Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes

doi:10.1083/jcb.123.2.431

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Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes

K Ainger, D Avossa, F Morgan, SJ Hill, C Barry, E Barbarese and JH Carson
Department of Biochemistry, University of Connecticut Health Center, Farmington 06030.

We have studied transport and localization of MBP mRNA in oligodendrocytes in culture by microinjecting labeled mRNA into living cells and analyzing the intracellular distribution of the injected RNA by confocal microscopy. Injected mRNA initially appears dispersed in the perikaryon. Within minutes, the RNA forms granules which, in the case of MBP mRNA, are transported down the processes to the periphery of the cell where the distribution again becomes dispersed. In situ hybridization shows that endogenous MBP mRNA in oligodendrocytes also appears as granules in the perikaryon and processes and dispersed in the peripheral membranes. The granules are not released by extraction with non-ionic detergent, indicating that they are associated with the cytoskeletal matrix. Three dimensional visualization indicates that MBP mRNA granules are often aligned in tracks along microtubules traversing the cytoplasm and processes. Several distinct patterns of granule movement are observed. Granules in the processes undergo sustained directional movement with a velocity of approximately 0.2 micron/s. Granules at branch points undergo oscillatory motion with a mean displacement of 0.1 micron/s. Granules in the periphery of the cell circulate randomly with a mean displacement of approximately 1 micron/s. The results are discussed in terms of a multi-step pathway for transport and localization of MBP mRNA in oligodendrocytes. This work represents the first characterization of intracellular movement of mRNA in living cells, and the first description of the role of RNA granules in transport and localization of mRNA in cells.
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Liu, J., Hu, J.-Y., Wu, F., Schwartz, J. H., Schacher, S. (2006). Two mRNA-Binding Proteins Regulate the Distribution of Syntaxin mRNA in Aplysia Sensory Neurons.. J. Neurosci. 26: 5204-5214 [Abstract] [Full Text]
Anitei, M., Ifrim, M., Ewart, M.-A., Cowan, A. E., Carson, J. H., Bansal, R., Pfeiffer, S. E. (2006). A role for Sec8 in oligodendrocyte morphological differentiation. J. Cell Sci. 119: 807-818 [Abstract] [Full Text]
Iwahashi, C. K., Yasui, D. H., An, H.-J., Greco, C. M., Tassone, F., Nannen, K., Babineau, B., Lebrilla, C. B., Hagerman, R. J., Hagerman, P. J. (2006). Protein composition of the intranuclear inclusions of FXTAS. Brain 129: 256-271 [Abstract] [Full Text]
Shav-Tal, Y., Singer, R. H. (2005). RNA localization. J. Cell Sci. 118: 4077-4081 [Full Text]
Tretyakova, I., Zolotukhin, A. S., Tan, W., Bear, J., Propst, F., Ruthel, G., Felber, B. K. (2005). Nuclear Export Factor Family Protein Participates in Cytoplasmic mRNA Trafficking. J. Biol. Chem. 280: 31981-31990 [Abstract] [Full Text]
Cui, Z.-Q., Zhang, Z.-P., Zhang, X.-E., Wen, J.-K., Zhou, Y.-F., Xie, W.-H. (2005). Visualizing the dynamic behavior of poliovirus plus-strand RNA in living host cells. Nucleic Acids Res 33: 3245-3252 [Abstract] [Full Text]
Erck, C., Peris, L., Andrieux, A., Meissirel, C., Gruber, A. D., Vernet, M., Schweitzer, A., Saoudi, Y., Pointu, H., Bosc, C., Salin, P. A., Job, D., Wehland, J. (2005). A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc. Natl. Acad. Sci. USA 102: 7853-7858 [Abstract] [Full Text]
