Presynaptic translation: Stepping out of the postsynaptic shadow

Frontiers in Neural Circuits

Volumn 3, Issue NOV, 2009, Pages

  Akins, Michael R ^a   Berk Rauch, Hanna E ^b   Fallon, Justin R ^a  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Autism; FMRP; Fragile X syndrome; Local translation; mRNA; mTOR; Presynaptic plasticity; Synaptic plasticity

Indexed keywords

EID: 79952441030     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.04.017.2009     Document Type: Review

References (78)

1. Alvarez, J., Giuditta, A., and Koenig, E. (2000). Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype: with a critique of slow transport theory. Prog. Neurobiol. 62, 1-62.
2. Aronov, S., Aranda, G., Behar, L., and Ginzburg, I. (2002). Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J. Cell. Sci. 115, 3817-3827.
3. Atlas, R., Behar, L., Elliott, E., and Ginzburg, I. (2004). The insulin-like growth factor mRNA binding-protein IMP-1 and the Ras-regulatory protein G3BP associate with tau mRNA and HuD protein in differentiated P19 neuronal cells. J. Neurochem. 89, 613-626.
4. Bailey, C. H., Montarolo, P., Chen, M., Kandel, E. R., and Schacher, S. (1992). Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron 9, 749-758.
5. Bassell, G. J., Zhang, H., Byrd, A. L., Femino, A. M., Singer, R. H., Taneja, K. L., Lifshitz, L. M., Herman, I. M., and Kosik, K. S. (1998). Sorting of betaactin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251-265.
6. Beaumont, V., Zhong, N., Fletcher, R., Froemke, R. C., and Zucker, R. S. (2001). Phosphorylation and local presynaptic protein synthesis in calcium- and calcineurin-dependent induction of crayfish long-term facilitation. Neuron 32, 489-501.
7. Bi, J., Tsai, N., Lin, Y., Loh, H. H., and Wei, L. (2006). Axonal mRNA transport and localized translational regulation of κ-opioid receptor in primary neurons of dorsal root ganglia. Proc. Natl. Acad. Sci. 103, 19919-19924.
8. Boylan, K. L. M., Mische, S., Li, M., Marqués, G., Morin, X., Chia, W., and Hays, T. S. (2008). Motility screen identifies Drosophila IGF-II mRNAbinding protein-zipcode-binding protein acting in oogenesis and synaptogenesis. PLoS Genet. 4, e36. doi: 10.1371/journal.pgen.0040036.
9. Bramham, C. R., and Wells, D. G. (2007). Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8, 776-789.
10. Brown, V., Jin, P., Ceman, S., Darnell, J. C., O'Donnell, W. T., Tenenbaum, S. A., Jin, X., Feng, Y., Wilkinson, K. D., Keene, J. D., Darnell, R. B., and Warren, S. T. (2001). Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in Fragile X syndrome. Cell 107, 477-487.
11. Bunge, M. B. (1973). Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture. J. Cell Biol. 56, 713-735.
12. Cai, D., Chen, S., and Glanzman, D. L. (2008). Postsynaptic Regulation of long-term facilitation in Aplysia. Curr. Biol. 18, 920-925.
13. Campbell, D. S., and Holt, C. E. (2001). Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026.
14. Casadio, A., Martin, K. C., Giustetto, M., Zhu, H., Chen, M., Bartsch, D., Bailey, C. H., and Kandel, E. R. (1999). 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.
15. Christie, S. B., Akins, M. R., Schwob, J. E., and Fallon, J. R. (2009). The FXG: a presynaptic Fragile X granule expressed in a subset of developing brain circuits. J. Neurosci. 29, 1514-1524.
16. Cox, L. J., Hengst, U., Gurskaya, N. G., Lukyanov, K. A., and Jaffrey, S. R. (2008). Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat. Cell Biol. 10, 149-159.
17. Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T., and Darnell, R. B. (2001). Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489-499.
