An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNP: Protein-RNA contacts and base-pair interaction with the pre-ribosomal RNA

Journal of Molecular Biology

Volumn 273, Issue 3, 1997, Pages 552-571

  Méreau, Agnès ^a   Fournier, Régis ^a   Grégoire, Anne ^a   Mougin, Annie ^a   Fabrizio, Patrizia ^b   Lührmann, Reinhard ^b   Branlant, Christiane ^a  

^a Biopôle de l Université de Lorraine   (France)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Pre rRNA processing; RNA protein interaction; RNA secondary structure; S. cerevisiae; U3 snoRNP

Indexed keywords

DIMETHYL SULFATE; RIBOSOME RNA; RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; BASE PAIRING; CELL GROWTH; GENE MUTATION; GENETIC CONSERVATION; MODEL; MOLECULAR INTERACTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RNA PROCESSING; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION;

SACCHAROMYCES CEREVISIAE;

EID: 0031592930     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1320     Document Type: Article

References (57)

1. 2+. Prog. Nucl. Acid Res. Mol. Biol. 53:1996;79-129.
2. Ares M., Igel A. H. Lethal and temperature-sensitive mutations and their suppressors identify an essential structural element in U2 small nuclear RNA. Genes Dev. 4:1990;2132-2145.
3. Aris J. P., Blobel G. cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera. Proc. Natl Acad. Sci. USA. 88:1991;931-935.
4. Bachellerie J. P., Michot B., Nicoloso M., Balakin A., Ni J., Fournier M. J. Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA. Trends Biochem. Sci. 20:1995;261-264.
5. 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. 86:1996;823-834.
6. 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. 10:1991;2645-2651.
7. Baserga S. J., Gilmore-Hebert M., Yang X. W. Distinct molecular signals for nuclear import of the nucleolar snRNA, U3. Genes Dev. 6:1992;1120-1130.
8. Beltrame M., Tollervey D. Identification and functional analysis of two U3 binding sites on yeast pre- ribosomal RNA. EMBO J. 11:1992;1531-1542.
9. Beltrame M., Tollervey D. Base pairing between U3 and the pre-ribosomal RNA is required for 18 S rRNA synthesis. EMBO J. 14:1995;4350-4356.
10. Beltrame M., Henry Y., Tollervey D. Mutational analysis of an essential binding site for the U3 snoRNA in the 5′ external transcribed spacer of yeast pre-rRNA (corrected and republished inNucl. Acids Res.25. Nucl. Acids Res. 22:1994;4057-4065.
11. Brulé F., Venema J., Ségault V., Tollervey D., Branlant C. The yeastHansenula wingei. RNA. 2:1996;183-197.
12. Dennis P. P., Russell A. G., Moniz De Sa M. Formation of the 5′ end pseudoknot in small subunit ribosomal RNA: involvement of U3-like sequences. RNA. 3:1997;337-343.
13. Domdey H., Apostol B., Lin R. J., Newman A., Brody E., Abelson J. Lariat structures are in vivo intermediates in yeast pre-mRNA splicing. Cell. 39:1984;611-621.
14. Eichler D. C., Craig N. Processing of eukaryotic ribosomal RNA. Prog. Nucl. Acid Res. Mol. Biol. 49:1994;197-239.
15. Elela S. A., Igel H., Ares M. RNase III cleaves eukaryotic preribosomal RNA at a U3 snoRNP-dependent site. Cell. 85:1996;115-124.
16. Enright C. A., Maxwell E. S., Sollnerwebb B. 5′ETS rRNA processing facilitated by four small RNAs: U14, E3, U17, and U3. RNA. 2:1996;1094-1099.
17. Epstein P., Reddy R., Busch H. Multiple states of U3 RNA in Novikoff hepatoma nucleoli. Biochemistry. 23:1984;5421-5425.
18. Fabrizio P., Esser S., Kastner B., Luhrmann R. Isolation ofS. cerevisiae. Science. 1994;261-265.
19. Fournier M. J., Maxwell E. S. The nucleolar snRNAs: catching up with the spliceosomal snRNAs. Trends Biochem Sci. 18:1993;131-135.
20. Gutell R. R., Larsen N., Woese C. R. Lessons from an evolving rRNA: 16 S and 23 S rRNA structures from a comparative perspective. Microbiol. Rev. 58:1994;10-26.
21. Guthrie C., Patterson B. Spliceosomal snRNAs. Annu. Rev. Genet. 22:1988;387-419.
22. Hartshorne T., Agabian N. A common core structure for U3 small nucleolar RNAs. Nucl. Acids Res. 22:1994;3354-3364.
23. Hughes J. M., Ares M. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18 S ribosomal RNA. EMBO J. 10:1991;4231-4239.
24. Hughes J. M., Konings D. A., Cesareni G. The yeast homologue of U3 snRNA. EMBO J. 6:1987;2145-2155.
25. Hughes J. M. X. Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit. 1996.
26. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:1983;163-168.