Liu, A., Stadelmann, C., Moscarello, M., Bruck, W., Sobel, A., Mastronardi, F. G., Casaccia-Bonnefil, P. (2005). Expression of Stathmin, a Developmentally Controlled Cytoskeleton-Regulating Molecule, in Demyelinating Disorders. J. Neurosci. 25: 737-747 [Abstract] [Full Text]
Wang, H., Tiedge, H. (2004). Translational Control at the Synapse. Neuroscientist 10: 456-466 [Abstract]
RYDER, S. P., WILLIAMSON, J. R. (2004). Specificity of the STAR/GSG domain protein Qk1: Implications for the regulation of myelination. RNA 10: 1449-1458 [Abstract] [Full Text]
Oostra, B. A., Willemsen, R. (2003). A fragile balance: FMR1 expression levels. Hum Mol Genet 12: R249-257 [Abstract] [Full Text]
Hamada, S., Ishiyama, K., Choi, S.-B., Wang, C., Singh, S., Kawai, N., Franceschi, V. R., Okita, T. W. (2003). The Transport of Prolamine RNAs to Prolamine Protein Bodies in Living Rice Endosperm Cells. Plant Cell 15: 2253-2264 [Abstract] [Full Text]
Tiruchinapalli, D. M., Oleynikov, Y., Kelic, S., Shenoy, S. M., Hartley, A., Stanton, P. K., Singer, R. H., Bassell, G. J. (2003). Activity-Dependent Trafficking and Dynamic Localization of Zipcode Binding Protein 1 and beta -Actin mRNA in Dendrites and Spines of Hippocampal Neurons. J. Neurosci. 23: 3251-3261 [Abstract] [Full Text]
Mallardo, M., Deitinghoff, A., Muller, J., Goetze, B., Macchi, P., Peters, C., Kiebler, M. A. (2003). From the Cover: Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. USA 100: 2100-2105 [Abstract] [Full Text]
Roegiers, F. (2003). Insights into mRNA transport in neurons. Proc. Natl. Acad. Sci. USA 100: 1465-1466 [Full Text]
De Diego Otero, Y., Severijnen, L.-A., van Cappellen, G., Schrier, M., Oostra, B., Willemsen, R. (2002). Transport of Fragile X Mental Retardation Protein via Granules in Neurites of PC12 Cells. Mol. Cell. Biol. 22: 8332-8341 [Abstract] [Full Text]
Nielsen, F. C., Nielsen, J., Kristensen, M. A., Koch, G., Christiansen, J. (2002). Cytoplasmic trafficking of IGF-II mRNA-binding protein by conserved KH domains. J. Cell Sci. 115: 2087-2097 [Abstract] [Full Text]
Ma, A. S. W., Moran-Jones, K., Shan, J., Munro, T. P., Snee, M. J., Hoek, K. S., Smith, R. (2002). Heterogeneous Nuclear Ribonucleoprotein A3, a Novel RNA Trafficking Response Element-binding Protein. J. Biol. Chem. 277: 18010-18020 [Abstract] [Full Text]
Kosik, K. S., Krichevsky, A. M. (2002). The Message and the Messenger: Delivering RNA in Neurons. Sci Signal 2002 : pe16-pe16 [Abstract] [Full Text]
Snee, M., Kidd, G. J., Munro, T. P., Smith, R. (2002). RNA trafficking and stabilization elements associate with multiple brain proteins. J. Cell Sci. 115: 4661-4669 [Abstract] [Full Text]
Aronov, S., Aranda, G., Behar, L., 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 [Abstract] [Full Text]
Mallardo, M., Schleich, S., Krijnse Locker, J. (2001). Microtubule-dependent Organization of Vaccinia Virus Core-derivd Early mRNAs into Distinct Cytoplasmic Structures. Mol. Biol. Cell 12: 3875-3891 [Abstract] [Full Text]
LEE, N. S., SUN, B., WILLIAMSON, R., GUNKEL, N., SALVATERRA, P. M., ROSSI, J. J. (2001). Functional colocalization of ribozymes and target mRNAs in Drosophila oocytes. FASEB J. 15: 2390-2400 [Abstract] [Full Text]
Aronov, S., Aranda, G., Behar, L., Ginzburg, I. (2001). Axonal Tau mRNA Localization Coincides with Tau Protein in Living Neuronal Cells and Depends on Axonal Targeting Signal. J. Neurosci. 21: 6577-6587 [Abstract] [Full Text]
