Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing

Journal of Cell Biology

Volumn 149, Issue 3, 2000, Pages 575-589

  Fath, Stephan ^a   Milkereit, Philipp ^a   Podtelejnikov, Alexandre V ^b   Bischler, Nicolas ^c   Schultz, Patrick ^c   Bier, Mirko ^a   Mann, Matthias ^b   Tschochner, Herbert ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

In vitro transcription; Matrix assisted laser desorption ionization (MALDI) mass spectrometry; Nucleolus; Ribosome biogenesis; Saccharomyces cerevisiae

Indexed keywords

RIBOSOME DNA; RIBOSOME RNA; RNA POLYMERASE; SMALL NUCLEAR RNA; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME STRUCTURE; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN PURIFICATION; RNA PROCESSING; RNA SYNTHESIS; YEAST;

CELL NUCLEOLUS; DNA, RIBOSOMAL; MACROMOLECULAR SUBSTANCES; MASS SPECTROMETRY; MICROSCOPY, IMMUNOELECTRON; NUCLEAR PROTEINS; RIBONUCLEOPROTEINS; RNA POLYMERASE I; RNA, RIBOSOMAL; RNA, SMALL NUCLEOLAR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; YEASTS;

EID: 0034193524     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.3.575     Document Type: Article

References (80)

