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. 2000 Jan;6(1):88–95. doi: 10.1017/s1355838200991623

Fibrillarin binds directly and specifically to U16 box C/D snoRNA.

A Fatica 1, S Galardi 1, F Altieri 1, I Bozzoni 1
PMCID: PMC1369896  PMID: 10668801

Abstract

Eukaryotic nucleoli contain a large family of box C/D small nucleolar ribonucleoprotein complexes (snoRNPs) that are involved in processing and site-specific methylation of pre-rRNA. Several proteins have been reported to be common factors of box C/D snoRNPs in lower and higher eukaryotes; nevertheless none of them has been clearly shown to directly interact with RNA. We previously identified in Xenopus laevis, by means of UV crosslinking in vivo, two proteins associated with box C/D snoRNAs, fibrillarin and p68. Here we show that fibrillarin interacts directly and specifically with the U16 box C/D snoRNA in a X. laevis oocyte nuclear extract and that it does not require p68 for binding. Specific binding is also obtained with a recombinant fibrillarin demonstrating that the protein is able to bind directly and specifically to U16 snoRNA by itself.

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Selected References

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  1. Bagni C., Lapeyre B. Gar1p binds to the small nucleolar RNAs snR10 and snR30 in vitro through a nontypical RNA binding element. J Biol Chem. 1998 May 1;273(18):10868–10873. doi: 10.1074/jbc.273.18.10868. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Baserga S. J., Yang X. D., Steitz J. A. An intact Box C sequence in the U3 snRNA is required for binding of fibrillarin, the protein common to the major family of nucleolar snRNPs. EMBO J. 1991 Sep;10(9):2645–2651. doi: 10.1002/j.1460-2075.1991.tb07807.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bortolin M. L., Ganot P., Kiss T. Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs. EMBO J. 1999 Jan 15;18(2):457–469. doi: 10.1093/emboj/18.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caffarelli E., Arese M., Santoro B., Fragapane P., Bozzoni I. In vitro study of processing of the intron-encoded U16 small nucleolar RNA in Xenopus laevis. Mol Cell Biol. 1994 May;14(5):2966–2974. doi: 10.1128/mcb.14.5.2966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caffarelli E., Fatica A., Prislei S., De Gregorio E., Fragapane P., Bozzoni I. Processing of the intron-encoded U16 and U18 snoRNAs: the conserved C and D boxes control both the processing reaction and the stability of the mature snoRNA. EMBO J. 1996 Mar 1;15(5):1121–1131. [PMC free article] [PubMed] [Google Scholar]
  7. Caffarelli E., Losito M., Giorgi C., Fatica A., Bozzoni I. In vivo identification of nuclear factors interacting with the conserved elements of box C/D small nucleolar RNAs. Mol Cell Biol. 1998 Feb;18(2):1023–1028. doi: 10.1128/mcb.18.2.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cavaillé J., Nicoloso M., Bachellerie J. P. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature. 1996 Oct 24;383(6602):732–735. doi: 10.1038/383732a0. [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. Ganot P., Bortolin M. L., Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell. 1997 May 30;89(5):799–809. doi: 10.1016/s0092-8674(00)80263-9. [DOI] [PubMed] [Google Scholar]
  11. Ganot P., Caizergues-Ferrer M., Kiss T. The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. Genes Dev. 1997 Apr 1;11(7):941–956. doi: 10.1101/gad.11.7.941. [DOI] [PubMed] [Google Scholar]
  12. Gary J. D., Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol. 1998;61:65–131. doi: 10.1016/s0079-6603(08)60825-9. [DOI] [PubMed] [Google Scholar]
  13. Gautier T., Bergès T., Tollervey D., Hurt E. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol Cell Biol. 1997 Dec;17(12):7088–7098. doi: 10.1128/mcb.17.12.7088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Girard J. P., Lehtonen H., Caizergues-Ferrer M., Amalric F., Tollervey D., Lapeyre B. GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast. EMBO J. 1992 Feb;11(2):673–682. doi: 10.1002/j.1460-2075.1992.tb05099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henras A., Henry Y., Bousquet-Antonelli C., Noaillac-Depeyre J., Gélugne J. P., Caizergues-Ferrer M. Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J. 1998 Dec 1;17(23):7078–7090. doi: 10.1093/emboj/17.23.7078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jiang W., Middleton K., Yoon H. J., Fouquet C., Carbon J. An essential yeast protein, CBF5p, binds in vitro to centromeres and microtubules. Mol Cell Biol. 1993 Aug;13(8):4884–4893. doi: 10.1128/mcb.13.8.4884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kenan D. J., Query C. C., Keene J. D. RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci. 1991 Jun;16(6):214–220. doi: 10.1016/0968-0004(91)90088-d. [DOI] [PubMed] [Google Scholar]
