Synaptic tagging — who's it?

Nature Reviews Neuroscience

Volumn 3, Issue 10, 2002, Pages 813-820

  Martin, Kelsey C ^a   Kosik, Kenneth S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ION CHANNEL; MICRORNA; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; PROTEIN KINASE;

ANIMAL; HUMAN; LONG TERM POTENTIATION; METABOLISM; NERVE CELL PLASTICITY; NON-PROGRAMMATIC; PHYSIOLOGY; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

NON-PROGRAMMATIC;

ACTINS; ANIMALS; HUMANS; ION CHANNELS; LONG-TERM POTENTIATION; MICRORNAS; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; NEURONAL PLASTICITY; PROTEIN KINASES; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 0036779479     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn942     Document Type: Article

References (73)

1. Martin, K. C. et al. Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-938 (1997).
2. Frey, U. & Morris, R. G. Synaptic tagging and long-term potentiation. Nature 385, 533-536 (1997).
3. Frey, U. & Morris, R. G. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP Neuropharmacology 37, 545-552 (1998).
4. Shi, S. H. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816 (1999).
5. Tovar, K. R. & Westbrook, G. L. Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255-264 (2002).
6. Ango, F. et al. Homer-dependent cell surface expression of metabotropic glutamate receptor type 5 in neurons. Mol. Cell. Neurosci. 20, 323-329 (2002).
7. El-Husseini, A. E. et al. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108, 849-863 (2002).
8. Lisman, J., Schulman, H. & Cline, H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Rev. Neurosci. 3, 175-190 (2002).
9. Osten, P., Valsamis, L., Harris, A. & Sacktor, T. C. Protein synthesis-dependent formation of protein kinase MZ in long- term potentiation. J. Neurosci. 16, 2444-2451 (1996).
10. Ling, D. S. et al. Protein kinase MZ is necessary and sufficient for LTP maintenance. Nature Neurosci. 5, 295-296 (2002).
11. Drier, E. A. et al. Memory enhancement and formation by atypical PKM activity in Drosophlla melanogaster. Nature Neurosci. 5, 316-324 (2002).
12. Casadio, A. et al. 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 (1999).
13. Chain, D. G., Hegde, A. N., Yamamoto, N., Liu-Marsh, B. & Schwartz, J. H. Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron- specific function of the ubiquitin system in Aplysla. J. Neurosci. 15, 7592-7603 (1995).
14. Hegde, A. N. et al. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysla. Cell 89, 115-126 (1997).
15. Chain, D. G. et al. Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysla. Neuron 22, 147-156 (1999).
16. Bailey, C. H. & Kandel, E. R. Structural changes accompanying memory storage. Annu. Rev. Physlol. 55, 397-426 (1993).
17. Schuster, C. M., Davis, G. W., Fetter, R. D. & Goodman, C. S. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17, 655-667 (1996).
18. Davis, G. W., Schuster, C. M. & Goodman, C. S. Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17, 669-679 (1996).
19. Bailey, C. H., Chen, M., Keller, F. & Kandel, E. R. Serotonin- mediated endocytosis of apCAM: an early step of learning- related synaptic growth in Aplysla. Science 256, 645-649 (1992).
20. Mayford, M., Barzilai, A., Keller, F., Schacher, S. & Kandel, E. R. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysla. Science 256, 638-644 (1992).
21. Dityatev, A., Dityateva, G. & Schachner, M. Synaptic strength as a function of post versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26, 207-117 (2000).
22. Tanaka, H. et al. Molecular modification of N-cadherin in response to synaptic activity. Neuron 25, 93-107 (2000).
23. Bozdagi, O., Shan, W., Tanaka, H., Benson, D. L. & Huntley, G. W. Increasing numbers of synaptic puncta during late- phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28, 245-259 (2000).
24. Murase, S., Mosser, E. & Schuman, E. M. Depolarization drives β-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91-105 (2002).
25. Lu, Q. et al. δ-Catenin, an adhesive junction-associated protein which promotes cell scattering. J. Cell Blol. 144, 519-532 (1999).
26. Izawa, I., Nishizawa, M., Ohtakara, K. & Inagaki, M. Densin-180 interacts with δ-catenin/neural plakophilin- related armadillo repeat protein at synapses. J. Blol. Chem. 277, 5345-5350 (2002).
27. Fischer, M., Kaech, S., Wagner, U., Brinkhaus, H. & Matus, A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nature Neurosci. 3, 887-894 (2000).
28. Star, E. N., Kwiatkowski, D. J. & Murthy, V. N. Rapid turnover of actin in dendritic spines and its regulation by activity. Nature Neurosci. 5, 239-246 (2002).
29. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).
30. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927 (1999).
31. Toni, N., Buchs, P. A., Nikonenko, I., Bron, C. R. & Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425 (1999).
32. Hatada, Y., Wu, F., Sun, Z. Y., Schacher, S. & Goldberg, D. J. Presynaptic morphological changes associated with long- term synaptic facilitation are triggered by actin polymerization at preexisting varicosities. J. Neurosci. 20, RC82 (2000).
33. Colicos, M. A., Collins, B. E., Sailor, M. J. & Goda, Y Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107, 605-616 (2001).
