Spb1p is a yeast nucleolar protein associated with Nop1p and Nop58p that is able to bind S-adenosyl-L-methionine in vitro

Molecular and Cellular Biology

Volumn 20, Issue 4, 2000, Pages 1370-1381

  Pintard, Lionel ^a   Kressler, Dieter ^b   Lapeyre, Bruno ^a  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; NUCLEOLIN; PROTEIN DERIVATIVE; S ADENOSYLMETHIONINE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE REPRESSION; GENE SILENCING; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; RNA PROCESSING; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

ALLELES; AMINO ACID SEQUENCE; BASE SEQUENCE; CONSERVED SEQUENCE; DNA PRIMERS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DELETION; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; RIBONUCLEOPROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; RNA, RIBOSOMAL; RNA-BINDING PROTEINS; S-ADENOSYLMETHIONINE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUPPRESSION, GENETIC; TEMPERATURE;

EID: 0033978580     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.4.1370-1381.2000     Document Type: Article

References (82)

1. Adam, S. A., T. Nakagawa, M. S. Swanson, T. K. Woodruff, and G. Dreyfuss. 1986. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol. 6:2932-2943.
2. Aletta, J. M., T. R. Cimato, and M. J. Ettinger. 1998. Protein methylation: a signal event in post-translational modification. Trends Biochem. Sci. 23: 89-91.
3. Aris, J. P., and G. Blobel. 1988. Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein. J. Cell Biol. 107:17-31.
4. Bachellerie, J. P., and J. Cavaille. 1997. Guiding ribose methylation of rRNA. Trends Biochem. Sci. 22:257-261.
5. Balakin, A. G., L. Smith, and M. J. Fournier. 1996. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 86:823-834.
6. Baserga, S. J., T. M. Agentis, S. Wormsley, D. A. Dunbar, and S. Lee. 1997. Mpp10p, a new protein component of the U3 snoRNP required for processing of 18S rRNA precursors. Nucleic Acids Symp. Ser. 36:64-67.
7. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
8. Bergès, T., E. Petfalski, D. Tollervey, and E. C. Hurt. 1994. Synthetic lethality with fibrillarin identifies NOP77p, a nucleolar protein required for pre-rRNA processing and modification. EMBO J. 13:3136-3148.
9. Bork, P., C. Ouzounis, C. Sander, M. Scharf, R. Schneider, and E. Sonnhammer. 1992. Comprehensive sequence analysis of the 182 predicted open reading frames of yeast chromosome III. Protein Sci. 1:1677-1690.
10. Bouvet, P., J. J. Diaz, K. Kindbeiter, J. J. Madjar, and F. Amalric. 1998. Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273:19025-19029.
11. Brown, T., and K. Mackey. 1997. Analysis of RNA by Northern and slot blot hybridization, p. 4.9.1-4.9.16. In F. M. Ausubel (ed.), Current protocols in molecular biology, vol. 1. John Wiley & Sons, New York, N.Y.
12. Christensen, M. E., and K. P. Fuxa. 1988. The nucleolar protein, B-36, contains a glycine and dimethylarginine-rich sequence conserved in several other nuclear RNA-binding proteins. Biochem. Biophys. Res. Commun. 155: 1278-1283.
13. Clarke, S. 1993. Protein methylation. Curr. Opin. Cell Biol. 5:977-983.
14. Cross, F. R., and A. H. Tinkelenberg. 1991. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle. Cell 65:875-883.
15. de la Cruz, J., D. Kressler, M. Rojo, D. Tollervey, and P. Linder. 1998. 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.
16. Eisinger, D. P., F. A. Dick, and B. L. Trumpower. 1997. Qsr1p, a 60S ribosomal subunit protein, is required for joining of 40S and 60S subunits. Mol. Cell. Biol. 17:5136-5145.
17. Frankel, A., and S. Clarke. 1999. RNase treatment of yeast and mammalian cell extracts affects in vitro substrate methylation by type I protein arginine N-methyltransferases. Biochem. Biophys. Res. Commun. 259:391-400.
18. Ganot, P., M. Caizergues-Ferrer, and T. Kiss. 1997. The family of box ACA small nucleolar RNAs is defined by an evolutionary conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. Genes Dev. 11:941-956.
19. Gary, J. D., and S. Clarke. 1998. RNA and protein interactions modulated by protein arginine methylation. Prog. Nucleic Acid Res. Mol. Biol. 61: 65-131.
20. Gary, J. D., W. J. Lin, M. C. Yang, H. R. Herschman, and S. Clarke. 1996. The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J. Biol. Chem. 271:12585-12594.
21. Gautier, T., T. Bergès, D. Tollervey, and E. Hurt. 1997. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol. Cell. Biol. 17:7088-7098.
22. Ghisolfi, L., G. Joseph, F. Amalric, and M. Erard. 1992. The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267:2955-2959.
