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. 1997 Apr 15;25(8):1591–1596. doi: 10.1093/nar/25.8.1591

Intracellular localization and unique conserved sequences of three small nucleolar RNAs.

N Selvamurugan 1, O H Joost 1, E S Haas 1, J W Brown 1, N J Galvin 1, G L Eliceiri 1
PMCID: PMC146614  PMID: 9092667

Abstract

Three human small nucleolar RNAs (snoRNAs), E1, E2 and E3, were reported earlier that have unique sequences, interact directly with unique segments of pre-rRNA in vivo and are encoded in introns of protein genes. In the present report, human and frog E1, E2 and E3 RNAs injected into the cytoplasm of frog oocytes migrated to the nucleus and specifically to the nucleolus. This indicates that the nucleolar and nuclear localization signals of these snoRNAs reside within their evolutionarily conserved segments. Homologs of these snoRNAs from several vertebrates were sequenced and this information was used to develop RNA secondary structure models. These snoRNAs have unique phylogenetically conserved sequences.

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Selected References

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  1. Balakin A. G., Smith L., Fournier M. J. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell. 1996 Sep 6;86(5):823–834. doi: 10.1016/s0092-8674(00)80156-7. [DOI] [PubMed] [Google Scholar]
  2. Baserga S. J., Gilmore-Hebert M., Yang X. W. Distinct molecular signals for nuclear import of the nucleolar snRNA, U3. Genes Dev. 1992 Jun;6(6):1120–1130. doi: 10.1101/gad.6.6.1120. [DOI] [PubMed] [Google Scholar]
  3. Brown J. W. Phylogenetic comparative analysis of RNA structure on Macintosh computers. Comput Appl Biosci. 1991 Jul;7(3):391–393. doi: 10.1093/bioinformatics/7.3.391. [DOI] [PubMed] [Google Scholar]
  4. Cecconi F., Crosio C., Mariottini P., Cesareni G., Giorgi M., Brenner S., Amaldi F. A functional role for some Fugu introns larger than the typical short ones: the example of the gene coding for ribosomal protein S7 and snoRNA U17. Nucleic Acids Res. 1996 Aug 15;24(16):3167–3172. doi: 10.1093/nar/24.16.3167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cecconi F., Mariottini P., Loreni F., Pierandrei-Amaldi P., Campioni N., Amaldi F. U17XS8, a small nucleolar RNA with a 12 nt complementarity to 18S rRNA and coded by a sequence repeated in the six introns of Xenopus laevis ribosomal protein S8 gene. Nucleic Acids Res. 1994 Mar 11;22(5):732–741. doi: 10.1093/nar/22.5.732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  7. Fischer U., Darzynkiewicz E., Tahara S. M., Dathan N. A., Lührmann R., Mattaj I. W. Diversity in the signals required for nuclear accumulation of U snRNPs and variety in the pathways of nuclear transport. J Cell Biol. 1991 May;113(4):705–714. doi: 10.1083/jcb.113.4.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fischer U., Lührmann R. An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus. Science. 1990 Aug 17;249(4970):786–790. doi: 10.1126/science.2143847. [DOI] [PubMed] [Google Scholar]
  9. Fragapane P., Prislei S., Michienzi A., Caffarelli E., Bozzoni I. A novel small nucleolar RNA (U16) is encoded inside a ribosomal protein intron and originates by processing of the pre-mRNA. EMBO J. 1993 Jul;12(7):2921–2928. doi: 10.1002/j.1460-2075.1993.tb05954.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gall J. G., Tsvetkov A., Wu Z., Murphy C. Is the sphere organelle/coiled body a universal nuclear component? Dev Genet. 1995;16(1):25–35. doi: 10.1002/dvg.1020160107. [DOI] [PubMed] [Google Scholar]
  12. Hamm J., Darzynkiewicz E., Tahara S. M., Mattaj I. W. The trimethylguanosine cap structure of U1 snRNA is a component of a bipartite nuclear targeting signal. Cell. 1990 Aug 10;62(3):569–577. doi: 10.1016/0092-8674(90)90021-6. [DOI] [PubMed] [Google Scholar]
  13. Ishikawa Y., Safrany G., Hisatake K., Tanaka N., Maeda Y., Kato H., Kominami R., Muramatsu M. Structure of the core promoter of human and mouse ribosomal RNA gene. Asymmetry of species-specific transcription. J Mol Biol. 1991 Mar 5;218(1):55–67. doi: 10.1016/0022-2836(91)90873-5. [DOI] [PubMed] [Google Scholar]
  14. Izaurralde E., Mattaj I. W. Transport of RNA between nucleus and cytoplasm. Semin Cell Biol. 1992 Aug;3(4):279–288. doi: 10.1016/1043-4682(92)90029-u. [DOI] [PubMed] [Google Scholar]
  15. Jacobson M. R., Cao L. G., Wang Y. L., Pederson T. Dynamic localization of RNase MRP RNA in the nucleolus observed by fluorescent RNA cytochemistry in living cells. J Cell Biol. 1995 Dec;131(6 Pt 2):1649–1658. doi: 10.1083/jcb.131.6.1649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kiss T., Filipowicz W. Small nucleolar RNAs encoded by introns of the human cell cycle regulatory gene RCC1. EMBO J. 1993 Jul;12(7):2913–2920. doi: 10.1002/j.1460-2075.1993.tb05953.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krieg P. A., Melton D. A. In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987;155:397–415. doi: 10.1016/0076-6879(87)55027-3. [DOI] [PubMed] [Google Scholar]
