Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons

Molecular Biology of the Cell

Volumn 10, Issue 9, 1999, Pages 2945-2953

  Köhrmann, Martin ^a,b   Luo, Ming ^c   Kaether, Christoph ^a   DesGroseillers, Luc ^c   Dotti, Carlos G ^a   Kiebler, Michael A ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; RNA;

ANIMAL CELL; ARTICLE; CELL GRANULE; CELLULAR DISTRIBUTION; DENDRITE; EMBRYO; HIPPOCAMPUS; MICROTUBULE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; RAT; RNA TRANSLATION; RNA TRANSPORT; SYNAPSE;

ANIMALIA;

EID: 0344466778     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.9.2945     Document Type: Article

References (39)

1. Ainger, K., Avossa, D., Morgan, F., Hill, S.J., Barry, C., Barbarese, E., and Carson, J.H. (1993). Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J. Cell Biol. 123, 431-441.
2. Bassell, G., 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 β-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251-265.
3. Bertrand, E., Chartrand, P., Schaefer, M., Shenoy, S.M., Singer, R.H., and Long, R.M (1998). Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2, 437-445.
4. Bradke, E, and Dotti, C.G. (1998). Videomicroscopy of living microinjected hippocampal neurons in culture. In: Microinjection and Transgenesis: Strategies and Protocols, ed A. Cid-Arregui and A. Garcia-Carrancá, Heidelberg: Springer-Verlag, 81-94.
5. Bradke, F., and Dotti, C.G. (1999). The role of local actin instability in axon formation. Science 283, 1931-1934.
6. Brady, S.T., Lasek, R.J., and Allen, R.D. (1982). Fast axonal transport in extruded cytoplasm from squid giant axon. Science 218, 1129-1131.
7. Carson, J.H., Kwon, S., and Barbarese, E. (1998). RNA trafficking in myelinating cells. Curr. Opin. Neurobiol. 8, 607-612.
8. Carson, J.H., Worboys, K., Ainger, K., and Barbarese, E. (1997). Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin. Cell. Motil. Cytoskeleton 38, 318-328.
9. de Hoop, M.J., Meyn, L., and Dotti, C.G. (1998). Culturing hippocampal neurons and astrocytes from fetal rodent brain. In: Cell Biology: A Laboratory Handbook, 2nd ed., ed. J.E. Celis, 2nd ed., San Diego: Academic Press, 154-163.
10. De Strooper, B., Simons, M., Multhaup, G., Van Leuven, F., Beyreuther, K., and Dotti, C.G. (1995). Production of intracellular amyloid-containing fragments in hippocampal neurons expressing human amyloid precursor protein and protection against amyloidogenesis by subtle amino acid substitutions in the rhodent sequence. EMBO J. 14, 4932-4938.
11. Deshler, J.O., Highett, M.I., Abramson, T., and Schnapp, B.J. (1998). A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr. Biol. 8, 489-496.
12. Deshler, J.O., Highett, M.I., and Schnapp, B.J. (1997). Localization of Xenopus Vg1 mRNA by VERA protein and the endoplasmic reticulum. Science 276, 1128-1131.
13. Driever, W., and Nüsslein-Volhard, C. (1988). The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner, Cell 54, 95-104.
14. Ephrussi, A., Dickinson, L.K., and Lehmann, R. (1991). Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37-50.
15. Ferrandon, D., Elphick, L., Nüsslein-Volhard, C., and St. Johnston, D. (1994). Staufen protein associates with the 3-UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79, 1221-1231.
16. Goslin, K., and Banker, G. (1997). Rat hippocampal neurons in low-density culture. In: Culturing Nerve Cells, ed. G. Banker and K. Goslin, Cambridge, MA: MIT Press, 251-281.
17. Haubensack, W., Narz, F., Heumann, R., and Leßmann, V. (1998). BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J. Cell Sci. 111, 1483-1493.