  18. Kiss-László Z., Henry Y., Bachellerie J. P., Caizergues-Ferrer M., Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell. 1996 Jun 28;85(7):1077–1088. doi: 10.1016/s0092-8674(00)81308-2. [DOI] [PubMed] [Google Scholar]
  19. Kiss-László Z., Henry Y., Kiss T. Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J. 1998 Feb 2;17(3):797–807. doi: 10.1093/emboj/17.3.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lafontaine D. L., Bousquet-Antonelli C., Henry Y., Caizergues-Ferrer M., Tollervey D. The box H + ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase. Genes Dev. 1998 Feb 15;12(4):527–537. doi: 10.1101/gad.12.4.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lafontaine D. L., Tollervey D. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem Sci. 1998 Oct;23(10):383–388. doi: 10.1016/s0968-0004(98)01260-2. [DOI] [PubMed] [Google Scholar]
  22. Lafontaine D. L., Tollervey D. Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability. RNA. 1999 Mar;5(3):455–467. doi: 10.1017/s135583829998192x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lapeyre B., Mariottini P., Mathieu C., Ferrer P., Amaldi F., Amalric F., Caizergues-Ferrer M. Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease. Mol Cell Biol. 1990 Jan;10(1):430–434. doi: 10.1128/mcb.10.1.430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lischwe M. A., Ochs R. L., Reddy R., Cook R. G., Yeoman L. C., Tan E. M., Reichlin M., Busch H. Purification and partial characterization of a nucleolar scleroderma antigen (Mr = 34,000; pI, 8.5) rich in NG,NG-dimethylarginine. J Biol Chem. 1985 Nov 15;260(26):14304–14310. [PubMed] [Google Scholar]
  25. 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]
  26. Meier U. T., Blobel G. NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria. J Cell Biol. 1994 Dec;127(6 Pt 1):1505–1514. doi: 10.1083/jcb.127.6.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Min H., Chan R. C., Black D. L. The generally expressed hnRNP F is involved in a neural-specific pre-mRNA splicing event. Genes Dev. 1995 Nov 1;9(21):2659–2671. doi: 10.1101/gad.9.21.2659. [DOI] [PubMed] [Google Scholar]
  28. Ni J., Tien A. L., Fournier M. J. Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell. 1997 May 16;89(4):565–573. doi: 10.1016/s0092-8674(00)80238-x. [DOI] [PubMed] [Google Scholar]
  29. Nicoloso M., Qu L. H., Michot B., Bachellerie J. P. Intron-encoded, antisense small nucleolar RNAs: the characterization of nine novel species points to their direct role as guides for the 2'-O-ribose methylation of rRNAs. J Mol Biol. 1996 Jul 12;260(2):178–195. doi: 10.1006/jmbi.1996.0391. [DOI] [PubMed] [Google Scholar]
  30. Niewmierzycka A., Clarke S. S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae. Identification of a novel protein arginine methyltransferase. J Biol Chem. 1999 Jan 8;274(2):814–824. doi: 10.1074/jbc.274.2.814. [DOI] [PubMed] [Google Scholar]
  31. Schimmang T., Tollervey D., Kern H., Frank R., Hurt E. C. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 1989 Dec 20;8(13):4015–4024. doi: 10.1002/j.1460-2075.1989.tb08584.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith C. M., Steitz J. A. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell. 1997 May 30;89(5):669–672. doi: 10.1016/s0092-8674(00)80247-0. [DOI] [PubMed] [Google Scholar]
  33. Tollervey D., Kiss T. Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol. 1997 Jun;9(3):337–342. doi: 10.1016/s0955-0674(97)80005-1. [DOI] [PubMed] [Google Scholar]
  34. Tollervey D., Lehtonen H., Carmo-Fonseca M., Hurt E. C. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 1991 Mar;10(3):573–583. doi: 10.1002/j.1460-2075.1991.tb07984.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tyc K., Steitz J. A. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 1989 Oct;8(10):3113–3119. doi: 10.1002/j.1460-2075.1989.tb08463.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Watkins N. J., Gottschalk A., Neubauer G., Kastner B., Fabrizio P., Mann M., Lührmann R. Cbf5p, a potential pseudouridine synthase, and Nhp2p, a putative RNA-binding protein, are present together with Gar1p in all H BOX/ACA-motif snoRNPs and constitute a common bipartite structure. RNA. 1998 Dec;4(12):1549–1568. doi: 10.1017/s1355838298980761. [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. Watkins N. J., Newman D. R., Kuhn J. F., Maxwell E. S. In vitro assembly of the mouse U14 snoRNP core complex and identification of a 65-kDa box C/D-binding protein. RNA. 1998 May;4(5):582–593. doi: 10.1017/s1355838298980128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wu P., Brockenbrough J. S., Metcalfe A. C., Chen S., Aris J. P. Nop5p is a small nucleolar ribonucleoprotein component required for pre-18 S rRNA processing in yeast. J Biol Chem. 1998 Jun 26;273(26):16453–16463. doi: 10.1074/jbc.273.26.16453. [DOI] [PMC free article] [PubMed] [Google Scholar]

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