1. Albert, A.C., M. Denton, M. Kermekchiev, and C.S. Pikaard. 1999. Histone acetyltransferase and protein kinase activities copurify with a putative RNA polymerase I holoenzyme self-sufficient for promoter-dependent transcription. Mol. Cell. Biol. 19:796-806.
2. Allmang, C., and D. Tollervey. 1998. The role of the 3′ external transcribed spacer in yeast pre-rRNA processing. J. Mol. Biol. 278:67-78.
3. 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.
4. Bell, P., M.C. Dabauvalle, and U. Scheer. 1992. In vitro assembly of prenucleolar bodies in Xenupus egg extract. J. Cell Biol. 118:1297-1304.
5. Beltrame, M., and D. Tollervey. 1992. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO (Eur. Mol. Biol. Organ.) J. 11:1531-1542.
6. Benton, B.M., J.H. Zang, and J. Thorner. 1944. A novel FK506- and rapamycin-binding protein (FPR3 gene product) in the yeast Saccharomyces cerevisiae is a proline rotamase localized to the nucleolus. J. Cell Biol. 127:623-639.
7. Brand, R.C., J. Klootwijk, C.P. Sibum, and R.J. Planta. 1979. Pseudouridylation of yeast ribosomal precursor RNA. Nucleic Acids Res. 7:121-134.
8. Cadwell, C., H.J. Yoon, Y. Zebarjadian, and J. Carbon. 1997. The yeast nucleolar protein Cbf5p is involved in rRNA biosynthesis and interacts genetically with the RNA polymerase I transcription factor RRN3. Mol. Cell. Biol. 17:6175-6183.
9. Chamberlain, J.R., Y. Lee, W.S. Lane, and D.R. Engelke. 1998. Purification and characterization of the nuclear RNase P holoenzyme complex reveals extensive subunit overlap with RNase MRP. Genes Dev. 12:1678-1690.
10. Clarke, E.M., C.L. Peterson, A.V. Brainard, and D.L. Riggs. 1996. Regulation of the RNA polymerase I and III transcription systems in response to growth conditions. J. Biol. Chem. 271:22189-22195.
11. Cormack, B.P., and K. Struhl. 1992. The TATA-binding protein is required for transcription by all three nuclear RNA polymerases in yeast cells. Cell. 69: 685-696.
12. Cuadros-Fernandez, J.M., and P. Esponada. 1996. Immunocytochemical localization of the nucleolar protein fibrillarin and RNA polymerase 1 during mouse early embryogenesis. Zygote. 4:49-58.
13. Dechampesme, A.-M., O. Koroleva, I. Leger-Silvestre, N. Gas, and S. Camier. 1999. Assembly of 5S ribosomal RNA is required at a specific step of the pre-rRNA processing pathway. J. Cell Biol. 145:1369-1380.
14. Dolinski, K., S. Muir, M. Cardenas, and J. Heitmann. 1997. All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 94:13093-13098.
15. Garcia Blanco, M.A., D.D. Miller, and M.P. Sheetz. 1995. Nuclear spreads: I. Visualization of bipartite ribosomal RNA domains. J. Cell Biol. 128:15-27.
16. Grandi, P., V. Doye, and E.C. Hurt. 1993. Purification of NSP1 reveals complex formation with 'GLFG' nucleoporins and a novel nuclear pore protein NIC96. EMBO (Eur. Mol. Biol. Organ.) J. 12:3061-3071.
17. Grosjean, H., L. Droogmans, R. Giege, and O.C. Uhlenbeck. 1990. Guanosine modifications in runoff transcripts of synthetic transfer RNA-Phe genes microinjected into Xenopus oocytes. Biochim. Biophys. Acta. 1050:267-273.
18. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 1-726.
19. 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 (Eur. Mol. Biol. Organ.) J. 17: 7078-7090.
20. Hozak, P. 1996. The nucleoskeleton and attached activities. Exp. Cell Res. 229: 267-271.
21. Hozak, P., P.R. Cook, C. Schofer, W. Mosgoller, and F. Wachtler. 1994. Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J. Cell Sci. 107:639-648.
22. Iborra, F.J., A. Pombo, D.A. Jackson, and P.R. Cook. 1996. Active RNA polymerases are localized within discrete transcription "factories' in human nuclei. J. Cell Sci. 109:1427-1436.
23. Jackson, D.A., and P.R. Cook. 1995. The structural basis of nuclear function. Int. Rev. Cytol. 162A:125-149.
24. Jackson, D.A., A.B. Hassan, R.J. Errington, and P.R. Cook. 1993. Visualization of focal sites of transcription within human nuclei. EMBO (Eur. Mol. Biol. Organ.) J. 12:1059-1065.
25. Jensen, O.N., A. Podtelejnikov, and M. Mann. 1996. Delayed extraction improves specificity in database searches by matrix-assisted laser desorption/ ionization peptide maps. Rapid Commun. Mass Spectrom. 10:1371-1378.
26. Jimenez Garcia, L.F., M.L. Segura Valdez, R.L. Ochs, L.I. Rothblum, R. Hannan, and D.L. Spector. 1994. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol. Biol. Cell. 5:955-966.
27. Jordan, P., M. Mannervik, L. Tora, and M. Carmo-Fonseca. 1996. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase 1 when rRNA synthesis is either active or inactive. J. Cell Biol. 133:225-234.
28. Keener, J., J.A. Dodd, D. Lalo, and M. Nomura. 1997. Histones H3 and H4 are components of upstream activation factor required for the high-level transcription of yeast rDNA by RNA polymerase I. Proc. Natl. Acad. Sci. USA. 94:13458-13462.