Nakamura, A., Amikura, R., Hanyu, K., Kobayashi, S. (2001). Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128: 3233-3242 [Abstract] [Full Text]
Beach, D. L., Bloom, K. (2001). ASH1 mRNA Localization in Three Acts. Mol. Biol. Cell 12: 2567-2577 [Abstract] [Full Text]
Mouland, A. J., Xu, H., Cui, H., Krueger, W., Munro, T. P., Prasol, M., Mercier, J., Rekosh, D., Smith, R., Barbarese, E., Cohen, E. A., Carson, J. H. (2001). RNA Trafficking Signals in Human Immunodeficiency Virus Type 1. Mol. Cell. Biol. 21: 2133-2143 [Abstract] [Full Text]
Pederson, T. (2001). Fluorescent RNA cytochemistry: tracking gene transcripts in living cells. Nucleic Acids Res 29: 1013-1016 [Abstract] [Full Text]
Rook, M. S., Lu, M., Kosik, K. S. (2000). CaMKIIalpha 3' Untranslated Region-Directed mRNA Translocation in Living Neurons: Visualization by GFP Linkage. J. Neurosci. 20: 6385-6393 [Abstract] [Full Text]
Duchaîne, T., Wang, H.-J., Luo, M., Steinberg, S. V., Nabi, I. R., DesGroseillers, L. (2000). A Novel Murine Staufen Isoform Modulates the RNA Content of Staufen Complexes. Mol. Cell. Biol. 20: 5592-5601 [Abstract] [Full Text]
Righi, M., Tongiorgi, E., Cattaneo, A. (2000). Brain-Derived Neurotrophic Factor (BDNF) Induces Dendritic Targeting of BDNF and Tyrosine Kinase B mRNAs in Hippocampal Neurons through a Phosphatidylinositol-3 Kinase-Dependent Pathway. J. Neurosci. 20: 3165-3174 [Abstract] [Full Text]
Wilhelm, J. E., Mansfield, J., Hom-Booher, N., Wang, S., Turck, C. W., Hazelrigg, T., Vale, R. D. (2000). Isolation of a Ribonucleoprotein Complex Involved in mRNA Localization in Drosophila Oocytes. JCB 148: 427-440 [Abstract] [Full Text]
Mas, P., Beachy, R. N. (1999). Replication of Tobacco Mosaic Virus on Endoplasmic Reticulum and Role of the Cytoskeleton and Virus Movement Protein in Intracellular Distribution of Viral RNA. JCB 147: 945-958 [Abstract] [Full Text]
Munro, T. P., Magee, R. J., Kidd, G. J., Carson, J. H., Barbarese, E., Smith, L. M., Smith, R. (1999). Mutational Analysis of a Heterogeneous Nuclear Ribonucleoprotein A2 Response Element for RNA Trafficking. J. Biol. Chem. 274: 34389-34395 [Abstract] [Full Text]
Mathisen, P. M., Johnson, J. M., Kawczak, J. A., Tuohy, V. K. (1999). Visinin-like Protein (VILIP) Is a Neuron-specific Calcium-dependent Double-stranded RNA-binding Protein. J. Biol. Chem. 274: 31571-31576 [Abstract] [Full Text]
Kwon, S., Barbarese, E., Carson, J. H. (1999). The Cis-Acting RNA Trafficking Signal from Myelin Basic Protein mRNA and Its Cognate Trans-Acting Ligand Hnrnp A2 Enhance CaP-Dependent Translation. JCB 147: 247-256 [Abstract] [Full Text]
Blichenberg, A., Schwanke, B., Rehbein, M., Garner, C. C., Richter, D., Kindler, S. (1999). Identification of a cis-Acting Dendritic Targeting Element in MAP2 mRNAs. J. Neurosci. 19: 8818-8829 [Abstract] [Full Text]
Zhang, H.L., Singer, R.H., Bassell, G.J. (1999). Neurotrophin Regulation of {beta}-Actin mRNA and Protein Localization within Growth Cones. JCB 147: 59-70 [Abstract] [Full Text]
Köhrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C. G., Kiebler, M. A. (1999). 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 [Abstract] [Full Text]
Aranda-Abreu, G. E., Behar, L., Chung, S., Furneaux, H., Ginzburg, I. (1999). Embryonic Lethal Abnormal Vision-Like RNA-Binding Proteins Regulate Neurite Outgrowth and Tau Expression in PC12 Cells. J. Neurosci. 19: 6907-6917 [Abstract] [Full Text]
