Synaptic tagging — who's it? (original) (raw)

References

  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).Shows that long-lasting, transcription-dependent forms of plasticity can occur in a synapse-specific manner; together with reference 12 , this paper provides evidence for synaptic tagging in Aplysia.
    Article CAS Google Scholar
  2. Frey, U. & Morris, R. G. Synaptic tagging and long-term potentiation. Nature 385, 533–536 (1997).This paper and reference 3 provide evidence for synaptic tagging in rat hippocampal neurons.
    Article CAS Google Scholar
  3. Frey, U. & Morris, R. G. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37, 545–552 (1998).
    Article CAS Google Scholar
  4. Shi, S. H. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811–1816 (1999).
    Article CAS Google Scholar
  5. Tovar, K. R. & Westbrook, G. L. Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255–264 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  7. El-Husseini, A. E. et al. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108, 849–863 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  9. Osten, P., Valsamis, L., Harris, A. & Sacktor, T. C. Protein synthesis-dependent formation of protein kinase Mζ in long-term potentiation. J. Neurosci. 16, 2444–2451 (1996).
    Article CAS Google Scholar
  10. Ling, D. S. et al. Protein kinase Mζ is necessary and sufficient for LTP maintenance. Nature Neurosci. 5, 295–296 (2002).
    Article CAS Google Scholar
  11. Drier, E. A. et al. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nature Neurosci. 5, 316–324 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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 Aplysia. J. Neurosci. 15, 7592–7603 (1995).
    Article CAS Google Scholar
  14. Hegde, A. N. et al. Ubiquitin C-terminal hydrolase is an immediate–early gene essential for long-term facilitation in Aplysia. Cell 89, 115–126 (1997).
    Article CAS Google Scholar
  15. Chain, D. G. et al. Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22, 147–156 (1999).
    Article CAS Google Scholar
  16. Bailey, C. H. & Kandel, E. R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55, 397–426 (1993).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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 Aplysia. Science 256, 645–649 (1992).
    Article CAS Google Scholar
  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 Aplysia. Science 256, 638–644 (1992).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  22. Tanaka, H. et al. Molecular modification of N-cadherin in response to synaptic activity. Neuron 25, 93–107 (2000).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  25. Lu, Q. et al. δ-Catenin, an adhesive junction-associated protein which promotes cell scattering. J. Cell Biol. 144, 519–532 (1999).
    Article CAS Google Scholar
  26. Izawa, I., Nishizawa, M., Ohtakara, K. & Inagaki, M. Densin-180 interacts with δ-catenin/neural plakophilin-related armadillo repeat protein at synapses. J. Biol. Chem. 277, 5345–5350 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  29. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).
    Article CAS Google Scholar
  30. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927 (1999).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  34. Beaumont, V., Zhong, N., Froemke, R. C., Ball, R. W. & Zucker, R. S. Temporal synaptic tagging by _I_h activation and actin: involvement in long-term facilitation and cAMP-induced synaptic enhancement. Neuron 33, 601–613 (2002).Provides evidence that the activation of presynaptic I h channels can serve as a synaptic tag at the crayfish neuromuscular junction. This tag does not interact with products of transcription; rather, it allows the neuron to integrate synaptic stimulation over time.
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).Shows that strong synaptic stimulation increases the percentage of spines containing polyribosome clusters in the rat hippocampus.
  37. Krichevsky, A. M. & Kosik, K. S. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32, 683–696 (2001).Provides evidence that RNA granules are storage sites for mRNAs in distal dendrites, and that depolarization releases mRNAs from the granules to polysomes, where they are actively translated.
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  39. Khan, A., Pepio, A. M. & Sossin, W. S. Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci. 21, 382–391 (2001).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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 αCaMKII mRNA polyadenylation at synapses. EMBO J. 21, 2139–2148 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  45. Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658–1662 (1995).
    Article CAS Google Scholar
  46. Kovalchuk, Y., Hanse, E., Kafitz, K. W. & Konnerth, A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729–1734 (2002).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  49. Tao, X., Finkbeiner, S., Arnold, D. B., Shaywitz, A. J. & Greenberg, M. E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20, 709–726 (1998).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  53. DiAntonio, A. et al. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449–452 (2001).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  56. Steward, O. & Schuman, E. M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299–325 (2001).
    Article CAS Google Scholar
  57. Ouyang, Y., Rosenstein, A., Kreiman, G., Schuman, E. M. & Kennedy, M. B. Tetanic stimulation leads to increased accumulation of Ca2+/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci. 19, 7823–7833 (1999).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  59. Job, C. & Eberwine, J. Identification of sites for exponential translation in living dendrites. Proc. Natl Acad. Sci. USA 98, 13037–13042 (2001).
    Article CAS Google Scholar
  60. Spencer, G. E. et al. Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J. Neurobiol. 44, 72–81 (2000).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article Google Scholar
  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).Shows that coincident, subthreshold application of serotonin to somata and processes of Aplysia neurons produces LTF that is dependent on local protein synthesis in the process.
    Article CAS Google Scholar
  65. Kang, H. & Schuman, E. M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402–1406 (1996).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  67. Miller, S. et al. Disruption of dendritic translation of CaMKIIα impairs stabilization of synaptic plasticity and memory consolidation. Neuron (in the press).Describes a mouse in which the α-CaMKII mRNA is not dendritically localized, and shows a role for local protein synthesis in late-phase LTP and long-term forms of memory.
  68. Lanahan, A. & Worley, P. Immediate–early genes and synaptic function. Neurobiol. Learn. Mem. 70, 37–43 (1998). | PubMed
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  70. Dubnau, J. & Tully, T. Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21, 407–444 (1998).
    Article CAS Google Scholar
  71. Grosshans, H. & Slack, F. J. Micro-RNAs: small is plentiful. J. Cell Biol. 156, 17–21 (2002).
    Article CAS Google Scholar
  72. Ambros, V. MicroRNAs: tiny regulators with great potential. Cell 107, 823–826 (2001).
    Article CAS Google Scholar
  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).Describes a mouse in which expression of a constitutively active form of the transcription factor CREB leads to a reduced threshold for producing long-lasting LTP. The subthreshold stimuli might produce tags that can capture the products of transcription that are induced by CREB activation.
    Article CAS Google Scholar

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