Assembly of 5S ribosomal RNA is required at a specific step of the pre- rRNA processing pathway

Journal of Cell Biology

Volumn 145, Issue 7, 1999, Pages 1369-1380

  Dechampesme, Anne Marie ^a   Koroleva, Olga ^a   Leger Silvestre, Isabelle ^b   Gas, Nicole ^b   Camier, Sylvie ^a,c  

^a DIF   (France)

^b CNRS   (France)

^c NONE   (United States)

Author keywords

5S ribosomal RNA; Cell nucleolus; Pre rRNA; Ribosomes; Yeasts

Indexed keywords

MUTANT PROTEIN; PROTEIN SUBUNIT; RIBOSOME RNA;

ARTICLE; ELECTRON MICROSCOPY; FUNGUS GROWTH; GENE MUTATION; GENE OVEREXPRESSION; GROWTH RATE; MUTAGENESIS; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RNA ANALYSIS; YEAST;

CELL NUCLEOLUS; CELL NUCLEUS; CYTOPLASM; FUNGAL PROTEINS; GENE EXPRESSION; GENES, FUNGAL; KINETICS; MOLECULAR WEIGHT; MUTATION; NUCLEIC ACID CONFORMATION; RIBOSOMAL PROTEINS; RIBOSOMES; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 5S; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

FUNGI;

EID: 0033612556     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.7.1369     Document Type: Article

References (51)

