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. 1995 Oct 16;14(20):5109–5114. doi: 10.1002/j.1460-2075.1995.tb00193.x

Vg1 RNA binding protein mediates the association of Vg1 RNA with microtubules in Xenopus oocytes.

Z Elisha 1, L Havin 1, I Ringel 1, J K Yisraeli 1
PMCID: PMC394614  PMID: 7588639

Abstract

Localized RNAs are found in a variety of somatic and developing cell types. In many cases, microtubules have been implicated as playing a role in facilitating transport of these RNAs. Here we report that Vg1 RNA, which is localized to the vegetal cortex of Xenopus laevis oocytes, is associated with microtubules in vivo. Because of the ubiquitous nature of tubulin, the association of specific RNAs with microtubules is likely to involve factors that recognize both RNA and microtubules. Vg1 RNA binding protein (Vg1 RBP), previously shown to bind with high affinity to the vegetal localization site in Vg1 RNA, appears to function in this capacity. Vg1 RBP is associated with microtubules: it is enriched in microtubule extracts of oocytes and is also co-precipitated by heterologous, polymerized tubulin. Furthermore, Vg1 RBP binding activity is required for the specific association of Vg1 RNA to microtubules in vitro. These data suggest a general model for how specific RNAs can be localized to particular sites via common cytoskeletal elements.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ainger K., Avossa D., Morgan F., Hill S. J., Barry C., Barbarese E., Carson J. H. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol. 1993 Oct;123(2):431–441. doi: 10.1083/jcb.123.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bassell G. J., Singer R. H., Kosik K. S. Association of poly(A) mRNA with microtubules in cultured neurons. Neuron. 1994 Mar;12(3):571–582. doi: 10.1016/0896-6273(94)90213-5. [DOI] [PubMed] [Google Scholar]
  3. Clark I., Giniger E., Ruohola-Baker H., Jan L. Y., Jan Y. N. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr Biol. 1994 Apr 1;4(4):289–300. doi: 10.1016/s0960-9822(00)00068-3. [DOI] [PubMed] [Google Scholar]
  4. Darnbrough C. H., Ford P. J. Identification in Xenopus laevis of a class of oocyte-specific proteins bound to messenger RNA. Eur J Biochem. 1981 Jan;113(3):415–424. doi: 10.1111/j.1432-1033.1981.tb05081.x. [DOI] [PubMed] [Google Scholar]
  5. DeSimone D. W., Norton P. A., Hynes R. O. Identification and characterization of alternatively spliced fibronectin mRNAs expressed in early Xenopus embryos. Dev Biol. 1992 Feb;149(2):357–369. doi: 10.1016/0012-1606(92)90291-n. [DOI] [PubMed] [Google Scholar]
  6. Ding D., Lipshitz H. D. Localized RNAs and their functions. Bioessays. 1993 Oct;15(10):651–658. doi: 10.1002/bies.950151004. [DOI] [PubMed] [Google Scholar]
  7. Durso N. A., Cyr R. J. A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1 alpha. Plant Cell. 1994 Jun;6(6):893–905. doi: 10.1105/tpc.6.6.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Edson K., Weisshaar B., Matus A. Actin depolymerisation induces process formation on MAP2-transfected non-neuronal cells. Development. 1993 Feb;117(2):689–700. doi: 10.1242/dev.117.2.689. [DOI] [PubMed] [Google Scholar]
  9. Elinson R. P. Changes in levels of polymeric tubulin associated with activation and dorsoventral polarization of the frog egg. Dev Biol. 1985 May;109(1):224–233. doi: 10.1016/0012-1606(85)90362-8. [DOI] [PubMed] [Google Scholar]
  10. Gard D. L. Gamma-tubulin is asymmetrically distributed in the cortex of Xenopus oocytes. Dev Biol. 1994 Jan;161(1):131–140. doi: 10.1006/dbio.1994.1015. [DOI] [PubMed] [Google Scholar]
  11. Gard D. L. Organization, nucleation, and acetylation of microtubules in Xenopus laevis oocytes: a study by confocal immunofluorescence microscopy. Dev Biol. 1991 Feb;143(2):346–362. doi: 10.1016/0012-1606(91)90085-h. [DOI] [PubMed] [Google Scholar]
  12. Garner C. C., Tucker R. P., Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature. 1988 Dec 15;336(6200):674–677. doi: 10.1038/336674a0. [DOI] [PubMed] [Google Scholar]
  13. Hirokawa N. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr Opin Cell Biol. 1994 Feb;6(1):74–81. doi: 10.1016/0955-0674(94)90119-8. [DOI] [PubMed] [Google Scholar]
  14. Matus A. Microtubule-associated proteins and neuronal morphogenesis. J Cell Sci Suppl. 1991;15:61–67. doi: 10.1242/jcs.1991.supplement_15.9. [DOI] [PubMed] [Google Scholar]
  15. Melton D. A. Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature. 1987 Jul 2;328(6125):80–82. doi: 10.1038/328080a0. [DOI] [PubMed] [Google Scholar]
