Skip to main content
NCBI home page
RNA logoLink to RNA
. 1996 Mar;2(3):264–273.

The interactions with Ro60 and La differentially affect nuclear export of hY1 RNA.

F H Simons 1, S A Rutjes 1, W J van Venrooij 1, G J Pruijn 1
PMCID: PMC1369369  PMID: 8608450

Abstract

Ro RNPs are evolutionarily conserved ribonucleoprotein particles that consist of a small RNA, known as Y RNA, associated with several proteins, such as La, Ro60, and Ro52. The Y RNAs (Y1-Y5), which are transcribed by RNA polymerase III, have been shown to reside almost exclusively in the cytoplasm as Ro RNPs. To obtain more insight into the nuclear export pathway of Y RNAs, hY1 RNA export was studied in Xenopus laevis oocytes. Injection of various hY1 RNA mutants showed that an intact Ro60 binding site is a prerequisite for nuclear export, whereas the presence of an intact La binding site resulted in strong nuclear retention of hY1 RNA. Competition studies with various classes of RNAs indicated that, in addition to Ro60, another titratable factor was necessary for nuclear export of hY1 RNA. This factor appears also to be involved in nuclear export of tRNA. Because export of hY1 RNA could not be blocked by a synthetic peptide containing the recently identified nuclear export signal of the HIV-1 Rev protein, nuclear export of hY1 RNA does not seem to be dependent on a Rev-like nuclear export signal.

Full Text

The Full Text of this article is available as a PDF (4.1 MB).