23. Ghisolfi, L., A. Kharrat, G. Joseph, F. Amalric, and M. Erard. 1992. Concerted activities of the RNA recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with preribosomal RNA. Eur. J. Biochem. 209:541-548.
24. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
25. Girard, J.-P., H. Lehtonen, M. Caizergues-Ferrer, F. Amalric, D. Tollervey, and B. Lapeyre. 1992. GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast. EMBO J. 11:673-682.
26. Guthrie, C., and R. G. Fink. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1-863.
27. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
28. Helser, T. L., R. A. Baan, and A. E. Dahlberg. 1981. Characterization of a 40S ribosomal subunit complex in polyribosomes of Saccharomyces cerevisiae treated with cycloheximide. Mol. Cell. Biol. 1:51-57.
29. Henras, A., Y. Henry, C. Bousquet-Antonelli, J. Noaillac-Depeyre, J. P. Gelugne, and M. Caizergues-Ferrer. 1998. Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J. 17:7078-7090.
30. Henriquez, R., G. Blobel, and J. P. Aris. 1990. Isolation and sequencing of NOP1. A yeast gene encoding a nucleolar protein homologous to a human autoimmune antigen. J. Biol. Chem. 265:2209-2215.
31. Higman, M. A., and E. G. Niles. 1994. Location of the S-adenosyl-L-methionine binding region of the vaccinia virus mRNA (guanine-7-)methyltrans-ferase. J. Biol. Chem. 269:14982-14987.
32. 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.
33. Hughes, J. M., and M. J. Ares. 1991. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10:4231-4239.
34. Hutchison, H. T., L. H. Hartwell, and C. S. McLaughlin. 1969. Temperature-sensitive yeast mutant defective in ribonucleic acid production. J. Bacteriol. 99:807-814.
35. Ingrosso, D., A. V. Fowler, J. Bleibaum, and S. Clarke. 1989. Sequence of the D-aspartyl/L-isoaspartyl protein methyltransferase from human erythrocytes. Common sequence motifs for protein, DNA, RNA, and small molecule S-adenosylmethionine-dependent methyltransferases. J. Biol. Chem. 264:20131-20139.
36. Jansen, R., D. Tollervey, and E. C. Hurt. 1993. A U3 snoRNP protein with homology to splicing factor PRP4 and G beta domains is required for ribosomal RNA processing. EMBO J. 12:2549-2558.
37. Jong, A. Y., M. W. Clark, M. Gilbert, A. Oehm, and J. L. Campbell. 1987. Saccharomyces cerevisiae SSB1 protein and its relationship to nucleolar RNA-binding proteins. Mol. Cell. Biol. 7:2947-2955.
38. Kiledjian, M., and G. Dreyfuss. 1992. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 11: 2655-2664.
39. Kim, S., G. H. Park, and W. K. Paik. 1998. Recent advances in protein methylation: enzymatic methylation of nucleic acid binding proteins. Amino Acids 15:291-306.
40. Klimasauskas, S., A. Timinskas, S. Menkevicius, D. Butkiene, V. Butkus, and A. Janulaitis. 1989. Sequence motifs characteristic of DNA[cytnsine-N4]methyltransferases: similarity to adenine and cytosine-C5 DNA-methyl-ases. Nucleic Acids Res. 17:9823-9832.
41. Koonin, E. V., P. Bork, and C. Sander. 1994. Yeast chromosome III: new gene functions. EMBO J. 13:493-503.
42. Kressler, D., J. de la Cruz, M. Rojo, and P. Linder. 1998. Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1855-1865.
43. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
44. Lafontaine, D. L., and D. Tollervey. 1998. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. 23:383-388.
45. Lafontaine, D. L., and D. Tollervey. 1999. Nop58p is a common component of the box C + D snoRNPs that is required for snoRNA stability. RNA 5: 455-467.
46. Lafontaine, D. L. J., C. Bousquet-Antonelli, Y. Henry, M. Caizergues-Ferrer, and D. Tollervey. 1998. The box H + ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase. Genes Dev. 12:527-537.
47. Lapeyre, B., F. Amalric, S. H. Ghaffari. S. V. Rao, T. S. Dumbar, and M. O. Olson. 1986. Protein and cDNA sequence of a glycine-rich, dimethylarginine-containing region located near the carboxyl-terminal end of nucleolin (C23 and 100 KDa). J. Biol. Chem. 261:9167-9173.
48. Lapeyre, B., P. Mariottini, C. Mathieu, P. Ferrer, F. Amaldi, F. Amalric, and M. Caizergues-Ferrer. 1990. Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease. Mol. Cell. Biol. 10:430-434.
49. Lee, S., and S. J. Baserga. 1999. Imp3p and Imp4p: two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol. Cell. Biol. 19:5441-5452.
50. Lee, W. C., Z. X. Xue, and T. Mélèse. 1991. The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs. J. Cell Biol. 113:1-12.
51. Li, H. D., J. Zagorski, and M. J. Fournier. 1990. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:1145-1152.
52. Lischwe, M. A., R. G. Cook, Y. S. Ahn, L. C. Yeoman, and H. Busch. 1985. Clustering of glycine and NG,NG-dimethylarginine in nucleolar protein C23. Biochemistry 24:6025-6028.