  16. Mowry K. L., Melton D. A. Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. Science. 1992 Feb 21;255(5047):991–994. doi: 10.1126/science.1546297. [DOI] [PubMed] [Google Scholar]
  17. Murray M. T., Schiller D. L., Franke W. W. Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):11–15. doi: 10.1073/pnas.89.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Oberman F., Yisraeli J. K. Two protocols for nonradioactive in situ hybridization to Xenopus oocytes. Trends Genet. 1995 Mar;11(3):83–84. doi: 10.1016/s0168-9525(00)89006-x. [DOI] [PubMed] [Google Scholar]
  19. Pokrywka N. J., Stephenson E. C. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development. 1991 Sep;113(1):55–66. doi: 10.1242/dev.113.1.55. [DOI] [PubMed] [Google Scholar]
  20. Pondel M. D., King M. L. Localized maternal mRNA related to transforming growth factor beta mRNA is concentrated in a cytokeratin-enriched fraction from Xenopus oocytes. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7612–7616. doi: 10.1073/pnas.85.20.7612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rebagliati M. R., Weeks D. L., Harvey R. P., Melton D. A. Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell. 1985 Oct;42(3):769–777. doi: 10.1016/0092-8674(85)90273-9. [DOI] [PubMed] [Google Scholar]
  22. Schwartz S. P., Aisenthal L., Elisha Z., Oberman F., Yisraeli J. K. A 69-kDa RNA-binding protein from Xenopus oocytes recognizes a common motif in two vegetally localized maternal mRNAs. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11895–11899. doi: 10.1073/pnas.89.24.11895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sloboda R. D., Rosenbaum J. L. Purification and assay of microtubule-associated proteins (MAPs). Methods Enzymol. 1982;85(Pt B):409–416. doi: 10.1016/0076-6879(82)85041-6. [DOI] [PubMed] [Google Scholar]
  24. Theurkauf W. E., Alberts B. M., Jan Y. N., Jongens T. A. A central role for microtubules in the differentiation of Drosophila oocytes. Development. 1993 Aug;118(4):1169–1180. doi: 10.1242/dev.118.4.1169. [DOI] [PubMed] [Google Scholar]
  25. Theurkauf W. E., Smiley S., Wong M. L., Alberts B. M. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development. 1992 Aug;115(4):923–936. doi: 10.1242/dev.115.4.923. [DOI] [PubMed] [Google Scholar]
  26. Tonissen K. F., Krieg P. A. Analysis of a variant Max sequence expressed in Xenopus laevis. Oncogene. 1994 Jan;9(1):33–38. [PubMed] [Google Scholar]
  27. Vallee R. B., Collins C. A. Purification of microtubules and microtubule-associated proteins from sea urchin eggs and cultured mammalian cells using taxol, and use of exogenous taxol-stabilized brain microtubules for purifying microtubule-associated proteins. Methods Enzymol. 1986;134:116–127. doi: 10.1016/0076-6879(86)34080-1. [DOI] [PubMed] [Google Scholar]
  28. Vallee R. B. Purification of brain microtubules and microtubule-associated protein 1 using taxol. Methods Enzymol. 1986;134:104–115. doi: 10.1016/0076-6879(86)34079-5. [DOI] [PubMed] [Google Scholar]
  29. Vallee R. B. Reversible assembly purification of microtubules without assembly-promoting agents and further purification of tubulin, microtubule-associated proteins, and MAP fragments. Methods Enzymol. 1986;134:89–104. doi: 10.1016/0076-6879(86)34078-3. [DOI] [PubMed] [Google Scholar]
  30. Wang S., Hazelrigg T. Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature. 1994 Jun 2;369(6479):400–403. doi: 10.1038/369400a0. [DOI] [PubMed] [Google Scholar]
  31. Weeks D. L., Melton D. A. A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-beta. Cell. 1987 Dec 4;51(5):861–867. doi: 10.1016/0092-8674(87)90109-7. [DOI] [PubMed] [Google Scholar]
  32. Wilhelm J. E., Vale R. D. RNA on the move: the mRNA localization pathway. J Cell Biol. 1993 Oct;123(2):269–274. doi: 10.1083/jcb.123.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wolffe A. P., Tafuri S., Ranjan M., Familari M. The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol. 1992 Apr;4(4):290–298. [PubMed] [Google Scholar]
  34. Yisraeli J. K., Melton D. A. The material mRNA Vg1 is correctly localized following injection into Xenopus oocytes. Nature. 1988 Dec 8;336(6199):592–595. doi: 10.1038/336592a0. [DOI] [PubMed] [Google Scholar]
  35. Yisraeli J. K., Sokol S., Melton D. A. A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development. 1990 Feb;108(2):289–298. doi: 10.1242/dev.108.2.289. [DOI] [PubMed] [Google Scholar]

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