Role of the yeast Rrp1 protein in the dynamics of pre-ribosome maturation

RNA

Volumn 10, Issue 5, 2004, Pages 813-827

  Horsey, Edward W ^a   Jakovljevic, Jelena ^a   Miles, Tiffany D ^a   Harnpicharnchai, Piyanun ^a   Woolford Jr , John L ^a,b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Pre ribosomes; Pre rRNA processing

Indexed keywords

FUNGAL PROTEIN; RIBOSOME RNA; RRP1 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; FLUORESCENCE MICROSCOPY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RIBOSOME; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; WESTERN BLOTTING; YEAST;

AMINO ACID SEQUENCE; CELL NUCLEOLUS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; RIBOSOMES; RNA PRECURSORS; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 1942501618     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.5255804     Document Type: Article

References (78)

1. Adams, C.C., Jakovljevic, J., Roman, J., Harnpicharnchai, P., and Woolford Jr., J.L. 2002. Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA 8: 150-165.
2. Andersen, J.S., Lyon, C.E., Fox, A.H., Leung, A.K.L., Lam, Y.W., Steen, H., Mann, M., and Lamond, A.I. 2002. Directed proteomic analysis of the human nucleolus. Curr. Biol. 12: 1-11.
3. Andrew, C., Hopper, A.K., and Hall, B.D. 1976. A yeast mutant defective in the processing of 27S rRNA precursor. Mol. Gen. Genet. 144: 29-37.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. 1994. Current protocols in molecular biology. Wiley, New York.
5. Baßler, J., Grandi, P., Gadal, O., Lessmann, T., Petfalski, E., Tollervey, D., Lechner, J., and Hurt, E. 2001. Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell 8: 517-529.
6. Basu, U., Kausik, S., Warner, J.R., and Maitra, U. 2001. The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 21:1453-1462.
7. Burger, F., Daugeron, M.-C., and Linder, P. 2000. Dbp10p, a putative RNA helicase from Saccharomyces cerevisiae, is required for ribosome biogenesis. Nucl. Acids Res. 28: 2315-2323.
8. BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426: 579-584.
9. de Beus, E., Brockenbrough, J.S., Hong, B., and Aris, J.P. 1994. Yeast NOP2 encodes an essential nucleolar protein with homology to a human proliferation marker. J. Cell Biol. 127: 1799-1813.
10. Dechampesme, A.M., Koroleva, O., Leger-Silvestre, I., Gas, N., and Camier, S. 1999. Assembly of 5S ribosomal RNA is required at a specific step of the pre-rRNA processing pathway. J. Cell. Biol. 145:1369-1380.
11. Deshmukh, M., Tsay, Y.-F., Paulovich, A.G., and Woolford Jr., J.L. 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.
12. Dragon, F., Gallagher, J.E.G., Compagnone-Post, P.A, Mitchell, B.M., Porwancher, K.A., Wehner, K.A., Wormsley, S., Settlage, R.E, Shabanowitz, J., Osheim, Y., et al. 2002. A large U3 snoRNP complex which is required for 18S rRNA biogenesis. Nature 417: 967-970.
13. Dunbar, D.A., Dragon, F., Lee, S.J., and Baserga, S.J. 2000. A nucleolar protein related to ribosomal protein L7 is required for an early step in large ribosomal subunit biogenesis. Proc. Natl. Acad. Sci. 97: 13027-13032.
14. Edskes, H.K., Ohtake, Y., and Wickner, R.B. 1998. Mak21p of Saccharomyces cerevisiae, a homolog of human CAATT-binding protein, is essential for 60S ribosomal subunit biogenesis. J. Biol. Chem. 273:28912-28920.
15. Eichler, D.C., and Craig, N. 1994. Processing of eukaryotic ribosomal RNA. Prog. Nucl. Acids Res. Mol. Biol. 49:197-237.
16. Emery, B., de la Cruz, J., Rocak, S., Deloche, O., and Linder, P. 2004. Has1p, a member of the DEAD-box family, is required for 40S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Mol. Microbiol. (in press).
