Processing of mammalian rRNA precursors at the 3' end of 18S rRNA - Identification of cis-acting signals suggests the involvement of U13 small nucleolar RNA

European Journal of Biochemistry

Volumn 242, Issue 2, 1996, Pages 206-213

  Cavaillé, Jérôme ^a   Hadjiolov, Asen A ^a   Bachellerie, Jean Pierre ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

18S rRNA; Mammals; RRNA processing; U13 small nucleolar RNA; U20 small nucleolar RNA

Indexed keywords

RIBOSOME RNA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FIBROBLAST; IN VITRO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; SITE DIRECTED MUTAGENESIS;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0029806013     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0206r.x     Document Type: Article

References (51)

1. Eichler, D. C. & Craig, N. (1994) Processing of eukaryotic ribosomal RNA, Prog. Nucleic Acid Res. Mol. Biol. 49, 197-239.
2. Hadjiolov, A. A. (1985) The nucleolus and ribosome biogenesis, p. 268, Springer, Wien/New York.
3. Maden, B. E. H. (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA, Prog. Nucleic Acid Res. Mol. Biol. 39, 241-303.
4. Sollner-Webb, B., Tycowski, K. T. & Sleitz, J. A. (1996) Ribosomal RNA processing in eukaryotes, Ribosomal RNA: structure, evolution, gene expression and function in protein synthesis (Zimmerman, R. A. & Dahlberg, A. E., eds) pp. 469-490, CRC Press, Boca Raton.
5. Warner, J. R. (1989) Synthesis of ribosomes in Saccharomyces cerevisiae, Microbiol. Rev. 53, 256-271.
6. Craig, N., Kass, S. & Sollner-Webb, B. (1987) Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA, Proc. Natl Acad. Sci. USA 84, 629-633.
7. Craig, N., Kass, S. & Sollner-Webb, B. (1991) Sequence organisation and RNA structural motifs directing the mouse primary rRNA processing event, Mol. Cell. Biol. 11, 458-467.
8. Kass, S., Craig, N. & Sollner-Webb, B. (1987) Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific, Mol. Cell. Biol. 7, 2891-2898.
9. Mougey, E. B., Pape, L. K. & Sollner-Webb, B. (1993) A U3 small nucleolar ribonucleoprotein-requiring processing event in the 5′ external transcribed spacer of Xenopus precursor rRNA, Mol. Cell. Biol. 13, 5990-5998.
10. Raué, H. A. & Planta, R. J. (1995) The pathway to maturity: processing of ribosomal RNA in Saccharomyces cerevisiae, Gene Expression 5, 71-77.
11. Van Nues, R. W., Venema, J., Rientjes, J. M. J., Dirks-Mulder, A. & Raué, H. A. (1995) Processing of eukaryotic pre-rRNA: The role of the transcribed spacers, Biochem. Cell Biol. 73, 789-801.
12. Venema, J. & Tollervey, D. (1995) Processing of pre-ribosomal RNA in Saccharomyces cerevisiae, Yeast 11, 1629-1650.
13. Vance, V. B., Thompson, E. A. & Bowman, L. H. (1985) Transfection of mouse ribosomal DNA into rat cells: faithful transcription and processing, Nucleic Acids Res. 13, 7499-7513.
14. Raziuddin, Little, R. D., Labella, T. & Schlessinger, D. (1989) Transcription and processing of RNA from mouse ribosomal DNA transfected into hamster cells, Mol. Cell. Biol. 10, 3868-3872.
15. Bowman, L. H., Rabin, B. & Schlessinger, D. (1981) Multiple ribosomal RNA cleavage pathways in mammalian cells, Nucleic Acids Res. 9, 4951-4966.
16. Hadjiolova, K. V., Nicoloso, M., Mazan, S., Hadjiolov, A. A. & Bachellerie, J. P. (1993) Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis, Eur. J. Biochem. 212, 211-215.
17. Todorov, I. T. & Hadjiolov, A. A. (1981) A precursor to the small ribosome in nucleoli of Friend erythroleukemia cells, Cell Biol. Intern. Rep. 5, 711-716.
18. Trapman, J. & Planta, R. J. (1976) Maturation of ribosomal ribonucleic acid in yeast. Kinetic analysis of labeling of high-molecular mass rRNA species, Biochim. Biophys. Acta 442, 265-274.
19. Udem, S. A. & Warner, J. R. (1973) The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast, J. Biol. Chem. 248, 1412-1416.
20. Hadjiolova, K. V., Normann, A., Cavaillé, J., Soupène, E., Mazan, S., Hadjiolov, A. A. & Bachellerie, J. P. (1994) Processing of truncated mouse or human rRNA transcribed from ribosomal minigenes transfected into mouse cells, Mol. Cell. Biol. 14, 4044-4056.
21. Michot, B., Bachellerie, J. P. & Raynal, F. (1983) Structure of mouse rRNA precursors. Complete sequence and potential folding of the spacer regions between 18S and 28S rRNA, Nucleic Acids Res. 11, 3375-3391.
22. Nicoloso, M., Caizergues-Ferrer, M., Michot, B., Azum, M. C. & Bachellerie, J. P. (1994) U20, a novel small nucleolar RNA, is encoded in an intron of the nucleolin gene of mammals, Mol. Cell. Biol. 14, 5766-5776.
23. Bachellerie, J. P., Michot, B., Nicoloso, M., Balakin, A., Ni, J. & Fournier, M. J. (1995) Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA, Trends Biochem. Sci. 20, 261-264.