18. De Paola, V., Holtmaat, A., Knott, G., Song, S., Wilbrecht, L., Caroni, P., and Svoboda, K. (2006). Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49, 861-875.
19. Doyle, J. P., Dougherty, J. D., Heiman, M., Schmidt, E. F., Stevens, T. R., Ma, G., Bupp, S., Shrestha, P., Shah, R. D., Doughty, M. L., Gong, S., Greengard, P., and Heintz, N. (2008). Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749-762.
20. Droz, B., and Barondes, S. M. (1969). Nerve endings: rapid appearance of labeled protein shown by electron microscope radioautography. Science 165, 1131-1133.
21. Feng, Y., Gutekunst, C., Eberhart, D. E., Yi, H., Warren, S. T., and Hersch, S. M. (1997). Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17, 1539-1547.
22. Gatto, C. L., and Broadie, K. (2008). Temporal requirements of the fragile X mental retardation protein in the regulation of synaptic structure. Development 135, 2637-2648.
23. Giustetto, M., Hegde, A. N., Si, K., Casadio, A., Inokuchi, K., Pei, W., Kandel, E. R., and Schwartz, J. H. (2003). Axonal transport of eukaryotic translation elongation factor 1α mRNA couples transcription in the nucleus to long-term facilitation at the synapse. Proc. Natl. Acad. Sci. U.S.A. 100, 13680-13685.
24. Glanzman, D. L., Kandel, E. R., and Schacher, S. (1990). Target-dependent structural changes accompanying longterm synaptic facilitation in Aplysia neurons. Science 249, 799-802.
25. Gogolla, N., Galimberti, I., and Caroni, P. (2007). Structural plasticity of axon terminals in the adult. Curr. Opin. Neurobiol. 17, 516-524.
26. Goldstein, A. Y., Wang, X., and Schwarz, T. L. (2008). Axonal transport and the delivery of pre-synaptic components. Curr. Opin. Neurobiol. 18, 495-503.
27. Grabham, P. W., Wu, F., Schacher, S., and Goldberg, D. J. (2005). Initiating morphological changes associated with long-term facilitation in Aplysia is independent of transcription or translation in the cell body. J. Neurobiol. 64, 202-212.
28. Hanson, J. E., and Madison, D. V. (2007). Presynaptic Fmr1 genotype influences the degree of synaptic connectivity in a mosaic mouse model of Fragile X syndrome. J. Neurosci. 27, 4014-4018.
29. Hatada, Y., Wu, F., Sun, Z., Schacher, S., and Goldberg, D. J. (2000). Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicositis. J. Neurosci. 20, 82RC.
30. Hengst, U., Cox, L. J., Macosko, E. Z., and Jaffrey, S. R. (2006). Functional and selective RNA interference in developing axons and growth cones. J. Neurosci. 26, 5727-5732.
31. Hirokawa, N., and Noda, Y. (2008). Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol. Rev. 88, 1089-1118.
32. Huang, C., and Hsu, K. (2004). Local protein synthesis and GABAB receptors regulate the reversibility of long-term potentiation at murine hippocampal mossy fibre-CA3 synapses. J. Physiol. 561, 91-108.
33. Kelleher, R. J., and Bear, M. F. (2008). The autistic neuron: troubled translation? Cell 135, 401-406.
34. Koenig, E., Martin, R., Titmus, M., and Sotelo-Silveira, J. R. (2000). Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelinated axons. J. Neurosci. 20, 8390-8400.
35. Leung, K., van Horck, F. P., Lin, A. C., Allison, R., Standart, N., and Holt, C. E. (2006). Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin- 1. Nat. Neurosci. 9, 1247-1256.
36. Lin, A. C., and Holt, C. E. (2007). Local translation and directional steering in axons. EMBO J. 26, 3729-3736.
37. Lin, A. C., and Holt, C. E. (2008). Function and regulation of local axonal translation. Curr. Opin. Neurobiol. 18, 60-68.
38. Liu, K., Hu, J.-Y., Wang, D., and Schacher, S. (2003). Protein synthesis at synapse versus cell body: enhanced but transient expression of long-term facilitation at isolated synapses. J. Neurobiol. 56, 275-286.
