RNA polymerase I-specific subunits promote polymerase clustering to enhance the rRNA gene transcription cycle

Journal of Cell Biology

Volumn 192, Issue 2, 2011, Pages 277-293

  Albert, Benjamin ^a,b   Léger Silvestre, Isabelle ^a,b   Normand, Christophe ^a,b   Ostermaier, Martin K ^a,b   Perez Fernandez ^a,b   Panov, Kostya I ^c   Zomerdijk, Joost C B M ^d   Schultz, Patrick ^e   Gadal, Olivier ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; ENZYME; PROTEIN RPA34; PROTEIN RPA49; PROTEIN SUBUNIT; RIBOSOME RNA; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE DELETION; GENE DOSAGE; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RNA GENE; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; STATISTICAL ANALYSIS;

CELL NUCLEOLUS; CELL NUCLEUS SHAPE; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, FUNGAL; GENES, RRNA; GENETIC COMPLEMENTATION TEST; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RNA POLYMERASE I; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 78951476311     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201006040     Document Type: Article

References (45)

1. Basi, G., E. Schmid, and K. Maundrell. 1993. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene. 123:131-136. doi:10.1016/0378-1119(93)90552-E
2. Beckouet, F., S. Labarre-Mariotte, B. Albert, Y. Imazawa, M. Werner, O. Gadal, Y. Nogi, and P. Thuriaux. 2008. Two RNA polymerase I subunits control the binding and release of Rrn3 during transcription. Mol. Cell. Biol. 28:1596-1605. doi:10.1128/MCB.01464-07
3. Berger, A.B., L. Decourty, G. Badis, U. Nehrbass, A. Jacquier, and O. Gadal. 2007. Hmo1 is required for TOR-dependent regulation of ribosomal protein gene transcription. Mol. Cell. Biol. 27:8015-8026. doi:10.1128/MCB.01102-07
4. Berger, A.B., G.G. Cabal, E. Fabre, T. Duong, H. Buc, U. Nehrbass, J.C. Olivo-Marin, O. Gadal, and C. Zimmer. 2008. High-resolution statistical mapping reveals gene territories in live yeast. Nat. Methods. 5:1031-1037. doi:10.1038/nmeth.1266
5. Bischler, N., L. Brino, C. Carles, M. Riva, H. Tschochner, V. Mallouh, and P. Schultz. 2002. Localization of the yeast RNA polymerase I-specific subunits. EMBO J. 21:4136-4144. doi:10.1093/emboj/cdf392
6. Boeke, J.D., F. LaCroute, and G.R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346. doi:10.1007/BF00330984
7. Bon, M., S.J. McGowan, and P.R. Cook. 2006. Many expressed genes in bacteria and yeast are transcribed only once per cell cycle. FASEB J. 20:1721-1723. doi:10.1096/fj.06-6087fje
8. Cioci, F., L. Vu, K. Eliason, M. Oakes, I.N. Siddiqi, and M. Nomura. 2003. Silencing in yeast rDNA chromatin: reciprocal relationship in gene expression between RNA polymerase I and II. Mol. Cell. 12:135-145. doi:10.1016/S1097-2765(03)00262-4
9. Cramer, P., K.J. Armache, S. Baumli, S. Benkert, F. Brueckner, C. Buchen, G.E. Damsma, S. Dengl, S.R. Geiger, A.J. Jasiak, et al. 2008. Structure of eukaryotic RNA polymerases. Annu. Rev. Biophys. 37:337-352. doi:10.1146/annurev. biophys.37.032807.130008
10. De Carlo, S., C. Carles, M. Riva, and P. Schultz. 2003. Cryo-negative staining reveals conformational flexibility within yeast RNA polymerase I. J. Mol. Biol. 329:891-902. doi:10.1016/S0022-2836(03)00510-2
11. Decourty, L., C. Saveanu, K. Zemam, F. Hantraye, E. Frachon, J.C. Rousselle, M. Fromont-Racine, and A. Jacquier. 2008. Linking functionally related genes by sensitive and quantitative characterization of genetic interaction profiles. Proc. Natl. Acad. Sci. USA. 105:5821-5826. doi:10.1073/pnas.0710533105