17. Fabian, G.R., and Hopper, A.K. 1987. RRP1, a Saccharomyces cerevisiae gene affecting rRNA processing and production of mature ribosomal subunits. J. Bacteriol. 169: 1571-1578.
18. Fath, S., Milkereit, P., Podtelejnikov, A.V., Bischler, N., Schultz, P., Bier, M., Mann, M., and Tschochner, H. 2000. Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing. J. Cell Biol. 149: 575-589.
19. Fatica, A., Cronshaw, A.D., Dlakic, M., and Tollervey, D. 2002. Ssf1p prevents premature processing of an early 66S ribosomal particle. Mol. Cell 9: 341-351.
20. Gadal, O., Strauß, D., Petfalski, E., Gleizes, P.-E., Gas, N., Tollervey, D., and Hurt, E. 2002. Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J. Cell Biol. 157: 941-951.
21. Gavin, A.C., Bösche, M., Krause, R., Grandim, P., Marzioch, M., Bauer, A., Schultzm, J., Rick, J.M., Michon, A., Cruciatm, C., et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
22. Geerlings, T.H., Vos, J.C., and Raué, H.A. 2000. The final step in the formation of 25S rRNA in Saccharomyces cerevisiae is performed by 5' → 3" exonucleases. RNA 6: 1698-1703.
23. Giaever, G., Chu, A.M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B., et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
24. Gorenstein, C. and Warner, J.R. 1977. Synthesis and turnover of ribosomal proteins in the absence of 60S subunit assembly in Saccharomyces cerevisiae. Molec. Gen. Genet. 157: 327-332.
25. Grandi, P., Rybin, V., Baßler, J., Petkalski, E., Strauß, D., Marzioch, M., Schäfer, T., Kuster, B., Tschochner, H., Tollervey, D., et al. 2002. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10: 105-115.
26. Hadjiolov, A. 1985. The nucleolus and ribosome biogenesis. Cell Biol. Monogr. 12:1-268.
27. Harnpicharnchai, P., Jakovljevic, J., Horsey, E., Miles, T., Roman, J., Rout, M., Meagher, D., Imai, B., Guo, Y., Brame, C.J., et al. 2001. Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell 8:505-515.
28. Helser, T., Baan, R., and Dahlberg, A. 1981. Characterization of a 40S ribosomal subunit complex in polyribosomes of Saccharomyces cerevisiae treated with cycloheximide. Mol. Cell. Biol. 1: 51-57.
29. Henry, Y., Wood, H., Morrissey, J.P., Petfalski, E., Kearsey, S., and Tollervey, D. 1994. The 5′ end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J. 13: 2452-2463.
30. Ho, Y., Gruhler, A., Heilbut, A., Bader, G.D., Moore, L., Adams, S., Millar, A., Taylor, P., Bennett, K., Boutilier, K., et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180-183.
31. Hong, B., Brockenbrough, J.S., Wu, P., and Aris, J.P. 1997. Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol. Cell. Biol. 17: 378-388.
32. Huber, M.D., Dworet, J.H., Shire, K., Frappier, L., and McAlear M.S. 2000. The budding yeast homolog of the human EBNA1-binding protein 2 (Ebp2p) is an essential nucleolar protein required for pre-rRNA processing. J. Biol. Chem. 275: 28764-28773.
33. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153: 163-168.
34. Johnston, M., and Davis, R. 1984. Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 4: 1440-1448.
35. Kaser, A., Bogenbruber, E., Hallegger, M., Doppler, E., Lepperdinger, G., Jantsch, M., Breitenbach, M., and Kreil, G. 2001. Brix from Xenopus laevis and Brx1p from yeast define a new family of proteins involved in the biogenesis of large ribosomal subunits. Biol. Chem. 382: 1637-1647.
36. Kim, J. and Hirsch, J.P. 1998. A nucleolar protein that affects mating efficiency in Saccharomyces cerevisiae by altering the morphological response to pheromone. Genetics 149: 795-805.