Selected References

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

  1. Boelens W. C., Palacios I., Mattaj I. W. Nuclear retention of RNA as a mechanism for localization. RNA. 1995 May;1(3):273–283. [PMC free article] [PubMed] [Google Scholar]
  2. Boire G., Craft J. Human Ro ribonucleoprotein particles: characterization of native structure and stable association with the La polypeptide. J Clin Invest. 1990 Apr;85(4):1182–1190. doi: 10.1172/JCI114551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chow C. S., Hartmann K. M., Rawlings S. L., Huber P. W., Barton J. K. Delineation of structural domains in eukaryotic 5S rRNA with a rhodium probe. Biochemistry. 1992 Apr 7;31(13):3534–3542. doi: 10.1021/bi00128a030. [DOI] [PubMed] [Google Scholar]
  4. Eckner R., Ellmeier W., Birnstiel M. L. Mature mRNA 3' end formation stimulates RNA export from the nucleus. EMBO J. 1991 Nov;10(11):3513–3522. doi: 10.1002/j.1460-2075.1991.tb04915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Farris A. D., O'Brien C. A., Harley J. B. Y3 is the most conserved small RNA component of Ro ribonucleoprotein complexes in vertebrate species. Gene. 1995 Mar 10;154(2):193–198. doi: 10.1016/0378-1119(94)00823-b. [DOI] [PubMed] [Google Scholar]
  6. Fischer U., Huber J., Boelens W. C., Mattaj I. W., Lührmann R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell. 1995 Aug 11;82(3):475–483. doi: 10.1016/0092-8674(95)90436-0. [DOI] [PubMed] [Google Scholar]
  7. Fischer U., Meyer S., Teufel M., Heckel C., Lührmann R., Rautmann G. Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J. 1994 Sep 1;13(17):4105–4112. doi: 10.1002/j.1460-2075.1994.tb06728.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gerace L. Nuclear export signals and the fast track to the cytoplasm. Cell. 1995 Aug 11;82(3):341–344. doi: 10.1016/0092-8674(95)90420-4. [DOI] [PubMed] [Google Scholar]
  9. Guddat U., Bakken A. H., Pieler T. Protein-mediated nuclear export of RNA: 5S rRNA containing small RNPs in xenopus oocytes. Cell. 1990 Feb 23;60(4):619–628. doi: 10.1016/0092-8674(90)90665-2. [DOI] [PubMed] [Google Scholar]
  10. Hamm J., Kazmaier M., Mattaj I. W. In vitro assembly of U1 snRNPs. EMBO J. 1987 Nov;6(11):3479–3485. doi: 10.1002/j.1460-2075.1987.tb02672.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamm J., Mattaj I. W. An abundant U6 snRNP found in germ cells and embryos of Xenopus laevis. EMBO J. 1989 Dec 20;8(13):4179–4187. doi: 10.1002/j.1460-2075.1989.tb08603.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hamm J., Mattaj I. W. Monomethylated cap structures facilitate RNA export from the nucleus. Cell. 1990 Oct 5;63(1):109–118. doi: 10.1016/0092-8674(90)90292-m. [DOI] [PubMed] [Google Scholar]
  13. He X. P., Bataillé N., Fried H. M. Nuclear export of signal recognition particle RNA is a facilitated process that involves the Alu sequence domain. J Cell Sci. 1994 Apr;107(Pt 4):903–912. doi: 10.1242/jcs.107.4.903. [DOI] [PubMed] [Google Scholar]
  14. Hendrick J. P., Wolin S. L., Rinke J., Lerner M. R., Steitz J. A. Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol. 1981 Dec;1(12):1138–1149. doi: 10.1128/mcb.1.12.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Izaurralde E., Lewis J., McGuigan C., Jankowska M., Darzynkiewicz E., Mattaj I. W. A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell. 1994 Aug 26;78(4):657–668. doi: 10.1016/0092-8674(94)90530-4. [DOI] [PubMed] [Google Scholar]
  16. Izaurralde E., Mattaj I. W. RNA export. Cell. 1995 Apr 21;81(2):153–159. doi: 10.1016/0092-8674(95)90323-2. [DOI] [PubMed] [Google Scholar]
  17. Jarmolowski A., Boelens W. C., Izaurralde E., Mattaj I. W. Nuclear export of different classes of RNA is mediated by specific factors. J Cell Biol. 1994 Mar;124(5):627–635. doi: 10.1083/jcb.124.5.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mathews M. B., Francoeur A. M. La antigen recognizes and binds to the 3'-oligouridylate tail of a small RNA. Mol Cell Biol. 1984 Jun;4(6):1134–1140. doi: 10.1128/mcb.4.6.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. O'Brien C. A., Margelot K., Wolin S. L. Xenopus Ro ribonucleoproteins: members of an evolutionarily conserved class of cytoplasmic ribonucleoproteins. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7250–7254. doi: 10.1073/pnas.90.15.7250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peek R., Pruijn G. J., van der Kemp A. J., van Venrooij W. J. Subcellular distribution of Ro ribonucleoprotein complexes and their constituents. J Cell Sci. 1993 Nov;106(Pt 3):929–935. doi: 10.1242/jcs.106.3.929. [DOI] [PubMed] [Google Scholar]
  21. Piñol-Roma S., Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 1992 Feb 20;355(6362):730–732. doi: 10.1038/355730a0. [DOI] [PubMed] [Google Scholar]
  22. Piñol-Roma S., Dreyfuss G. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science. 1991 Jul 19;253(5017):312–314. doi: 10.1126/science.1857966. [DOI] [PubMed] [Google Scholar]
  23. Piñol-Roma S., Dreyfuss G. hnRNP proteins: localization and transport between the nucleus and the cytoplasm. Trends Cell Biol. 1993 May;3(5):151–155. doi: 10.1016/0962-8924(93)90135-n. [DOI] [PubMed] [Google Scholar]
  24. Pruijn G. J., Slobbe R. L., van Venrooij W. J. Analysis of protein--RNA interactions within Ro ribonucleoprotein complexes. Nucleic Acids Res. 1991 Oct 11;19(19):5173–5180. doi: 10.1093/nar/19.19.5173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pruijn G. J., Thijssen J. P., Smith P. R., Williams D. G., Van Venrooij W. J. Anti-La monoclonal antibodies recognizing epitopes within the RNA-binding domain of the La protein show differential capacities to immunoprecipitate RNA-associated La protein. Eur J Biochem. 1995 Sep 1;232(2):611–619. doi: 10.1111/j.1432-1033.1995.611zz.x. [DOI] [PubMed] [Google Scholar]
  26. Pruijn G. J., Wingens P. A., Peters S. L., Thijssen J. P., van Venrooij W. J. Ro RNP associated Y RNAs are highly conserved among mammals. Biochim Biophys Acta. 1993 Dec 14;1216(3):395–401. doi: 10.1016/0167-4781(93)90006-y. [DOI] [PubMed] [Google Scholar]
  27. Simons F. H., Pruijn G. J., van Venrooij W. J. Analysis of the intracellular localization and assembly of Ro ribonucleoprotein particles by microinjection into Xenopus laevis oocytes. J Cell Biol. 1994 Jun;125(5):981–988. doi: 10.1083/jcb.125.5.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Slobbe R. L., Pluk W., van Venrooij W. J., Pruijn G. J. Ro ribonucleoprotein assembly in vitro. Identification of RNA-protein and protein-protein interactions. J Mol Biol. 1992 Sep 20;227(2):361–366. doi: 10.1016/0022-2836(92)90890-v. [DOI] [PubMed] [Google Scholar]
  29. Stefano J. E. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3' termini of RNA polymerase III transcripts. Cell. 1984 Jan;36(1):145–154. doi: 10.1016/0092-8674(84)90083-7. [DOI] [PubMed] [Google Scholar]
  30. Tobian J. A., Drinkard L., Zasloff M. tRNA nuclear transport: defining the critical regions of human tRNAimet by point mutagenesis. Cell. 1985 Dec;43(2 Pt 1):415–422. doi: 10.1016/0092-8674(85)90171-0. [DOI] [PubMed] [Google Scholar]
  31. Van Horn D. J., Eisenberg D., O'Brien C. A., Wolin S. L. Caenorhabditis elegans embryos contain only one major species of Ro RNP. RNA. 1995 May;1(3):293–303. [PMC free article] [PubMed] [Google Scholar]
  32. Veldhoven C. H., Pruijn G. J., Meilof J. F., Thijssen J. P., Van der Kemp A. W., Van Venrooij W. J., Smeenk R. J. Characterization of murine monoclonal antibodies against 60-kD Ro/SS-A and La/SS-B autoantigens. Clin Exp Immunol. 1995 Jul;101(1):45–54. doi: 10.1111/j.1365-2249.1995.tb02275.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wolin S. L., Steitz J. A. Genes for two small cytoplasmic Ro RNAs are adjacent and appear to be single-copy in the human genome. Cell. 1983 Mar;32(3):735–744. doi: 10.1016/0092-8674(83)90059-4. [DOI] [PubMed] [Google Scholar]
  34. Wolin S. L., Steitz J. A. The Ro small cytoplasmic ribonucleoproteins: identification of the antigenic protein and its binding site on the Ro RNAs. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1996–2000. doi: 10.1073/pnas.81.7.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zasloff M. tRNA transport from the nucleus in a eukaryotic cell: carrier-mediated translocation process. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6436–6440. doi: 10.1073/pnas.80.21.6436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. van Venrooij W. J., Slobbe R. L., Pruijn G. J. Structure and function of La and Ro RNPs. Mol Biol Rep. 1993 Aug;18(2):113–119. doi: 10.1007/BF00986765. [DOI] [PubMed] [Google Scholar]

Articles from RNA are provided here courtesy of The RNA Society

RESOURCES