1. Allison, L.A., M.T. North, and L.A. Neville. 1995. Differential binding of oocyte-type and somatic-type 5S rRNA to TFIIIA and ribosomal protein L5 in Xenopus oocytes: specialization for storage versus mobilization. Dev. Biol. 168:284-295.
2. Archambault, J., C.A. Milne, K.T. Schappert, B. Baum, J.D. Friesen, and J. Segall. 1992. The deduced sequence of the transcription factor TFIIIA from Saccharomyces cerevisiae reveals extensive divergence from Xenopus TFIIIA. J. Biol. Chem. 267:3282-3288.
3. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1987. Current Protocols in Molecular Biology. Vols. 1 and 2. G.P.A. Wiley-Interscience, New York. 1.0.1-16.21.9.
4. Baim, S.B., D.F. Pietras, D.C. Eustice, and F. Sherman. 1985. A mutation allowing an mRNA secondary structure diminishes translation of Saccharomyces cerevisiae iso-1-cytochrome c. Mol. Cell. Biol. 5:1839-1846.
5. Blobel, G. 1971. Isolation of a 5S RNA-protein complex from mammalian ribosomes. Proc. Natl. Acad. Sci. USA. 68:1881-1885.
6. Bogdanov, A.A., O.A. Dontsova, S.S. Dokudovskaya, and I.N. Lavrik. 1995. Structure and function of 5S rRNA in the ribosome. Biochem. Cell Biol. 73: 869-876.
7. Camier, S., A.M. Dechampesme, and A. Sentenac. 1995. The only essential function of TFIIIA in yeast is the transcription of 5S rRNA genes. Proc. Natl. Acad. Sci. USA. 92:9338-9342.
8. de la Cruz, J., D. Kressler, M. Rojo, D. Tollervey, and P. Linder. 1998a. Spb4p, an essential putative RNA helicase, is required for a late step in the assembly of 60S ribosomal subunits in Saccharomyces cerevisiae. RNA. 4:1268-1281.
9. de la Cruz, J., D. Kressler, D. Tollervey, and P. Linder. 1998b. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO (Eur. Mol. Biol. Organ.) J. 17:1128-1140.
10. Deshmukh, M., Y.-F. Tsay, A.G. Paulovich, and J.L.J. Woolford. 1993. Yeast ribosomal protein L1 is required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol. Cell. Biol. 13:2835-2845.
11. Dohme, F., and K.H. Nierhaus. 1976. Role of 5S RNA in assembly and function of the 50S subunit from Escherichia coli. Proc. Natl. Acad. Sci. USA. 73: 2221-2225.
12. Donis-Keller, H., A.M. Maxam, and W. Gilbert. 1977. Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res. 4:2527-2538.
13. Dontsova, O., V. Tishkov, S. Dokudovskaya, A. Bogdanov, T. Doring, J. Rinke-Appel, S. Thamm, B. Greuer, and R. Brimacombe. 1994. Stem-loop IV of 5S rRNA lies close to the peptidyltransferase center. Proc Natl. Acad. Sci. USA. 91:4125-4129.
14. England, T.E., A.G. Bruce, and O.C. Uhlenbeck. 1980. Specific labeling of 3′ termini of RNA with T4 RNA ligase. Methods Enzymol. 65:65-74.
15. Gautier, T., T. Berges, D. Tollervey, and E. Hurt. 1997. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Noplp and are required for ribosome biogenesis. Mol. Cell. Biol. 17:7088-7098.
16. Guddat, U., A.H. Bakken, and T. Pieler. 1990. Protein-mediated nuclear export of RNA: 5S rRNA containing small RNPs in Xenopus oocytes. Cell. 60:619-628.
17. Hadjiolov, A.A. 1985. The Nucleolus and Ribosome Biogenesis. Springer-Verlag New York Inc., New York. 268 pp.
18. Higuchi, R., B. Krummel, and R.K. Saiki. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:7351-7367.
19. Hong, B., J.S. Brockenbrough, P. Wu, and J.P. Aris. 1997. Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol. Cell. Biol. 17:378-388.
20. Jacquet, M.A., R. Ehrlich, and C. Reiss. 1989. In vivo gene expression directed by synthetic promoter constructions restricted to the -10 and -35 consensus hexamers of E. coli. Nucleic Acids Res. 17:2933-2945.
21. Kadowaki, T., S. Chen, M. Hitomi, E. Jacobs, C. Kumagai, S. Liang, R. Schneiter, D. Singleton, J. Wisniewska, and A.M. Tartakoff. 1994. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants [published erratum appears in J. Cell Biol. 1994. 126: 1627]. J. Cell Biol. 126:649-659.
22. Leger-Silvestre, I., J. Noaillac-Depeyre, M. Faubladier, and N. Gas. 1997. Structural and functional analysis of the nucleolus of the fission yeast Schizosaccharomyces pombe. Eur. J. Cell. Biol. 72:13-23.
23. LinMarq, N., and S.G. Clarkson. 1998. Efficient synthesis, termination, and release of RNA polymerase III transcripts in Xenopus extracts depleted of La protein. EMBO (Eur. Mol. Biol. Organ.) J. 17:2033-2041.
24. Matsumoto, Y., R. Fishel, and R.B. Wickner. 1990. Circular single-stranded RNA replicon in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 87: 7628-7632.
25. Michael, W.M., and G. Dreyfuss. 1996. Distinct domains in ribosomal protein L5 mediate 5 S rRNA binding and nucleolar localization. J. Biol. Chem. 271: 11571-11574.
