RNA trafficking in myelinating cells

Current Opinion in Neurobiology

Volumn 8, Issue 5, 1998, Pages 607-612

  Carson, John H ^a   Kwon, Sunjong ^a   Barbarese, Elisa ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; KINESIN; MESSENGER RNA; MYELIN; MYELIN BASIC PROTEIN;

MICROTUBULE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REVIEW; RNA TRANSLATION; RNA TRANSPORT;

EID: 0032191101     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(98)80088-3     Document Type: Article

References (44)

1. Colman DR, Kreibich G, Frey AB, Sabatini DD. Synthesis and incorporation of myelin polypeptides into CNS myelin. J Cell Biol. 95:1982;598-608.
2. Verity NA, Campagnoni AT. Regional expression of myelin protein genes in the developing mouse brain: in situ hybridization. J Neurosci Res. 21:1988;238-248.
3. Holmes E, Hermanson G, Cole R, de Vellis J. Developmental expression of glial-specification mRNAs in primary cultures of rat brain visualized by in situ hybridization. J Neurosci Res. 19:1988;389-396.
4. Brophy PJ, Boccaccio GL, Colman DR. The distribution of myelin basic protein mRNAs within myelinating oligodendrocytes. Trends Neurosci. 16:1993;515-521.
5. Holz A, Schaeren-Wiemers N, Schaefer C, Pott U, Colello RJ, Schwab E. Molecular and developmental characterization of novel cDNAs of the myelin-associated/oligodendrocytic basic protein. J Neurosci. 16:1996;467-477.
6. Ghandour MS, Skoff RP. Double-labeling in situ hybridization analysis of mRNAs for carbonic anhydrase II and myelin basic protein: expression in developing cultured glial cells. Glia. 4:1991;1-10.
7. Landry CF, Watson JB, Kashima T, Campagnoni AT. Cellular influences on RNA sorting in neurons and glia: an in situ hybridization histochemical study. Brain Res Mol Brain Res. 27:1994;1-11.
8. Amur-Umarjee S, Schonmann V, Campagnoni AT. Neuronal regulation of myelin basic protein mRNA translocation in oligodendrocytes is mediated by platelet-derived growth factor. Dev Neurosci. 19:1997;143-151.
9. Ainger K, Avossa D, Morgan F, Hill SJ, Barry C, Barbarese E, Carlson JH. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol. 123:1993;431-441.
10. Barbarese E, Koppel DE, Deutscher MP, Smith CL, Ainger K, Morgan F, Carson JH. Protein translation components are colocalized in granules in oligodendrocytes. J Cell Sci. 108:1995;2781-2790.
11. Sundell CL, Singer RH. Actin mRNA localizes in the absence of protein synthesis. J Cell Biol. 111:1990;2397-2403.
12. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS. Translocation of RNA granules in living neurons. J Neurosci. 16:1996;7812-7820.
13. Knowles RB, Kosik KS. Neurotrophin-3 signals redistribute RNA in neurons. Proc Natl Acad Sci USA. 94:1997;14804-14808.
14. Ferrandon D, Elphick L, Nüsslein-Volhard C, St Johnston D. Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell. 79:1994;1221-1232.
15. Kloc M, Etkin LD. Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development. 121:1995;289-297.
16. Forristall C, Pondell M, Chen L, King ML. Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development. 121:1995;201-208.
17. of outstanding interest Ainger K, Avossa D, Diana AS, Barry C, Barbarese E, Carson JH. Transport and localization elements in myelin basic protein mRNA. J Cell Biol. 138:1997;1077-1087 The authors identified two distinct cis-acting RNA trafficking signals in MBP mRNA: the RNA transport signal (RTS), a 21 nucleotide sequence that is necessary and sufficient to mediate transport along oligodendrocyte processes, and the RNA localization signal (RLS), which is necessary and sufficient for localization of RNA to the myelin compartment. This represents the first time distinct transport and localization elements have been resolved in a single RNA.
18. Kindler S, Müller R, Chung WJ, Garner CC. Molecular characterization of dendritically localized transcripts of MAP2. Brain Res Mol Brain Res. 36:1996;63-69.
19. Deshler JO, Highett MI, Schnapp BJ. Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science. 276:1997;1128-1131.
20. Deshler JO, Highett MI, Abramson T, Schnapp BJ. A highly conserved RNA binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol. 8:1998;489-496.
21. Havin L, Git A, Elisha Z, Oberman F, Yaniv K, Schwarz SP, Standart N, Yisraeli JK. RNA-binding protein conserved in both microtubule-and microfilament-based RNA localization. Genes Dev. 12:1998;1593-1598.