39. Lyles, V., Zhao, Y., and Martin, K. C. (2006). Synapse formation and mRNA localization in cultured aplysia neurons. Neuron 49, 349-356.
40. Martin, K. C., Casadio, A., Zhu, H., Yaping, E., Rose, J. C., Chen, M., Bailey, C. H., and Kandel, E. R. (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.
41. Menon, K. P., Andrews, S., Murthy, M., Gavis, E. R., and Zinn, K. (2009). The translational repressors nanos and pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J. Neurosci. 29, 5558-5572.
42. Menon, K. P., Sanyal, S., Habara, Y., Sanchez, R., Wharton, R. P., Ramaswami, M., and Zinn, K. (2004). The translational repressor pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF- 4E. Neuron 44, 663-676.
43. Merianda, T. T., Lin, A. C., Lam, J. S., Vuppalanchi, D., Willis, D. E., Karin, N., Holt, C. E., and Twiss, J. L. (2009). A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol. Cell. Neurosci. 40, 128-142.
44. Miller, L. C., Blandford, V., McAdam, R., Sanchez-Carbente, M. R., Badeaux, F., DesGroseillers, L., and Sossin, W. S. (2009). Combinations of DEAD box proteins distinguish distinct types of RNA: protein complexes in neurons. Mol. Cell. Neurosci. 40, 485-495.
45. Miniaci, M. C., Kim, J., Puthanveettil, S. V., Si, K., Zhu, H., Kandel, E. R., and Bailey, C. H. (2008). Sustained CPEBdependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron 59, 1024-1036.
46. Miyashiro, K. Y., Beckel-Mitchener, A., Purk, T. P., Becker, K. G., Barret, T., Liu, L., Carbonetto, S., Weiler, I. J., Greenough, W. T., and Eberwine, J. (2003). RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37, 417-431.
47. Nicoll, R. A., and Schmitz, D. (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863-876.
48. Pan, L., Zhang, Y. Q., Woodruff, E., and Broadie, K. (2004). The Drosophila Fragile X gene negatively regulates neuronal elaboration and synaptic differentiation. Curr. Biol. 14, 1863-1870.
49. Pelkey, K. A., and McBain, C. J. (2008). Target-cell-dependent plasticity within the mossy fibre-CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites. J. Physiol. (Lond.) 586, 1495-1502.
50. Roche, F. K., Marsick, B. M., and Letourneau, P. C. (2009). Protein synthesis in distal axons is not required for growth cone responses to guidance cues. J. Neurosci. 29, 638-652.
51. Salin, P. A., Malenka, R. C., and Nicoll, R. A. (1996). Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16, 797-803.
52. Schacher, S., Wu, F., Panyko, J. D., Sun, Z., and Wang, D. (1999). Expression and branch-specific export of mRNA are regulated by synapse formation and interaction with specific postsynaptic targets. J. Neurosci. 19, 6338-6347.
53. Sebeo, J., Hsiao, K., Bozdagi, O., Dumitriu, D., Ge, Y., Zhou, Q., and Benson, D. L. (2009). Requirement for protein synthesis at developing synapses. J. Neurosci. 29, 9778-9793.
54. Sherff, C. M., and Carew, T. J. (1999). Coincident induction of long-term facilitation in aplysia: cooperativity between cell bodies and remote synapses. Science 285, 1911-1914.
55. Sherff, C. M., and Carew, T. J. (2004). Parallel somatic and synaptic processing in the induction of intermediate- term and long-term synaptic facilitation in Aplysia. Proc. Natl. Acad. Sci. U.S.A. 101, 7463-7468.
56. Si, K., Giustetto, M., Etkin, A., Hsu, R., Janisiewicz, A. M., Miniaci, M. C., Kim, J., Zhu, H., and Kandel, E. R. (2003a). A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific longterm facilitation in Aplysia. Cell 115, 893-904.