27. Jansen R. P., Hurt E. C., Kern H., Lehtonen H., Carmo-Fonseca M., Lapeyre B., Tollervey D. Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J. Cell. Biol. 113:1991;715-729.
28. Jansen R., Tollervey D., Hurt E. C. A U3 snoRNP protein with homology to splicing factor PRP4 and G beta domains is required for ribosomal RNA processing. EMBO J. 12:1993;2549-2558.
29. Jarmolowski A., Zagorski J., Li H. V., Fournier M. J. Identification of essential elements in U14 RNA ofSaccharomyces cerevisiae. EMBO J. 9:1990;4503-4509.
30. Jeppesen C., Stebbins-Boaz B., Gerbi S. A. Nucleotide sequence determination and secondary structure ofXenopus. Nucl. Acids Res. 16:1988;2127-2148.
31. Kass S., Tyc K., Steitz J. A., Sollner-Webb B. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell. 60:1990;897-908.
32. Kramer B., Kramer W., Fritz H. J. Different base/base mismatches are corrected with different efficiencies by the methyl-directed DNA mismatch-repair system ofE. coli. Cell. 38:1984;879-887.
33. Lapeyre B., Mariottini P., Mathieu C., Ferrer P., Amaldi F., Amalric F., Caizergues-Ferrer M. Molecular cloning ofXenopus. Mol. Cell. Biol. 10:1990;430-434.
34. Lübben B., Marshallsay C., Rottmann N., Lührmann R. Isolation of U3 snoRNP from CHO cells: a novel 55 kDa protein binds to the central part of U3 snoRNA. Nucl. Acids Res. 21:1993;5377-5385.
35. Maser R. L., Calvet J. P. U3 small nuclear RNA can be psoralen-cross-linked in vivo to the 5′ external transcribed spacer of pre-ribosomal-RNA. Proc. Natl Acad. Sci. USA. 86:1989;6523-6527.
36. Mougey E. B., Pape L. K., Sollner-Webb B. A U3 small nuclear ribonucleoprotein-requiring processing event in the 5′ external transcribed spacer ofXenopus. Mol. Cell. Biol. 13:1993;5990-5998.
37. Mougin A., Grégoire A., Banroques J., Ségault V., Fournier R., Brulé F., Chevrier-Miller M., Branlant C. Secondary structure of the yeastSaccharomyces cerevisiae. RNA. 2:1996;1079-1093.
38. Myslinski E., Ségault V., Branlant C. An intron in the genes for U3 small nucleolar RNAs of the yeastSaccharomyces cerevisiae. Science. 247:1990;1213-1216.
39. Parker K. A., Steitz J. A. Structural analysis of the human U3 ribonucleoprotein particle reveal a conserved sequence available for base pairing with pre-rRNA. Mol. Cell. Biol. 7:1987;2899-2913.
40. Raué H. A., Planta R. J. The pathway to maturity: Processing of ribosomal RNA inSaccharomyces cerevisiae. Gene Expr. 5:1995;71-77.
41. Reddy R., Henning D., Busch H. Substitutions, insertions, and deletions in two highly conserved U3 RNA species. J. Biol. Chem. 255:1980;7029-7033.
42. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
43. 3. EMBO J. 9:1990;2299-2308.
44. 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. 8:1989;4015-4024.
45. Ségault V., Mougin A., Grégoire A., Banroques J., Branlant C. An experimental study ofSaccharomyces cerevisiae. Nucl. Acids Res. 20:1992;3443-3451.
46. Shannon K. W., Guthrie C. Suppressors of a U4 snRNA mutation define a novel U6 snRNP protein with RNA- binding motifs. Genes Dev. 5:1991;773-785.
47. Stotz A., Linder P. The ADE2 gene fromSaccharomyces cerevisiae. Gene. 95:1990;91-98.
48. Stroke I. L., Weiner A. M. Genes and pseudogenes from rat U3A and U3B small nuclear RNA. J. Mol. Biol. 184:1985;183-193.
49. Stroke I. L., Weiner A. M. The 5′ end of U3 snRNA can be crosslinkedin vivo. J. Mol. Biol. 210:1989;497-512.
50. Suh D., Busch H., Reddy R. Isolation and characterization of a human U3 small nucleolar RNA gene. Biochem. Biophys. Res. Commun. 137:1986;1133-1140.
51. Terns M. P., Grimm C., Lund E., Dahlberg J. E. A common maturation pathway for small nucleolar RNAs. EMBO J. 14:1995;4860-4871.
52. Tiollais P., Galibert F., Boiron M. Evidence for the existence of several molecular species in the "45S fraction" of mammalian ribosomal precursor RNA. Proc. Natl Acad. Sci. USA. 68:1971;1117-1120.
53. 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. 10:1991;573-583.
54. Tyc K., Steitz J. A. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 8:1989;3113-3119.
55. Tyc K., Steitz J. A. A new interaction between the mouse 5′ external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucl. Acids Res. 20:1992;5375-5382.
56. Tycowski K. T., Shu M. D., Steitz J. A. A small nucleolar RNA is processed from an intron of the human gene encoding ribosomal protein S3. Genes Dev. 7:1993;1176-1190.
57. Udem S. A., Warner J. R. Ribosomal RNA synthesis inSaccharomyces cerevisiae. J. Mol. Biol. 65:1972;227-242.