22. of outstanding interest Hoek K, Kidd GJ, Carson JH, Smith R. hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. Biochemistry. 37:1998;7021-7029 Identifies hnRNP A2 as the major trans-acting factor that binds to the RNA transport signal in MBP mRNA. This protein shuttles between the nucleus and cytoplasm, and it has previously been implicated in nuclear export of mRNA. This work suggests that hnRNP A2 has important cytoplasmic functions as well.
23. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 62:1993;289-321.
24. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G. A novel receptor-mediated nuclear import pathway. Cell. 86:1996;985-994.
25. Siomi H, Dreyfuss G. A nuclear localization domain in the hnRNP A1 protein. J Cell Biol. 129:1995;551-560.
26. Michael WM, Choi M, Dreyfuss G. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 83:1995;415-422.
27. Nakielny S, Siomi MC, Siomi H, Michael WM, Pollard V, Dreyfuss G. Transportin: nuclear transport receptor of a novel nuclear protein import pathway. Exp Cell Res. 229:1996;261-266.
28. Nakielny S, Dreyfuss G. Nuclear export of proteins and RNAs. Curr Opin Cell Biol. 9:1997;420-429.
29. Siomi MC, Eder PS, Kataoka N, Wan L, Liu Q, Dreyfuss G. Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J Cell Biol. 138:1997;1181-1192.
30. Nakielny S, Dreyfuss G. Import and export of the nuclear protein import receptor transportin by a mechanisms independent of GTP hydrolysis. Curr Biol. 8:1997;89-95.
31. Visa N, Alzhanova-Ericsson AT, Sun X, Kiseleva E, Bjorkroth B, Wurtz T, Daneholt B. A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell. 84:1996;253-264.
32. Izaurralde E, Jarmolowski A, Beisel C, Mattaj IW, Dreyfuss G, Fischer U. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J Cell Biol. 137:1997;27-35.
33. Jackson RJ, Wickens M. Translational controls impinging on the 5′-untranslated region and initiation factor proteins. Curr Opin Genet Dev. 7:1997;233-241.
34. Svitkin YV, Meerovitch K, Lee HS, Dholakia JN, Kenan DJ, Agol VI, Sonenberg N. Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. J Virol. 68:1994;1544-1550.
35. Sachs AB, Sarnow P, Hentze MW. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell. 89:1997;831-838.
36. of outstanding interest Carson JH, Worboys K, Ainger K, Barbarese E. Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin. Cell Motil Cytoskel. 38:1997;318-328 Identifies microtubules as the tracks for anterograde transport of MBP mRNA in oligodendrocytes, and kinesin as the molecular motor. Microbules have been implicated in translocation of other mRNAs, but this represents the first time kinesin has been implicated as a molecular motor for RNA movement.
37. Yisraeli JK, Sokol S, Melton DA. A two-step model for localization of mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development. 108:1990;289-298.
38. Pokrywka NJ, Stephenson EC. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development. 113:1991;55-66.
39. Glotzer JB, Saffrich R, Glotzer M, Ephrussi A. Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Curr Biol. 7:1997;326-337.
40. Bassel GJ, Singer RH, Kosik KS. Association of poly(A) mRNA with microtubules in cultured neurons. Neuron. 12:1994;571-582.
41. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci. 18:1998;251-265.
42. of special interest Lunn KF, Baas PW, Duncan ID. Microtubule organization and stability in the oligodendrocyte. J Neurosci. 17:1997;4921-4932 Demonstrates that microtuble polarity is predominantly plus-end distal in oligodendrocyte processes. This provides the ultrastructural basis for anterograde transport of RNA granules in oligodendrocytes. Electron micrographs showing microtubule discontinuities at branch points provide a plausible explanation for pausing and oscillation of RNA granules as they negotiate branch points.
43. Barry C, Pearson C, Barbarese E. Morphological organization of oligodendrocyte processes during development in culture and in vivo. Dev Neurosci. 18:1996;233-242.
44. King SM, Barbarese E, Dillman JF III, Patel-King RS, Carson JH, Pfister KK. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved M, 8,000 light chain. J Biol Chem. 271:1996;19358-19366.