29. Keener, J., C. Josaitis, J. Dodd, and M. Nomura. 1998. Reconstitution of yeast RNA polymerase I transcription in vitro from purified factors. J. Biol. Chem. 273:33795-33802.
30. Keys, D.A., L. Vu, J.S. Steffan, J.A. Dodd, R.T. Yamamoto, Y. Nogi, and M. Nomura. 1994. RRN6 and RRN7 encode subunits of a multiprotein complex essential for the initiation of rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae. Genes Dev. 8:2349-2362.
31. Keys, D.A., B.S. Lee, J.A. Dodd, T.T. Nguyen, L. Vu, E. Fantino, L.M. Burson, Y. Nogi, and M. Nomura. 1996. Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex. Genes Dev. 10:887-903.
32. Lafontaine, D., and D. Tollervey. 1998. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. TIBS (Trends Biochem. Sci.). 23:383-388.
33. 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.
34. Lai, J.-S., and W. Herr. 1992. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. USA. 89:6958-6962.
35. Lalo, D., J.S. Steffan, J.A. Dodd, and M. Nomura. 1996. RRN11 encodes the third subunit of the complex containing Rrn6p and Rrn7p that is essential for the initiation of rDNA transcription by yeast RNA polymerase I. J. Biol. Chem. 271:21062-21067.
36. Lamond, A., and M. Mann. 1997. Cell biology and the genome projects - a concerted strategy for characterizing multiprotein complexes by using mass spectrometry. Trends Cell Biol. 7:139-142.
37. Lang, W.H., B.E. Morrow, Q. Ju, J.R. Warner, and R.H. Reeder. 1994. A model for transcription termination by RNA polymerase I. Cell. 79:527-534.
38. Lazdins, I.B., M. Delannoy, and B. Sollner-Webb. 1997. Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization. Chromosoma. 105:481-495.
39. Leger-Silvestre, I., M.P. Gulli, J. Noaillac-Depeyre, M. Faubladier, H. Sicard, M. Caizergues-Ferrer, and N. Gas. 1997. Ultrastructural changes in the Schizosaccharomyces pombe nucleolus following the disruption of the gar2+ gene, which encodes a nucleolar protein structurally related to nucleolin. Chromosoma. 105:542-552.
40. Leger-Silvestre, I., S. Trumtel, J. Noaillac-Depeyre, and N. Gas. 1999. Functional compartmentalization of the nucleus in the budding yeast Saccharomyces cerevisiae. Chromsoma. 108:103-113.
41. Lin, C.W., B. Moorefield, J. Payne, P. Aprikian, K. Mitomo, and R.H. Reeder. 1996. A novel 66-kilodalton protein complexes with Rrn6, Rrn7, and TATA-binding protein to promote polymerase I transcription initiation in Saccharomyes cerevisiae. Mol. Cell. Biol. 16:6436-6443.
42. Milkereit, P., and H. Tschochner. 1998. A specialized form of RNA polymerase I. essential for initiation and growth dependent regulation of rRNA synthesis, is disrupted during transcription. EMBO (Eur. Mol. Biol. Organ.) J. 17: 3692-3703.
43. Milkereit, P., P. Schultz, and H. Tschochner. 1997. Resolution of RNA polymerase I into dimers and monomers and their function in transcription. Biol. Chem. 378:1433-1443.
44. Mitchell, P., E. Petfalski, A. Shevehenko, M. Mann, and D. Tollervey. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell. 91:457-466.
45. Morrissey, J.P., and D. Tollervey. 1997. U14 small nucleolar RNA makes multiple contacts with the pre-ribosomal RNA. Chromosoma. 105:515-522.
46. Mosgoeller, W., C. Schofer, J. Wesierska Gadek, M. Steiner, M. Muller, and F. Wachtler. 1998. Ribosomal gene transcription is organised in foci within nucleolar components. Histochem. Cell Biol. 109:111-118.
47. Mougey, E.B., M. O'Reilly, Y. Osheim, O.L. Miller, Jr., A. Beyer, and B. Sollner Webb. 1993. The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev. 7:1609-1619.
48. Musters, W., J. Knol, P. Maas, A.F. Dekker, H. van Heerikhuizen, and R.J. Planta. 1989a. Linker scanning of the yeast RNA polymerase I promoter. Nucleic Acids Res. 17:9661-9678.
49. Nogi, Y., R. Yano, and M. Nomura. 1991. Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Proc. Natl. Acad. Sci. USA. 88:3962-3966.
50. Oakes, M., Y. Nogi, M.W. Clark, and M. Nomura. 1993. Structural alterations of the nucleolus in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Mol. Cell. Biol. 13:2441-2455.
51. Oakes, M., J.P. Aris, J.S. Brockenbrough, H. Wai, L. Vu, and M. Nomura. 1998. Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J. Cell Biol. 143:23-34.
52. Pombo, A., D.A. Jackson, M. Hollinshead, Z. Wang, R.G. Roeder, and P.R. Cook. 1999. Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III. EMBO (Eur. Mol. Biol. Organ.) J. 18:2241-2253.
53. Riggs, D.L., C.L. Peterson, J.Q. Wickham, L.M. Miller, E.M. Clarke, J.A. Crowell, and J.C. Sergere. 1995. Characterization of the components of reconstituted Saccharomyces cerevisiae RNA polymerase I transcription complexes. J. Biol. Chem. 270:6205-6210.