57. Si, K., Lindquist, S., and Kandel, E. R. (2003b). A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115, 879-891.
58. Smith, C. L., Afroz, R., Bassell, G. J., Furneaux, H. M., Perrone-Bizzozero, N. I., and Burry, R. W. (2004). GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J. Neurobiol. 61, 222-235.
59. Stettler, D. D., Yamahachi, H., Li, W., Denk, W., and Gilbert, C. D. (2006). Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 49, 877-887.
60. Steward, O., and Levy, W. B. (1982). Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 2, 284-291.
61. Sudhof, T. C. (2008). Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911.
62. Sutton, M. A., and Schuman, E. M. (2006). Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127, 49-58.
63. Taylor, A. M., Berchtold, N. C., Perreau, V. M., Tu, C. H., Li Jeon, N., and Cotman, C. W. (2009). Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29, 4697-4707.
64. Taylor, A. M., Blurton-Jones, M., Rhee, S. W., Cribbs, D. H., Cotman, C. W., and Jeon, N. L. (2005). A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2, 599-605.
65. Tessier, C. R., and Broadie, K. (2008). Drosophila fragile X mental retardation protein developmentally regulates activity-dependent axon pruning. Development 135, 1547-1557.
66. Trudeau, L. E., and Castellucci, V. F. (1995). Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors. J. Neurosci. 15, 1275-1284.
67. van Niekerk, E. A., Willis, D. E., Chang, J. H., Reumann, K., Heise, T., and Twiss, J. L. (2007). Sumoylation in axons triggers retrograde transport of the RNAbinding protein La. Proc. Natl. Acad. Sci. U.S.A 104, 12913-12918.
68. Wang, D. O., Kim, S. M., Zhao, Y., Hwang, H., Miura, S. K., Sossin, W. S., and Martin, K. C. (2009). Synapse- and stimulus-specific local translation during long-term neuronal plasticity. Science 324, 1536-1540.
69. Wang, W., Niekerk, E. V., Willis, D. E., and Twiss, J. L. (2007). RNA transport and localized protein synthesis in neurological disorders and neural repair. Dev. Neurobiol. 67, 1166-1182.
70. Willis, D., Li, K. W., Zheng, J., Chang, J. H., Smit, A., Kelly, T., Merianda, T. T., Sylvester, J., van Minnen, J., and Twiss, J. L. (2005). Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 25, 778-791.
71. Willis, D. E., van Niekerk, E. A., Sasaki, Y., Mesngon, M., Merianda, T. T., Williams, G. G., Kendall, M., Smith, D. S., Bassell, G. J., and Twiss, J. L. (2007). Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol. 178, 965-980.
72. Wu, K. Y., Hengst, U., Cox, L. J., Macosko, E. Z., Jeromin, A., Urquhart, E. R., and Jaffrey, S. R. (2005). Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024.
73. Yan, D., Wu, Z., Chisholm, A. D., and Jin, Y. (2009). The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138, 1005-1018.
74. Yin, H. H., Davis, M. I., Ronesi, J. A., and Lovinger, D. M. (2006). The role of protein synthesis in striatal long-term depression. J. Neurosci. 26, 11811-11820.
75. Zhang, J., Hou, L., Klann, E., and Nelson, D. L. (2009). Altered hippocampal synaptic plasticity in the Fmr1 gene family knockout mouse models. J. Neurophysiol. 101, 2572-2580.
76. Zhang, X., and Poo, M. (2002). Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36, 675-688.
77. Zhang, Y. Q., Bailey, A. M., Matthies, H. J. G., Renden, R. B., Smith, M. A., Speese, S. D., Rubin, G. M., and Broadie, K. (2001). Drosophila Fragile X-related gene regulates the MAP1B homolog futsch to control synaptic structure and function. Cell 107, 591-603.
78. Zheng, J., Kelly, T. K., Chang, B., Ryazantsev, S., Rajasekaran, A. K., Martin, K. C., and Twiss, J. L. (2001). A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. 21, 9291-9303.