37. Kressler, D., Linder, P., and de la Cruz, J. 1999. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 7897-7912.
38. Kumar, A. and Warner, J.R. 1972. Characterization of ribosomal precursor particles from HeLa cell nucleoli. J. Mol. Biol. 63: 233-246.
39. Long, R.M., Gu, W., Meng, X., Gonsalvez, G., Singer, R.H., and Chartrand, P. 2001. An exclusively nuclear RNA-binding protein affects asymmetric localization of ASH1 mRNA and Ash1p in yeast. J. Cell Biol. 153: 307-318.
40. Longtine, M.S., McKenzie 3rd, A., Demarini, D.J., Shah, G., Wach, A., Brachat, A., Philppsen, P., and Pringle, J.R. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
41. Magoulas, C. and Fried, M. 1996. The Surf-6 gene of the mouse surfeit locus encodes a novel nucleolar protein. DNA Cell Biol. 15: 305-316.
42. Milkereit, P., Gadal, O., Podtelejnikov, A., Trumtel, S., Gas, N., Petfalski, E., Tollervey, D., Mann, M., Hurt, E., and Tschochner, H. 2001. Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105: 499-509.
43. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M., and Tollervey, D. 1997. The exosome; a conserved eukaryotic RNA processing complex containing multiple 3′ to 5′ exonucleases. Cell 91: 457-466.
44. Morita, D., Miyoshi, K., Matsui, Y., Toh, E.A., Shinkawa, H., Miyakawa, T., and Mizuta, K. 2002. Rpf2p, an evolutionarily conserved protein, interacts with ribosomal protein L11 and is essential for the processing of 27SB pre-rRNA to 25S rRNA and the 60S ribosomal subunit assembly in Saccharomyces cerevisiae. J. Biol. Chem. 277:28780-28786.
45. Nissan, T.A., Baßler, J., Petfalski, E., Tollervey, D., and Hurt, E. 2002. Pre-60S particles on the road to ribosomes. EMBO J. 21: 5539-5547.
46. Ohtake, Y. and Wickner, R.B. 1995. Yeast virus propagation depends critically on free 60S ribosomal subunit concentration. Mol. Cell. Biol. 15: 2772-2781.
47. Olson, M.O.J., Dundr, M., and Szebeni, A. 2000. The nucleolus: An old factory with unexpected capabilities. Trends Cell Biol. 10: 189-196.
48. Pestov, D.G., Stockelman, M.G., Strezoska, Z., and Lau, L.F. 2001. ERB1, the yeast homolog of mammalian BOP1, is an essential gene required for maturation of the 25S and 5.8S ribosomal RNAs. Nucl. Acids Res. 29: 3621-3630.
49. Prestayko, A.W., Klomp, G.R., Schmoll, A.I., and Busch, H. 1974. Comparison of proteins of ribosomal subunits and nucleolar preribosomal particles from Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Biochemistry 13: 1945-1951.
50. Pringle, J., Preston, R.A., Adams, A.E., Stearns, T., Drubin, D.G., Haarer, B.K., and Jones, E.W. 1989. Fluorescence microscopy methods for yeast. Methods Cell Biol. 31: 357-435.
51. Raué, H.A. 2003. Pre-ribosomal RNA processing and assembly in Saccharomyces cerevisiae. The machine that makes the machine. In The nucleolus (ed. M.O.J. Olson). Kluwer Academic/Plenum Publishers.
52. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotech. 17: 1030-1032.
53. Ripmaster, T.L., Vaughn, G.P., and Woolford Jr., J.L. 1992. A putative ATP-dependent RNA helicase involved in Saccharomyces cerevisiae ribosome assembly. Proc. Natl. Acad. Sci. 89: 11131-11135.
54. Rotenberg, M.O., Moritz, M., and. Woolford Jr., J.L. 1988. Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of halfmer polyribosomes. Genes Dev. 2: 160-172.
55. Saveanu, C., Bienvenu, D., Namane, A, Gleizes, P.E., Gas, N., Jacquier, A., and Fromont-Racine, M. 2001. Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J. 20: 6475-6484.
56. Savino, T.M., Bastos, R., Jansen, E., and Hernandez-Verdun, D. 1999. The nucleolar antigen Nop52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis. J. Cell Sci. 112: 1889-1900.
