, CULTURED; CEREBRAL CORTEX; CYTOSKELETAL PROTEINS; DENDRITIC SPINES; FEMALE; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MALE; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MONTE CARLO METHOD; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; PROTEIN BIOSYNTHESIS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SYNAPSES; TRANSFECTION;

EID: 84865078915     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23073     Document Type: Article

References (43)

1. Aakalu G, Smith WB, Jiang C, Nguyen N, Schuman EM. 2001. Dynamic visualization of dendritic protein synthesis in hippocampal neurons. Neuron 30: 489-502.
2. Aitken CE, Petrov A, Puglisi JD. 2010. Single ribosome dynamics and the mechanism of translation. Annu Rev Biophys 39: 491-513.
3. Bassell GJ, Singer RH, Kosik KS. 1994. Association of poly(A) mRNA with microtubules in cultured neurons. Neuron 12: 571-582.
4. Bramham CR. 2008. Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18: 524-531.
5. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576.
6. Cervera M, Dreyfuss G, Penman S. 1981. Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells. Cell 23: 113-120.
7. 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: 445-459.
8. Cook D, Sanchez-Carbente, MDR, LaChance C, Radzioch D, Tremblay S, Khandjian EW, DesGroseillers L, Murai KK. 2011. Fragile X related protein 1 clusters with ribosomes and messenger RNAs at a subset of dendritic spines in the mouse hippocampus. PLOS One 6: e26120.
9. Dieterich DC, Hodas JJ, Gouzer G, Shadrin IY, Ngo JT, Triller A, Tirrell DA, Schuman EM. 2010. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat Neurosci 13: 897-905.
10. Dynes JL, Steward O. 2007. Dynamics of bi-directional transport of Arc mRNA in neuronal dendrites. J Comp Neurol 500: 433-447.
11. Dynes JL, Steward O (eds.). 2008. Dendritic transport of mRNA, the IEG Arc, and synaptic modifications involved in memory consolidation. Vol. 4. Oxford: Elsevier.
12. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, et al. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr Biol 13: 161-167.
13. Guzowski JF, McNaughton BL, Barnes CA, Worley PF. 1999. Environment-specific induction of the immediate early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2: 1120-1124.
14. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA. 2000. 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 20: 3993-4001.
15. Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA. 2005. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15: 599-606.
16. Herb A, Wisden W, Catania dMV, Marechal D, Dresse A, Seeberg PH. 1997. Prominent dendritic localization in forebrain neurons of a novel mRNA and its product, dendrin. Mol Cell Neurosci 8: 367-374.
17. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, Adams SR, Garner CC, Tsien RY, Ellisman MH, Malenka RC. 2004. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 7: 244-253.
18. Kao DI, Aldridge GM, Weiler IJ, Greenough WT. 2010. Altered mRNA transport, docking, and protein translation in neurons lacking fragile X mental retardation protein. Proc Natl Acad Sci U S A 107: 15601-15606.
19. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS. 1996. Translocation of RNA granules in living neurons. J Neurosci 16: 7812-7820.
20. Kremerskothen J, Kindler S, Finger I, Veltel S, Barnekow A. 2006. Postsynaptic recruitment of Dendrin depends on both dendritic mRNA transport and synaptic anchoring. J Neurochem 96: 1659-1666.
21. Link W, Konietzko G, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D. 1995. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci 92: 5734-5738.
22. Lyford G, Yamagata K, Kaufmann W, Barnes C, Sanders L, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF. 1995. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14: 433-445.
23. Marshall RA, Aitken CE, Dorywalska M, Puglisi JD. 2008. Translation at the single-molecule level. Annu Rev Biochem 77: 177-203.
24. Martone ME, Pollock JA, Jones YZ, Ellisman MH. 1996. Ultrastructural localization of dendritic messenger RNA in adult rat hippocampus. J Neurosci 16: 7437-7446.
25. Messaoudi E, Kanhema T, Soule 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: 10445-10455.
26. Miyashita T, Kubik S, Lewandowski G, Guzowski JF. 2008. Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem 89: 269-284.
27. Okada D, Ozawa F, Inokuchi K. 2009. Input-specific spine entry of soma-derived Vesl-1S protein conforms to synaptic tagging. Science 324: 904-909.
28. 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.
29. Park S, Park JM, Kim S, Kim JA, Shepherd JD, Smith-Hicks CL, Chowdhury S, Kaufmann W, Kuhl D, Ryazanov AG, Huganir RL, Linden DJ, Worley PF. 2008. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59: 70-83.
30. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bösl MR, Lipp HP, Grant SG, Bliss TV, Wolfer DP, Kuhl D. 2006. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
31. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT. 2006. Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52: 461-474.
32. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev 23: 1-11.
33. Sage D, Neumann FR, Hediger F, Gasser SM, Unser M. 2005. Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans Image Process 14: 1372-1383.
34. Sanes JR, Lichtman JW. 1999. Can molecules explain long-term potentiation? Nat Neurosci 2: 597-604.
35. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, Kuhl D, Huganir RL, Worley PF. 2006. Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52: 475-484.
36. 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: 284-291.
37. Steward O, Worley PF. 2001. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 30: 227-240.
38. 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: 741-751.
39. Tada T, Simonetta A, Batterton M, Kinoshita M, Edbauer D, Sheng M. 2007. Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr Biol 17: 1752-1758.
40. Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ. 2003. Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23: 3251-3261.
41. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li XD, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD. 2008. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135: 535-548.
42. Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM. 2008. Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59: 84-97.
43. Xie Y, Vessey JP, Konecna A, Dahm R, Macchi P, Kiebler MA. 2007. The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr Biol 17: 1746-1751.