A GFP-based system to uncouple mRNA transport from translation in a single living neuron

Molecular Biology of the Cell

Volumn 14, Issue 4, 2003, Pages 1570-1582

  Macchi, Paolo ^a   Hemraj, Indradeo ^a   Goetze, Bernhard ^a   Grunewald, Barbara ^a   Mallardo, Massimo ^a   Kiebler, Michael A ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; GREEN FLUORESCENT PROTEIN; IRON; MESSENGER RNA; PROTEIN KINASE (CALCIUM,CALMODULIN);

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; EMBRYO; GENETIC TRANSFECTION; HIPPOCAMPUS; IRON RESPONSIVE ELEMENT; NERVE CELL; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; RNA TRANSLATION; RNA TRANSPORT; STOP CODON; SYNAPSE;

5' UNTRANSLATED REGIONS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; CELLS, CULTURED; COS CELLS; CRICETINAE; DENDRITES; FERRITINS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; IRON; LUMINESCENT PROTEINS; NEURONS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN BIOSYNTHESIS; RATS; RECOMBINANT PROTEINS; RNA, MESSENGER; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 0038644529     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0505     Document Type: Article

References (47)

1. Aakalu, G., Smith, W.B., Nguyen, N., Jiang, C., and Schuman, E.M. (2001). Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30, 489-502.
2. Bailey, C.H., Bartsch, D., and Kandel, E.R. (1996). Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. USA 93, 13445-13452.
3. Blichenberg, A., Schwanke, B., Rehbein, M., Garner, C.C., Richter, D., and Kindler, S. (1999). Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci. 19, 8818-8829.
4. 2+/calmodulin-dependent protein kinase II. Eur. J. Neurosci. 13, 1881-1888.
5. 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.
6. Crino, P., Khodakhah, K., Becker, K., Ginsberg, S., Hemby, S., and Eberwine, J. (1998). Presence and phosphorylation of transcription factors in developing dendrites. Proc. Natl. Acad. Sci. USA 95, 2313-2318.
7. De Gregorio, E., Preiss, T., and Hentze, M.W. (1999). Translation driven by an eIF4G core domain in vivo. EMBO J. 18, 4865-4874.
8. Duchaîne, T., Wang, H.J., Luo, M., Steinberg, S.V., Nabi, I.R., and DesGroseillers, L. (2000). A novel murine Staufen isoform modulates the RNA content of Staufen complexes. Mol. Cell. Biol. 20, 5592-5601.
9. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
10. Feig, S., and Lipton, P. (1993). Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. J. Neurosci. 13, 1010-1021.
11. Fischer, M., Kaech, S., Knutti, D., and Matus, A. (1998). Rapid actin-based plasticity in dendritic spines. Neuron 20, 847-854.
12. Frey, U., Krug, M., Reymann, K.G., and Matthies, H. (1988). Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452, 57-65.
13. Frey, U., and Morris, R.G. (1997). Synaptic tagging and long-term potentiation. Nature 385, 533-536.
14. Goldin, M., Segal, M., and Avignone, E. (2001). Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J. Neurosci. 21, 186-193.
15. Goossen, B., Caughman, S.W., Harford, J.B., Klausner, R.D., and Hentze, M.W. (1990). Translational repression by a complex between the iron-responsive element of ferritin mRNA and its specific cytoplasmic binding protein is position-dependent in vivo. EMBO J. 9, 4127-4133.
16. Goslin, K., Asmussen, H., and Banker, G. (1998). Rat hippocampal neurons in low-density culture. In: Culturing Nerve Cells, ed. G. Banker and K. Goslin, Cambridge, MA: MIT Press, 339-370.
17. Henderson, B.R., and Kuhn, L.C. (1995). Differential modulation of the RNA-binding proteins IRP-1 and IRP-2 in response to iron. IRP-2 inactivation requires translation of another protein. J. Biol. Chem. 270, 20509-15.
18. Hentze, M.W., Caughman, S.W., Rouault, T.A., Barriocanal, J.G., Dancis, A., Harford, J.B., and Klausner, R.D. (1987). Identification of the iron-responsive element for the translational regulation of humanferritin mRNA. Science 238, 1570-1573.
19. Hentze, M.W., and Kühn, L.C. (1996). Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 93, 8175-8182.
20. Ishimoto, T., Fujimori, K., Kasai, M., and Taguchi, T. (2000). Dendritic translocation of the rat ferritin H chain mRNA. Biochem. Biophys. Res. Commun. 272, 789-793.