24. Tyc, K. & Steitz, J. A. (1989) U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus, EMBO J. 8, 3113-3119.
25. Maxwell, E. S. & Fournier, M. J. (1995) The small nucleolar RNAs, Annu. Rev. Biochem. 35, 897-934.
26. Bachellerie, J. P., Qu, L. H., Nicoloso, M., Michot, B., Caizergues-Ferrer, M., Cavaillé, J. & Renalier, M. H. (1995) Novel intron-encoded small nucleolar RNAs with long sequence complementarities to mature rRNAs involved in ribosome biogenesis, Biochem. Cell Biol. 73, 835-843.
27. Steitz, J. A. & Tycowski, K. T. (1995) Small RNA chaperones for ribosome biogenesis, Science 270, 1626-1627.
28. Hadjiolova, K. V., Hadjiolov, A. A. & Bachellerie, J. P. (1995) Actinomycin D stimulates the transcription of rRNA minigenes transfected into mouse cells. Implications for the in vivo hypersensitivity of rRNA gene transcription, Eur. J. Biochem. 228, 605-615.
29. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
30. McCallum, F. S. & Maden, B. E. H. (1985) Human ribosomal RNA sequence inferred from DNA sequence, Biochem. J. 232, 725-733.
31. Gonzales, I. L., Sylvester, J. E., Smith, T. F., Stambolian, D. & Schmickel, R. D. (1990) Ribosomal RNA gene sequences and hominoid phylogeny, Mol. Biol. Evol. 7, 203-217.
32. Kunkel, T. A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection, Proc. Natl Acad. Sci. USA 82, 488-492.
33. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem. 162, 156-159.
34. Van Nues, R. W., Rientjes, J. M. J., van der Sande, C. A. F. M., Zerp, S. F., Sluiter, C., Venema, J., Planta, R. J. & Raué, H. A. (1994) Separate structural elements within internal transcribed spacer 1 of Saccharomyces cerevisiae precursor ribosomal RNA direct the formation of 17S and 26S rRNA, Nucleic Acids Res. 22, 912-919.
35. Shumard, C. M., Torres, C. & Eichler, D. C. (1990) In vitro processing at the 3′-terminal region of pre-18S rRNA by a nucleolar endoribonuclease, Mol. Cell. Biol. 10, 3868-3872.
36. Hannon, G. J., Maroney, P. A., Branch, A., Benenfield, B. J., Robertson, H. D. & Nilsen, T. W. (1989) Accurate processing of human pre-rRNA in vitro, Mol. Cell. Biol. 9, 4422-4431.
37. Yu, Y. T. & Nilsen, T. W. (1992) Sequence requirements for maturation of the 5′-terminus of human 18S rRNA in vitro, J. Biol. Chem. 267, 9264-9268.
38. Bowman, L. H., Goldman, W. E., Goldberg, G. I., Herbert, M. B. & Schlessinger, D. (1983) Location of initial cleavage sites in mouse pre-rRNA, Mol. Cell. Biol. 3, 1501-1510.
39. Henry, Y., Wood, H., Morrissey, J. P., Petfalski, E., Kearsey, S. & Tollervey, D. (1994) The 5′-end of yeast 5.8 S rRNA is generated by exonucleases from an upstream cleavage site, EMBO J. 13, 2452-2463.
40. Stevens, A., Hsu, C. L., Isham, K. R. & Larimer, F. W. (1991) Fragments of the internal transcribed spacer 1 of pre-rRNA accumulate in Saccharomyces cerevisiae lacking 5′→3′ exoribonuclease I, J. Bact. 173, 7024-7028.
41. Georgiev, O. I., Nosikov, V. V., Braga, E. A. & Hadjiolov, A. A. (1984) Sequence heterogeneity in the internal transcribed spacers of two rat ribosomal DNA clones, Biochem. Internat. 8, 225-229.
42. Venema, J., Henry, Y. & Tollervey, D. (1995) Two distinct recognition signals define the site of endonucleolytic cleavage at the 5′-end of yeast 18S rRNA, EMBO J. 14, 4883-4892.
43. Raué, H. A., Klootwijk, J. & Musters, W. (1988) Evolutionary conservation of structure and function of high molecular weight ribosomal RNA, Progress Biophys. Mol. Biol. 51, 77-129.
44. Nicoloso, M., Qu, L. H., Michot, B. & Bachellerie, J. P. (1996) 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. 260, 178-195.
45. Kiss-Laszlo, Z., Henry, Y., Bachellerie, J. P., Caizergues-Ferrer, M. & Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs, Cell 85, 1077-1088.
46. Caboche, M. & Bachellerie, J. P. (1977) RNA methylation and control of eukaryotic RNA biosynthesis. Effects of cycloleucine, a specific inhibitor of methylation, on ribosomal RNA maturation, Eur. J. Biochem. 74, 19-29.
47. Tollervey, D. H., Lehtonen, H., Jansen, R., Kern, H. & Hurt, E. C. (1993) Temperature sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation and ribosome assembly, Cell 72, 443-457.
48. 6A residues in E. coli 16S ribosomal RNA. Effects on ribosome function and activity of the ksgA methyltransferase, Biochim. Biophys. Acta 1050, 18-26.
49. Zimmerman, R. A. (1996) The decoding domain, Ribosomal RNA: structure, evolution, gene expression and function in protein synthesis (Zimmerman, R. A. & Dahlberg, R. A., eds) pp. 277-309. CRC Press, Boca Raton.
50. Lafontaine, D., Vandenhaute, J. & Tollervey, D. (1995) The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast, Genes & Dev. 9, 2470-2481.
51. Mitchell, P., Petfalski, E. & Tollervey, D. (1996) The 3′ end of yeast 5.8S rRNA is generated by an exonuclease processing mechanism, Genes & Dev. 10, 502-513.