  18. Lafontaine D., Tollervey D. Trans-acting factors in yeast pre-rRNA and pre-snoRNA processing. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):803–812. doi: 10.1139/o95-088. [DOI] [PubMed] [Google Scholar]
  19. Lund E., Paine P. L. Nonaqueous isolation of transcriptionally active nuclei from Xenopus oocytes. Methods Enzymol. 1990;181:36–43. doi: 10.1016/0076-6879(90)81110-g. [DOI] [PubMed] [Google Scholar]
  20. Maxwell E. S., Fournier M. J. The small nucleolar RNAs. Annu Rev Biochem. 1995;64:897–934. doi: 10.1146/annurev.bi.64.070195.004341. [DOI] [PubMed] [Google Scholar]
  21. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  22. Murray V. Improved double-stranded DNA sequencing using the linear polymerase chain reaction. Nucleic Acids Res. 1989 Nov 11;17(21):8889–8889. doi: 10.1093/nar/17.21.8889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nag M. K., Thai T. T., Ruff E. A., Selvamurugan N., Kunnimalaiyaan M., Eliceiri G. L. Genes for E1, E2, and E3 small nucleolar RNAs. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9001–9005. doi: 10.1073/pnas.90.19.9001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Brien C. A., Wolin S. L. A possible role for the 60-kD Ro autoantigen in a discard pathway for defective 5S rRNA precursors. Genes Dev. 1994 Dec 1;8(23):2891–2903. doi: 10.1101/gad.8.23.2891. [DOI] [PubMed] [Google Scholar]
  25. Peculis B. A., Steitz J. A. Sequence and structural elements critical for U8 snRNP function in Xenopus oocytes are evolutionarily conserved. Genes Dev. 1994 Sep 15;8(18):2241–2255. doi: 10.1101/gad.8.18.2241. [DOI] [PubMed] [Google Scholar]
  26. Rimoldi O. J., Raghu B., Nag M. K., Eliceiri G. L. Three new small nucleolar RNAs that are psoralen cross-linked in vivo to unique regions of pre-rRNA. Mol Cell Biol. 1993 Jul;13(7):4382–4390. doi: 10.1128/mcb.13.7.4382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ruff E. A., Rimoldi O. J., Raghu B., Eliceiri G. L. Three small nucleolar RNAs of unique nucleotide sequences. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):635–638. doi: 10.1073/pnas.90.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schmidt C., Lipsius E., Kruppa J. Nuclear and nucleolar targeting of human ribosomal protein S6. Mol Biol Cell. 1995 Dec;6(12):1875–1885. doi: 10.1091/mbc.6.12.1875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schnapp A., Rosenbauer H., Grummt I. Trans-acting factors involved in species-specificity and control of mouse ribosomal gene transcription. 1991 May 29-Jun 12Mol Cell Biochem. 104(1-2):137–147. doi: 10.1007/BF00229813. [DOI] [PubMed] [Google Scholar]
  30. Selvamurugan N., Eliceiri G. L. The gene for human E2 small nucleolar RNA resides in an intron of a laminin-binding protein gene. Genomics. 1995 Nov 20;30(2):400–401. [PubMed] [Google Scholar]
  31. Selvamurugan N., Nag M. K., Eliceiri G. L. Intron-encoded small nucleolar RNAs: new RNA sequence variants and genomic loci. Biochim Biophys Acta. 1995 Jan 25;1260(2):230–234. doi: 10.1016/0167-4781(94)00222-o. [DOI] [PubMed] [Google Scholar]
  32. Shaw P. J., Jordan E. G. The nucleolus. Annu Rev Cell Dev Biol. 1995;11:93–121. doi: 10.1146/annurev.cb.11.110195.000521. [DOI] [PubMed] [Google Scholar]
  33. Spector D. L. Macromolecular domains within the cell nucleus. Annu Rev Cell Biol. 1993;9:265–315. doi: 10.1146/annurev.cb.09.110193.001405. [DOI] [PubMed] [Google Scholar]
  34. Séraphin B. How many intronic snRNAs? Trends Biochem Sci. 1993 Sep;18(9):330–331. doi: 10.1016/0968-0004(93)90067-w. [DOI] [PubMed] [Google Scholar]
  35. Terns M. P., Dahlberg J. E. Retention and 5' cap trimethylation of U3 snRNA in the nucleus. Science. 1994 May 13;264(5161):959–961. doi: 10.1126/science.8178154. [DOI] [PubMed] [Google Scholar]
  36. Terns M. P., Grimm C., Lund E., Dahlberg J. E. A common maturation pathway for small nucleolar RNAs. EMBO J. 1995 Oct 2;14(19):4860–4871. doi: 10.1002/j.1460-2075.1995.tb00167.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watkins N. J., Leverette R. D., Xia L., Andrews M. T., Maxwell E. S. Elements essential for processing intronic U14 snoRNA are located at the termini of the mature snoRNA sequence and include conserved nucleotide boxes C and D. RNA. 1996 Feb;2(2):118–133. [PMC free article] [PubMed] [Google Scholar]
  38. Woese C. R., Gutell R., Gupta R., Noller H. F. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev. 1983 Dec;47(4):621–669. doi: 10.1128/mr.47.4.621-669.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. doi: 10.1126/science.2468181. [DOI] [PubMed] [Google Scholar]

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