57. Savino, T.M., Gébrane-Younés, J., De Mey, J., Sibarita, J., and Hernandez-Verdun, D. 2001. Nucleolar assembly of the rRNA processing machinery in living cells. J. Cell Biol. 153: 1097-1110.
58. Schäfer, T., Strauß, D., Petfalski, E., Tollervey, D., and Hurt, E. 2003. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 22:1370-1380.
59. Scherl, A., Coute, Y., Deon, C., Calle, A., Kindbeiter, K., Sanchez, J.-C., Greco, A., Hochstrasser, D., and Diaz, J.J. 2002. Functional proteomic analysis of the human nucleolus. Mol. Biol. Cell 13: 4100-4109.
60. Schmitt, M.E. and Clayton, D.A. 1993. Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol. Cell Biol. 13: 7935-7941.
61. Senger, B., Lafontaine, D.L.J., Graindorge, J., Gadal, O., Camasses, A., Sanni, A., Garmier, J., Breitenbach, M., Hurt, E., and Fasiolo, F. 2001. The nucleolar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8: 1363-1373.
62. Sherman, F., Fink, G.R., and Hicks, J.B. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
63. Si, K. and Maitra, U. 1999. The Saccharomyces cerevisiae homologue of mammalian translation initiation factor 6 does not function as a translation initiation factor. Mol. Cell. Biol. 19: 1416-1426.
64. Sun, C. and Woolford Jr., J.L. 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.
65. Trapman, J. and Planta, R.J. 1976. Maturation of ribosomes in yeast. I Kinetic analysis by labeling of high molecular weight rRNA species. Biochim. Biophys. Acta 442: 265-274.
66. Trapman, J., Retèl, J., and Planta, R.J. 1975. Ribosomal precursor particles from yeast. Exp. Cell Res. 90: 95-104.
67. Tsochner, H. and Hurt, E. 2003. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13: 255-263.
68. Tsujii, R., Miyoshi, K., Tsuno, A., Matsui, Y., Toh-E, A., Miyakawa, T., and Mizuta, K. 2000. Ebp2p, a yeast homologue of a human protein that interacts with Epstein-Barr virus nuclear antigen 1, is required for pre-rRNA processing and ribosomal subunit assembly. Genes Cells 5: 543-553.
69. Udem, S.A. and Warner, J.R. 1973. The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J. Biol. Chem. 248: 1412-1416.
70. Venema, J. and Tollervey, D. 1996. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO J. 15: 5701-5714.
71. Venema, J. and Tollervey, D. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Ann. Rev. Genet. 11: 1629-1650.
72. Venema, J., Planta, R.J., and Raué, H.A. 1998. In vivo mutational analysis of ribosomal RNA in Saccharomyces cerevisiae. Methods Mol. Biol. 77: 257-270.
73. Warner, J. and Soeiro, R. 1967. Nascent ribosomes from HeLa cells. Biochemistry 58: 1984-1990.
74. Wehner, K.A. and Baserga, S.J. 2002. The σ70-like motif: a eukaryotic RNA binding domain unique to a superfamily of proteins required for ribosome biogenesis. Mol. Cell 9: 329-339.
75. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Banham, R., Benito, R., Boeke, J.D., Bussey, H., et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
76. Woolford Jr., J.L. and Warner, J.R. 1991. The ribosome and its synthesis. In The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis, and energetics (eds. J.R. Broach et al.), pp. 587-626. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
77. Yu, Y. and Hirsch, J.P. 1995. An essential gene pair in Saccharomyces cerevisiae with a potential role in mating. DNA Cell Biol. 14: 411-418.
78. Zanchin, N.I.T., Roberts, P., DeSilva, A., Sherman, F., and Goldfarb, D. 1997. Saccharomyces cerevisiae Nip7p is required for efficient 60S ribosome subunit biogenesis. Mol. Cell. Biol. 17: 5001-5015.