18. Hazelrigg, T. (1998). The destinies and destinations of RNAs (meeting review). Cell 95, 451-460.
19. Hoek, K., Kidd, G.J., Carson, J.H., and Smith, R. (1998). hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. Biochemistry 37, 7021-7029.
20. Holmes, E., Hermanson, G., Cole, R., and de Vellis, J. (1988). Developmental expression of glial-specific mRNAs in primary cultures of rat brain visualized by in situ hybridization. J. Neurosci. 19, 389-396.
21. Kaether, C., Salm, T., Glombik, M., Almers, W., and Gerdes, H.-H. (1997). Targeting of GFP to neuroendocrine secretory granules: a new tool for real time studies of regulated protein secretion. Eur. J. Cell Biol. 74, 133-142.
22. Kiebler, M., Hemraj, I., Verkade, P., Köhrmann, M., Fortes, P., Marión, R.M., Ortín, 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. Knowles, R.B., and Kosik, K.S. (1997). Neurotrophin-3 signals redistribute RNA in neurons. Proc. Natl. Acad. Sci. USA 94, 14804-14808.
24. Knowles, R.B., Sabry, J.H., Martone, M.E., Deerinck, T.J., Ellisman, M.H., Bassell, G.J., and Kosik, K.S. (1996). Translocation of RNA granules in living neurons. J. Neurosci. 16, 7812-7820.
25. Kuhl, D., and Skehel, P. (1998). Dendritic localization of mRNAs. Curr. Opin. Neurobiol. 8, 600-606.
26. Marión, R.M., Fortes, P., Beloso, A., Dotti, C.G., and Ortín, J. (1999). A human sequence homologue of staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough ER. Mol. Cell. Biol. 19, 2212-2219.
27. 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.
28. Muslimov, I.A., Santi, E., Homel, P., Perini, S., Higgins, D., and Tiedge, H. (1997). RNA transport in dendrites: a cis-acting targeting element is contained within neuronal BC1 RNA. J. Neurosci. 17, 4722-4733.
29. Ross, A.F., Oleynikov, Y., Kislauskis, E.H., Taneja, K.L., and Singer, R.H. (1997). Characterization of a β-actin mRNA zipcode-binding protein. Mol. Cell. Biol. 17, 2158-2165.
30. Simons, M., De Strooper, B., Multhaup, G., Tienari, P.J., Dotti, C.G., and Beyreuther, K. (1996). Amyloidogenic processing of the human amyloid precursor protein in primary cultures of rat hippocampal neurons. J. Neurosci. 16, 899-908.
31. Spector, I., Shochet, N.R., Blasberger, D., and Kashman, Y. (1989). Latrunculins - novel marine macrolides that disrupt microfilament organization and affect cell growth: I. comparison with cytochalasin D. Cell Motil. Cytoskeleton 13, 127-144.
32. St. Johnston, D. (1995). The intracellular localization of mRNAs. Cell 81, 161-170.
33. St. Johnston, D., Beuchle, D., and Nuesslein-Volhard, C. (1991). staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63.
34. Tiedge H, Bloom FE, Richter D. (1999). RNA, whither goest thou? Science 283, 186-187.
35. Wacker, I., Kaether, A., Krömer, A., Migala, A., Almers, W., and Gerdes, H.-H. (1997). Microtubule-dependent transport of secretory vesicles visualized in real time with a GFP-tagged secretory protein. J. Cell Sci. 110, 1453-1463.
36. Wallace, C.S., Lyford, G.L., Worley, P.F., and Steward, O. (1998). Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. J. Neurosci. 18, 26-35.
37. Wang, S., and Hazelrigg, T. (1994). Implications for bed mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature 369, 400-403.
38. Wickham, L., Duchaîne, T., Luo, M., Nabi, I.R., and DesGroseillers, L. (1999). Mammalian Staufen is a double-stranded RNA- and tubulin-binding protein which localizes to the rough ER. Mol. Cell. Biol. 19, 2220-2230.
39. Wilhelm, J.E., and Vale, R.D. (1993). RNA on the move: the mRNA localization pathway. J. Cell Biol. 323, 269-274.