26. Moore, P.B. 1996. The structure and function of 5S ribosomal RNA. In Ribosomal RNA: Structure, Evolution, Processing and Function in Protein Biosynthesis. R. A. Zimmermann and A.E. Dahlberg, editors. CRC Press, Boca Raton, FL. 199-236.
27. Moritz, M., B.A. Pulaski, and J.L. Woolford, Jr. 1991. Assembly of 60S ribosomal subunits is perturbed in temperature-sensitive yeast mutants defective in ribosomal protein L16. Mol. Cell. Biol. 11:5681-5692.
28. Nazar, R.N., M. Yaguchi, G.E. Willick, C.F. Rollin, and C. Roy. 1979. The 5S RNA binding protein from yeast (Saccharomyces cerevisiae) ribosomes. Evolution of the eukaryotic 5S RNA binding protein. Eur. J. Biochem. 102: 573-582.
29. Picard, B., and M. Wegnez. 1979. Isolation of a 7S particle from Xenopus laevis oocytes: a 5S RNA-protein complex. Proc. Natl. Acad. Sci. USA. 76:241-245.
30. Picard, B., M. le Maire, M. Wegnez, and H. Denis. 1980. Biochemical research on oogenesis. Composition of the 42-S storage particles of Xenopus laevis oocytes. Eur. J. Biochem. 109:359-368.
31. Ripmaster, T.L., G.P. Vaughn, and J.L. Woolford, Jr. 1992. A putative ATP-dependent RNA helicase involved in Saccharomyces cerevisiae ribosome assembly. Proc. Natl. Acad. Sci. USA. 89:11131-11135.
32. Rodriguez-Cousino, N., L.M. Esteban, and R. Esteban. 1991. Molecular cloning and characterization of W double-stranded RNA, a linear molecule present in Saccharomyces cerevisiae. Identification of its single-stranded RNA form as 20 S RNA. J. Biol. Chem. 266:12772-12778.
33. Rudt, F., and T. Pieler. 1996. Cytoplasmic retention and nuclear import of 5S ribosomal RNA containing RNPs. EMBO (Eur. Mol. Biol. Organ.) J. 15: 1383-1391.
34. Schmitt, M.E., T.A. Brown, and B.L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18:3091-3092.
35. Sergiev, P., S. Dokudovskaya, E. Romanova, A. Topin, A. Bogdanov, R. Brimacombe, and O. Dontsova. 1998. The environment of 5S rRNA in the ribosome: cross-links to the GTPase-associated area of 23S rRNA. Nucleic Acids Res. 26:2519-2525.
36. Shaw, P.J., and E.G. Jordan. 1995. The nucleolus. Annu. Rev. Cell. Dev. Biol. 11:93-121.
37. Stefano, J.E. 1984. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell. 36:145-154.
38. Steitz, J.-A., C. Berg, J.P. Hendrick, H. La Branche-Chabot, A. Metspalu, J. Rinke, and T. Yario. 1988. A 5S rRNA/L5 complex is a precursor to ribosome assembly in mammalian cells. J. Cell Biol. 106:545-556.
39. Trapman, J., R.J. Planta, and H.A. Raue. 1976. Maturation of ribosomes in yeast. II. Position of the low molecular weight rRNA species in the maturation process. Biochim. Biophys. Acta. 442:275-284.
40. Van Ryk, D.I., Y. Lee, and R.N. Nazar. 1992. Unbalanced ribosome assembly in Saccharomyces cerevisiae expressing mutant 5 S rRNAs. J. Biol. Chem. 267:16177-16181.
41. Venema, J., and D. Tollervey. 1995. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast. 11:1629-1650.
42. Vilardell, J., and J.R. Warner. 1997. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Mol. Cell. Biol. 17:1959-1965.
43. Warner, J.R. 1989. Synthesis of ribosomes in Saccharomyces cerevisiae. Microbiol Rev. 53:256-271.
44. Warner, J.R., and R. Soeiro. 1967. Nascent ribosomes from HeLa cells. Proc. Natl. Acad. Sci. USA. 58:1984-1990.
45. Wejksnora, P.J., and J.E. Haber. 1978. Ribonucleoprotein particle appearing during sporulation in yeast. J. Bacteriol. 134:246-260.
46. Woolford, J.L., and J.R. Warner. 1991. The ribosome and its synthesis. In The Molecular and Cellular Biology of the yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics. J.R. Broach, J.R. Pringle, and E.W. Jones, editors. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 1:587-626.
47. Yeh, L.C., and J.C. Lee. 1995a. Contributions of multiple basic amino acids in the C-terminal region of yeast ribosomal protein L1 to 5 S rRNA binding and 60 S ribosome stability. J. Mol. Biol. 246:295-307.
48. Yeh, L.C., and J.C. Lee. 1995b. Involvement of multiple basic amino acids in yeast ribosomal protein L1 in 5S rRNA recognition. Nucleic Acids Symp. Ser. 33:63-65.
49. Yeh, L.C., M. Deshmukh, J.L. Woolford, and J.C. Lee. 1996. Involvement of lysine 270 and lysine 271 of yeast 5S rRNA binding protein in RNA binding and ribosome assembly. Biochim. Biophys. Acta. 1308:133-141.
50. Yoo, C.J., and S.L. Wolin. 1994. La proteins from Drosophila melanogaster and Saccharomyces cerevisiae: a yeast homolog of the La autoantigen is dispensable for growth. Mol. Cell. Biol. 14:5412-5424.
51. Zanchin, N.I.T., P. Roberts, A. De Silva, F. Sherman, and D.S. Goldfarb. 1997. Saccharomyces cerevisiae Nip7p is required for efficient 60S ribosome subunit biogenesis. Mol. Cell. Biol. 17:5001-5015.