Marion, R. M., Fortes, P., Beloso, A., Dotti, C., Ortin, J. (1999). A Human Sequence Homologue of Staufen Is an RNA-Binding Protein That Is Associated with Polysomes and Localizes to the Rough Endoplasmic Reticulum. Mol. Cell. Biol. 19: 2212-2219 [Abstract] [Full Text]
Wickham, L., Duchaine, T., Luo, M., Nabi, I. R., 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 [Abstract] [Full Text]
BASSELL, G. J., OLEYNIKOV, Y., SINGER, R. H. (1999). The travels of mRNAs through all cells large and small. FASEB J. 13: 447-454 [Full Text]
JANSEN, R.-P. (1999). RNA�cytoskeletal associations. FASEB J. 13: 455-466 [Abstract] [Full Text]
Munchow, S, Sauter, C, Jansen, R. (1999). Association of the class V myosin Myo4p with a localised messenger RNA in budding yeast depends on She proteins. J. Cell Sci. 112: 1511-1518 [Abstract]
Punnonen, E.-L., Fages, C., Wartiovaara, J., Rauvala, H. (1999). Ultrastructural Localization of �-Actin and Amphoterin mRNA in Cultured Cells: Application of Tyramide Signal Amplification and Comparison of Detection Methods. J. Histochem. Cytochem. 47: 99-112 [Abstract] [Full Text]
Kiebler, M. A., Hemraj, I., Verkade, P., Kohrmann, M., Fortes, P., Marion, R. M., Ortin, J., 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 [Abstract] [Full Text]
DeFranco, C., Chicurel, M. E., Potter, H. (1998). A General RNA-Binding Protein Complex That Includes the Cytoskeleton-associated Protein MAP 1A. Mol. Biol. Cell 9: 1695-1708 [Abstract] [Full Text]
Muslimov, I. A., Banker, G., Brosius, J., Tiedge, H. (1998). Activity-dependent Regulation of Dendritic BC1 RNA in Hippocampal Neurons in Culture. JCB 141: 1601-1611 [Abstract] [Full Text]
Martin, R, Vaida, B, Bleher, R, Crispino, M, Giuditta, A (1998). Protein synthesizing units in presynaptic and postsynaptic domains of squid neurons. J. Cell Sci. 111: 3157-3166 [Abstract]
Fages, C, Kaksonen, M, Kinnunen, T, Punnonen, E., Rauvala, H (1998). Regulation of mRNA localization by transmembrane signalling: local interaction of HB-GAM (heparin-binding growth-associated molecule) with the cell surface localizes beta-actin mRNA. J. Cell Sci. 111: 3073-3080 [Abstract]
Iborra, F., Jackson, D., Cook, P. (1998). The path of transcripts from extra-nucleolar synthetic sites to nuclear pores: transcripts in transit are concentrated in discrete structures containing SR proteins. J. Cell Sci. 111: 2269-2282 [Abstract]
Wallace, C. S., Lyford, G. L., Worley, P. F., Steward, O. (1998). Differential Intracellular Sorting of Immediate Early Gene mRNAs Depends on Signals in the mRNA Sequence. J. Neurosci. 18: 26-35 [Abstract] [Full Text]
Antic, D, Keene, J. (1998). Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J. Cell Sci. 111: 183-197 [Abstract]
Knowles, R. B., Kosik, K. S. (1997). Neurotrophin-3 signals redistribute RNA in�neurons. Proc. Natl. Acad. Sci. USA 94: 14804-14808 [Abstract] [Full Text]
Tongiorgi, E., Righi, M., Cattaneo, A. (1997). Activity-Dependent Dendritic Targeting of BDNF and TrkB mRNAs in Hippocampal Neurons. J. Neurosci. 17: 9492-9505 [Abstract] [Full Text]
Ainger, K., Avossa, D., Diana, A. S., Barry, C., Barbarese, E., Carson, J. H. (1997). Transport and Localization Elements in Myelin Basic Protein mRNA. JCB 138: 1077-1087 [Abstract] [Full Text]
Lunn, K. F., Baas, P. W., Duncan, I. D. (1997). Microtubule Organization and Stability in the Oligodendrocyte. J. Neurosci. 17: 4921-4932 [Abstract] [Full Text]