53. r = 34,000; pI. 8.5) rich in NG,NG-dimethylarginine. J. Biol. Chem. 260:14304-14310.
54. Loo, S., P. Laurenson, M. Foss, A. Dillin, and J. Rine. 1995. Roles of ABF1, NPL3, and YCL54 in silencing in Saccharomyces cerevisiae. Genetics 141: 889-902.
55. Luthe, D. S. 1983. A simple technique for the preparation and storage of sucrose gradients. Anal. Biochem. 135:230-232.
56. Morrissey, J. P., and D. Tollervey. 1993. Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol. Cell. Biol. 13:2469-2477.
57. Niewmierzycka, A., and S. Clarke. 1999. S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae. Identification of a novel protein arginine methyltransferase. J. Biol. Chem. 274:814-824.
58. Niman, H. L., R. A. Houghten, L. E. Walker, R. A. Reisfeld, I. A. Wilson, J. M. Hogle, and R. A. Lerner. 1983. Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc. Natl. Acad. Sci. USA 80:4949-4953.
59. Nomura, M. 1973. Assembly of bacterial ribosomes. Science 179:864-873.
60. Oliver, S. G., Q. J. van der Aart, M. L. Agostoni-Carbone, M. Aigle, L. Alberghina, D. Alexandraki, G. Antoine, R. Anwar, J. P. Ballesta, P. Benit, et al. 1992. The complete DNA sequence of yeast chromosome III. Nature 357: 38-46.
61. Sachs, A. B., and R. W. Davis. 1989. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58:857-867.
62. Sachs, A. B., and R. W. Davis. 1990. Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase and RPL46. Science 247: 1077-1079.
63. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
64. Scheer, U., and D. Weisenberger. 1994. The nucleolus. Curr. Opin. Cell Biol. 6:354-359.
65. Schimmang, T., D. Tollervey, H. Kern, R. Frank, and E. C. Hurt. 1989. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 8:4015-4024.
66. Schluckebier, G., M. O'Gara, W. Saenger, and X. Cheng. 1995. Universal catalytic domain structure of AdoMet-dependent methyltransferases. J. Mol. Biol. 247:16-20.
67. Sillevis-Smitt, W. W., J. M. Vlak, I. Molenaar, and T. H. Rozijn. 1973. Nucleolar function of the dense crescent in the yeast nucleus. A biochemical and ultrastructural study. Exp. Cell Res. 80:313-321.
68. Sun, C., and J. L. Woolford, Jr. 1994. The yeast NOP4 gene product is an essential nucleolar protein required for pre-rRNA processing and accumulation of 60S ribosomal subunits. EMBO J. 13:3127-3135.
69. Tollervey, D. 1996. Trans-acting factors in ribosome synthesis. Exp. Cell Res. 229:226-232.
70. Tollervey, D. 1987. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 6:4169-4175.
71. Tollervey, D., and T. Kiss. 1997. Function and synthesis of small nucleolar RNAs. Curr. Opin. Cell Biol. 9:337-342.
72. Tollervey, D., H. Lehtonen, M. Carmo-Fonseca, and E. C. Hurt. 1991. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10:573-583.
73. Tollervey, D., H. Lehtonen, R. Jansen, H. Kern, and E. C. Hurt. 1993. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 72:443-457.
74. Tomovasu, T., T. Yuki, S. Morimura, H. Mori, K. Yamanaka, H. Niki, S. Hiraga, and T. Ogura. 1993. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175:1344-1351.
75. Tron, T., M. Yang, F. A. Dick, M. E. Schmitt, and B. L. Trumpower. 1995. QSR1, an essential yeast gene with a genetic relationship to a subunit of the mitochondrial cytochrome bc1 complex, is homologous to a gene implicated in eukaryotic cell differentiation. J. Biol. Chem. 270:9961-9970.
76. Valentini, S. R., V. H. Weiss, and P. A. Silver. 1999. Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 3′-end formation. RNA 5:272-280.
77. Venema, J., and D. Tollervey. 1995. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast 11:1629-1650.
78. Warner, J. R. 1990. The nucleolus and ribosome formation. Curr. Opin. Cell Biol. 2:521-527.
79. Watkins, N. J., A. Gottschalk, G. Neubauer, B. Kastner, P. Fabrizio, M. Mann, and R. Luhrmann. 1998. Cbf5p, a potential pseudouridine synthase, and Nhp2p, a putative RNA-binding protein, are present together with Garlp in all H BOX/ACA-motif snoRNPs and constitute a common bipartite structure. RNA 4:1549-1568.
80. Wiederkehr, T., R. F. Pretot, and L. Minvielle-Sebastia. 1998. Synthetic lethal interactions with conditional poly(A) polymerase allles identify LCP5, a gene involved in 18S rRNA maturation. RNA 4:1357-1372.
81. Wu, P., J. S. Brockenbrough, A. C. Metcalfe, S. Chen, and J. P. Aris. 1998. Nop5p is a small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast. J. Biol. Chem. 273:16453-16463.
82. Zhong, T., and K. T. Arndt. 1993. The yeast SIS1 protein, a DnaJ homolog, is required for the initiation of translation. Cell 73:1175-1186.