21. Kang, H., and Schuman, E.M. (1996). A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406.
22. Kiebler, M.A., Hemraj, I., Verkade, P., K6hrmann, M., Fortes, P., Marion, R.M., Ortin, J., and Dotti, C.G. (1999). The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J. Neurosci. 19, 288-297.
23. Köhrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C.G., and Kiebler, M.A. (1999a). Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10, 2945-2953.
24. Köhrmann, M., Haubensak, W., Hemraj, I., Kaether, C., Lessmann, V.J., and Kiebler, M.A. (1999b). Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J. Neurosci. Res. 58, 831-835.
25. Kuhl, D., and Skehel, P. (1998). Dendritic localization of mRNAs. Curr. Opin. Neurobiol. 8, 600-606.
26. LaVaute, T. et al. (2001). Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat. Genet. 27, 209-214.
27. Malgaroli, A., and Tsien, R.W. (1992). Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357, 134-139.
28. Martin, K.C., Casadio, A., Zhu, H.E.Y., 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.
29. Martin, K.C., Barad, M., and Kandel, E.R. (2000). Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 10, 587-592.
30. Mayford, M., Baranes, D., Podsypanina, K., and Kandel, E.R. (1996). The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc. Natl. Acad. Sci. USA 93, 13250-13255.
31. Miller, S., Yasuda, M., Coats, J.K., Jones, Y., Martone, M.E., and Mayford, M. (2002). Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36, 507-519.
32. Mori, Y., Imaizumi, K., Katayama, T., Yoneda, T., and Tohyama, M. (2000). Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat. Neurosci. 3, 1079-1084.
33. Nguyen, P.V., Abel, T., and Kandel, E.R. (1994). Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104-1107.
34. Paraskeva, E., Gray, N.K., Schlager, B., Wehr, K., and Hentze, M.W. (1999). Ribosomal pausing and scanning arrest as mechanisms of translational regulation from cap-distal iron-responsive elements. Mol. Cell. Biol. 19, 807-816.
35. Rook, M.S., Lu, M., and Kosik, K.S. (2000). CaMKII alpha 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20, 6385-6393.
36. Rosa, P., Hille, A., Lee, R.W., Zanini, A., De Camilli, P., and Huttner, W.B. (1985). Secretogranins I and II: two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway. J. Cell Biol. 101, 1999-2011.
37. Rouault, T.A., Hentze, M.W., Caughman, S.W., Harford, J.B., and Klausner, R.D. (1988). Binding of a cytosolic protein to the ironresponsive element of human ferritin messenger RNA. Science 241, 1207-1210.
38. Schalinske, K.L., Chen, O.S., and Eisenstein, R.S. (1998). Iron differentially stimulates translation of mitochondrial aconitase and ferritin mRNAs in mammalian cells. Implications for iron regulatory proteins as regulators of mitochondrial citrate utilization. J. Biol. Chem. 273, 3740-3746.
39. Siddappa, A.J., Rao, R.B., Wobken, J.D., Leibold, E.A., Connor, J.R., and Georgieff, M.K. (2002). Developmental changes in the expression of iron regulatory proteins and iron transport proteins in the perinatal rat brain. J. Neurosci. Res. 68, 761-775.
40. Smith, W.B., Aakalu, G., and Schuman, E.M. (2001). Local protein synthesis in neurons. Curr. Biol. 11, R901-R903.
41. St. Johnston, D. (1995). The intracellular localization of messenger RNAs. Cell 81, 161-170.
42. Stanton, P.K., and Sarvey, J.M. (1984). Blockage of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci. 4, 3080-3088.
43. Steward, O., and Schuman, E.M. (2001). Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299-325.
44. Wells, D.G., Dong, X., Quinlan, E.M., Huang, Y.S., Bear, M.F., Richter, J.D., and Fallon, J.R. (2001). A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J. Neurosci. 21, 9541-9548.
45. Wickham, L., Duchaine, T., Luo, M., Nabi, IR., and DesGroseillers, L. (1999). Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2220-2230.
46. Wu, L. et al. (1998). CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21, 1129-1139.
47. Zucker, M., and Stiegler, P. (1981). Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 9, 133.