34. Beaumont, V., Zhong, N., Froemke, R. C., Ball, R. W. & Zucker, R. S. Temporal synaptic tagging by Ih activation and actin: involvement in long-term facilitation and cAMP-induced synaptic enhancement. Neuron 33, 601-613 (2002).
35. Beaumont, V., Zhong, N., Fletcher, R., Froemke, R. C. & Zucker, R. S. Phosphorylation and local presynaptic protein synthesis in calcium- and calcineurin-dependent induction of crayfish long-term facilitation. Neuron 32, 489-501 (2001).
36. Ostroff, L. E., Fiala, J. C., Allwardt, B. & Harris, K. M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron (in the press).
37. Krichevsky, A. M. & Kosik, K. S. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32, 683-696 (2001).
38. Rook, M. S., Lu, M. & Kosik, K. S. CaMKIIα 3' untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20, 6385-6393 (2000).
39. Khan, A., Pepio, A. M. & Sossin, W. S. Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysla synaptosomes. J. Neurosci. 21, 382-391 (2001).
40. Scheetz, A. J., Nairn, A. C. & Constantine-Paton, M. NMDA receptor-mediated control of protein synthesis at developing synapses. Nature Neurosci. 3, 211-216 (2000).
41. Huang, Y. S., Jung, M. Y, Sarkissian, M. & Richter, J. D. n-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and aCaMKII mRNA polyadenylation at synapses. EMBO J. 21, 2139-2148 (2002).
42. Pinkstaff, J. K., Chappell, S. A., Mauro, V. P., Edelman, G. M. & Krushel, L. A. Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc. Natl Acad. Sci. USA 98, 2770-2775 (2001).
43. Lohof, A. M., Ip, N. Y. & Poo, M. M. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353 (1993).
44. Levine, E. S., Dreyfus, C. F., Black, I. B. & Plummer, M. R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl Acad. Sci. USA 92, 8074-8077 (1995).
45. Kang, H. & Schuman, E. M. Long-lasting neurotrophin- induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662 (1995).
46. Kovalchuk, Y, Hanse, E., Kafitz, K. W. & Konnerth, A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729-1734 (2002).
47. Patterson, S. L., Grover, L. M., Schwartzkroin, P A. & Bothwell, M. Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088 (1992).
48. Korte, M. et al. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl Acad. Sci. USA 92, 8856-8860 (1995).
49. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20, 709-726 (1998).
50. Tongiorgi, E., Righi, M. & Cattaneo, A. Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17, 9492-9505 (1997).
51. 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 21, 741-751 (1998).
52. Palacios, I. M. & Johnston, D. S. Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu. Rev. Cell Dev. Biol. 17, 569-614 (2001).
53. DiAntonio, A. et al. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452 (2001).
54. Campbell, D. S. & Holt, C. E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026 (2001).
55. Callen, E. J. & Boyd, T L. Examination of a backchaining/counterconditioning process during the extinction of conditioned fear. Behav. Res. Ther. 28, 261-271 (1990).
56. Steward, O. & Schuman, E. M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299-325 (2001).
57. 2+/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci. 19, 7823-7833 (1999).
58. Aakalu, G., Smith, W. B., Nguyen, N., Jiang, C. & Schuman, E. M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30, 489-502 (2001).
59. Job, C. & Eberwine, J. Identification of sites for exponential translation in living dendrites. Proc. Natl Acad. Sci. USA 98, 13037-13042 (2001).
60. Spencer, G. E. et al. Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J. Neurobiol. 44, 72-81 (2000).
61. Ghirardi, M., Montarolo, P G. & Kandel, E. R. A novel intermediate stage in the transition between short- and long- term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14, 413-420 (1995).
62. Sutton, M. A. & Carew, T. J. Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 26, 219-231 (2000).
63. Sutton, M. A., Ide, J., Masters, S. E. & Carew, T. J. Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in Aplysia. Learn. Mem. 9, 29-40 (2002).
64. Sherff, C. M. & Carew, T. J. Coincident induction of long- term facilitation in Aplysia: cooperativity between cell bodies and remote synapses. Science 285, 1911-1914 (1999).
65. Kang, H. & Schuman, E. M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406 (1996).
66. Huber, K. M., Kayser, M. S. & Bear, M. F. Role for rapid dendritic protein synthesis in hippocampal mGluR- dependent long-term depression. Science 288, 1254-1257 (2000).
67. Miller, S. et al. Disruption of dendritic translation of CaMKIIa impairs stabilization of synaptic plasticity and memory consolidation. Neuron (in the press).
68. Lanahan, A. & Worley, P. Immediate-early genes and synaptic function. Neurobiol. Learn. Mem. 70, 37-43 (1998).
69. Leil, T. A., Ossadtchi, A., Cortes, J. S., Leahy, R. M. & Smith, D. J. Finding new candidate genes for learning and memory. J. Neurosci. Res. 68, 127-137 (2002).
70. Dubnau, J. & Tully, T. Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21, 407-444 (1998).
71. Grosshans, H. & Slack, F. J. Micro-RNAs: small is plentiful. J. Cell Biol. 156, 17-21 (2002).
72. Ambros, V. MicroRNAs: tiny regulators with great potential. Cell 107, 823-826 (2001).
73. Barco, A., Alarcon, J. M. & Kandel, E. R. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108, 689-703 (2002)