Muslimov, I. A., Santi, E., Homel, P., Perini, S., Higgins, D., Tiedge, H. (1997). RNA Transport in Dendrites: A cis-Acting Targeting Element Is Contained within Neuronal BC1 RNA. J. Neurosci. 17: 4722-4733 [Abstract] [Full Text]
Deshler, J. O., Highett, M. I., Schnapp, B. J. (1997). Localization of Xenopus Vg1 mRNA by Vera Protein and the Endoplasmic Reticulum. Science 276: 1128-1131 [Abstract] [Full Text]
Kramer, E.-M., Koch, T., Niehaus, A., Trotter, J. (1997). Oligodendrocytes Direct Glycosyl Phosphatidylinositol-anchored Proteins to the Myelin Sheath in Glycosphingolipid-rich Complexes. J. Biol. Chem. 272: 8937-8945 [Abstract] [Full Text]
Racca, C., Gardiol, A., Triller, A. (1997). Dendritic and Postsynaptic Localizations of Glycine Receptor alpha �Subunit mRNAs. J. Neurosci. 17: 1691-1700 [Abstract] [Full Text]
Clark, I., Jan, L., Jan, Y. (1997). Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124: 461-470 [Abstract]
Knowles, R. B., Sabry, J. H., Martone, M. E., Deerinck, T. J., Ellisman, M. H., Bassell, G. J., Kosik, K. S. (1996). Translocation of RNA Granules in Living Neurons. J. Neurosci. 16: 7812-7820 [Abstract] [Full Text]
Hardy, R. J., Loushin, C. L., Friedrich Jr., V. L., Chen, Q., Ebersole, T. A., Lazzarini, R. A., Artzt, K. (1996). Neural Cell Type-Specific Expression of QKI Proteins Is Altered in quakingviable Mutant Mice. J. Neurosci. 16: 7941-7949 [Abstract] [Full Text]
Martone, M. E., Pollock, J. A., Jones, Y. Z., Ellisman, M. H. (1996). Ultrastructural Localization of Dendritic Messenger RNA in Adult Rat Hippocampus. J. Neurosci. 16: 7437-7446 [Abstract] [Full Text]
King, S. M., Barbarese, E., Dillman, J. F. III, Patel-King, R. S., Carson, J. H., Pfister, K. K. (1996). Brain Cytoplasmic and Flagellar Outer Arm Dyneins Share a Highly Conserved Mr 8,000Light Chain. J. Biol. Chem. 271: 19358-19366 [Abstract] [Full Text]
Veyrune, J., Campbell, G., Wiseman, J, Blanchard, J., Hesketh, J. (1996). A localisation signal in the 3' untranslated region of c-myc mRNA targets c-myc mRNA and beta-globin reporter sequences to the perinuclear cytoplasm and cytoskeletal-bound polysomes. J. Cell Sci. 109: 1185-1194 [Abstract]
Heinlein, M., Epel, B. L., Padgett, H. S., Beachy, R. N. (1995). Interaction of Tobamovirus Movement Proteins with the Plant Cytoskeleton. Science 270: 1983-1985 [Abstract]
Barbarese, E, Koppel, D., Deutscher, M., Smith, C., Ainger, K, Morgan, F, Carson, J. (1995). Protein translation components are colocalized in granules in oligodendrocytes. J. Cell Sci. 108: 2781-2790 [Abstract]
Esteban, M., Giovinazzo, G, Goday, C (1995). Chromatin diminution is strictly correlated to somatic cell behavior in early development of the nematode Parascaris univalens. J. Cell Sci. 108: 2393-2404 [Abstract]
Forristall, C, Pondel, M, Chen, L, King, M. (1995). Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development 121: 201-208 [Abstract]
Lane, M E, Kalderon, D (1994). RNA localization along the anteroposterior axis of the Drosophila oocyte requires PKA-mediated signal transduction to direct normal microtubule organization.. Genes Dev. 8: 2986-2995 [Abstract]
Webster, P., Suen, J, Macdonald, P. (1994). Drosophila virilis oskar transgenes direct body patterning but not pole cell formation or maintenance of mRNA localization in D. melanogaster. Development 120: 2027-2037 [Abstract]
Gu, W., Pan, F., Zhang, H., Bassell, G. J., Singer, R. H. (2002). A predominantly nuclear protein affecting cytoplasmic localization of {beta}-actin mRNA in fibroblasts and neurons. JCB 156: 41-52 [Abstract] [Full Text]