54. Saez-Vasquez, J., and C.S. Pikaard. 1997. Extensive purification of a putative RNA polymerase I holoenzyme from plants that accurately initiates rRNA gene transcription in vitro. Proc. Natl. Acad. Sci. USA. 94:11869-11874.
55. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 1-18.86.
56. Scheer, U., and R. Hock. 1999. Structure and function of the nucleolus. Curr. Opin. Cell Biol. 11:385-390.
57. Schultz, M.C., R.H. Reeder, and S. Hahn. 1992. Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II, and III promoters. Cell. 69:697-702.
58. Schultz, P., H. Celia, M. Riva, S.A. Darst, P. Colin, R.D. Kornberg, A. Sentenac, and P. Oudet. 1990. Structural study of the yeast RNA polymerase A. Electron microscopy of lipid-bound molecules and two-dimensional crystals. J. Mol. Biol. 216:353-362.
59. Seither, P., S. Iben, and I. Grummt. 1998. Mammalian RNA polymerase I exists as a holoenzyme with associated basal transcription factors. J. Mol. Biol. 275: 43-53.
60. Shevchenko, A., O.N. Jensen, A.V. Podtelejnikov, F. Sagliocco, M. Wilm, O. Vorm, P. Mortensen, A. Shevchenko, H. Boucherie, and M. Mann. 1996a. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. USA. 93:14440-14445.
61. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996b. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 68: 850-858.
62. Simos, G., H. Tekotte, H. Grosjean, A. Segref, K. Sharma, D. Tollervey, and E. Hurt. 1996. Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO (Eur. Mol. Biol. Organ.) J. 15:2270-2284.
63. Smith, C.M., and J.A. Steitz. 1997. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell. 89:669-672.
64. Steffan, J.S., D.A. Keys, J.A. Dodd, and M. Nomura. 1996. The role of TBP in rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae: TBP is required for upstream activation factor dependent recruitment of core factor. Genes Dev. 10:2551-2563.
65. Steffan, J.S., D.A. Keys, L. Vu, and M. Nomura. 1998. Interaction of TATA-binding protein with upstream activation factor is required for activated transcription of ribosomal DNA by RNA polymerase I in Saccharomyces cerevisiae in vivo. Mol. Cell. Biol. 18:3752-3761.
66. Stewart, S.E., and G.S. Roeder. 1989. Transcription by RNA polymerase I stimulates mitotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 9:3464-3472.
67. Szweykowska Kulinska, Z., B. Senger, G. Keith, F. Fasiolo, and H. Grosjean. 1994. Intron-dependent formation of pseudouridines in the anticodon of Saccharomyces cerevisiae minor tRNA(Ile). EMBO (Eur. Mol. Biol. Organ.) J. 13:4636-4644.
68. Tollervey, D., and T. Kiss. 1997. Function and synthesis of small nucleolar RNAs. Curr. Opin. Cell Biol. 9:337-342.
69. Tschochner, H. 1996. A novel RNA polymerase I-dependent RNase activity that shortens nascent transcripts from the 3′ end. Proc. Natl. Acad. Sci. USA. 93:12914-12919.
70. Tschochner, H., and P. Milkereit. 1997. RNA polymerase I from S. cerevisiae depends on an additional factor to release terminated transcripts from the template. FEBS Lett. 410:461-466.
71. Veinot Drebot, L.M., R.A. Singer, and G.C. Johnston. 1988. Rapid initial cleavage of nascent pre-rRNA transcripts in yeast. J. Mol. Biol. 199:107-113.
72. Venema, J., and D. Tollervey. 1995. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast. 11:1629-1650.
73. Venema, J., and D. Tollervey. 1996. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 15:57111-5714.
74. Verheggen, C., S. Le Panse, G. Almouzni, and D. Hernandez Verdun. 1998. Presence of pre-rRNAs before activation of polymerase I transcription in the building process of nucleoli during early development of Xenopus laevis. J. Cell Biol. 142:1167-1180.
75. Vorm, O., P. Roepstorff, and M. Mann. 1994. Improved resolution and very high sensitivity in MALDI TOF of matrix surfaces made by fast evaporation. Anal. Chem. 66:3281-3287.
76. Wansink, D.G., W. Schul, I. van der Kraan, B. van Steensel, R. van Driel, and L. de Jong. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122:283-293.
77. 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 Gar1p in all H BOX/ACA-motif snoRNPs and constitute a common bipartite structure. RNA. 4:1549-1568.
78. Weipoltshammer, K., C. Schofer, F. Wachtler, and P. Hozak. 1996. The transcription unit of ribosomal genes is attached to the nuclear skeleton. Exp. Cell Res. 227:374-379.
79. Yamamoto, R.T., Y. Nogi, J.A. Dodd, and M. Nomura. 1996. RRN3 gene of Saccharomyces cerevisiae encodes an essential RNA polymerase 1 transcription factor which interacts with the polymerase independently of DNA template. EMBO (Eur. Mol. Biol. Organ.) J. 15:3964-3973.
80. Zatsepina, O.V., O.A. Dudnic, I.T. Todorov, M. Thiry, H. Spring, and M.F. Trendelenburg. 1997. Experimental induction of prenucleolar bodies (PNBs) in interphase cells: interphase PNBs show similar characteristics as those typically observed at telophase of mitosis in untreated cells. Chromosoma. 105:418-430.