12. French, S.L., Y.N. Osheim, F. Cioci, M. Nomura, and A.L. Beyer. 2003. In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol. 23:1558-1568. doi:10.1128/MCB.23.5.1558-1568. 2003
13. Gadal, O., S. Mariotte-Labarre, S. Chédin, E. Quemeneur, C. Carles, A. Sentenac, and P. Thuriaux. 1997. A34.5, a nonessential component of yeast RNA polymerase I, cooperates with subunit A14 and DNA topoisomerase I to produce a functional rRNA synthesis machine. Mol. Cell. Biol. 17:1787-1795.
14. Gadal, O., D. Strauss, E. Petfalski, P.E. Gleizes, N. Gas, D. Tollervey, and E. Hurt. 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. doi:10.1083/jcb.200111039
15. Galy, V., O. Gadal, M. Fromont-Racine, A. Romano, A. Jacquier, and U. Nehrbass. 2004. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell. 116:63-73. doi:10.1016/S0092-8674(03)01026-2
16. Geiger, S.R., K. Lorenzen, A. Schreieck, P. Hanecker, D. Kostrewa, A.J. Heck, and P. Cramer. 2010. RNA polymerase I contains a TFIIF-related DNA-binding subcomplex. Mol. Cell. 39:583-594. doi:10.1016/j.molcel.2010.07.028
17. Hanada, K., C.Z. Song, K. Yamamoto, K. Yano, Y. Maeda, K. Yamaguchi, and M. Muramatsu. 1996. RNA polymerase I associated factor 53 binds to the nucleolar transcription factor UBF and functions in specific rDNA transcription. EMBO J. 15:2217-2226.
18. Henras, A., C. Dez, J. Noaillac-Depeyre, Y. Henry, and M. Caizergues-Ferrer. 2001. Accumulation of H/ACA snoRNPs depends on the integrity of the conserved central domain of the RNA-binding protein Nhp2p. Nucleic Acids Res. 29:2733-2746. doi:10.1093/nar/29.13.2733
19. Hernandez-Verdun, D., P. Roussel, and J. Gébrane-Younès. 2002. Emerging concepts of nucleolar assembly. J. Cell Sci. 115:2265-2270.
20. Huet, J., J.M. Buhler, A. Sentenac, and P. Fromageot. 1975. Dissociation of two polypeptide chains from yeast RNA polymerase A. Proc. Natl. Acad. Sci. USA. 72:3034-3038. doi:10.1073/pnas.72.8.3034
21. Kuhn, C.D., S.R. Geiger, S. Baumli, M. Gartmann, J. Gerber, S. Jennebach, T. Mielke, H. Tschochner, R. Beckmann, and P. Cramer. 2007. Functional architecture of RNA polymerase I. Cell. 131:1260-1272. doi:10.1016/j.cell.2007. 10.051
22. Künzler, M., and E.C. Hurt. 1998. Cse1p functions as the nuclear export receptor for importin alpha in yeast. FEBS Lett. 433:185-190. doi:10.1016/S0014-5793(98)00892-8
23. Kwapisz, M., F. Beckouët, and P. Thuriaux. 2008. Early evolution of eukaryotic DNA-dependent RNA polymerases. Trends Genet. 24:211-215. doi:10.1016/j.tig.2008.02.002
24. Lechertier, T., V. Sirri, D. Hernandez-Verdun, and P. Roussel. 2007. A B23-interacting sequence as a tool to visualize protein interactions in a cellular context. J. Cell Sci. 120:265-275. doi:10.1242/jcs.03345
25. Liljelund, P., S. Mariotte, J.M. Buhler, and A. Sentenac. 1992. Characterization and mutagenesis of the gene encoding the A49 subunit of RNA polymerase A in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 89:9302-9305. doi:10.1073/pnas.89.19.9302
26. Miller, O.L. Jr., and B.R. Beatty. 1969. Visualization of nucleolar genes. Science. 164:955-957. doi:10.1126/science.164.3882.955
27. Minakhin, L., S. Bhagat, A. Brunning, E.A. Campbell, S.A. Darst, R.H. Ebright, and K. Severinov. 2001. Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. Proc. Natl. Acad. Sci. USA. 98:892-897. doi:10.1073/pnas.98.3.892
28. Misteli, T. 2001. The concept of self-organization in cellular architecture. J. Cell Biol. 155:181-185. doi:10.1083/jcb.200108110
29. Nakagawa, K., K. Hisatake, Y. Imazawa, A. Ishiguro, M. Matsumoto, L. Pape, A. Ishihama, and Y. Nogi. 2003. The fission yeast RPA51 is a functional homolog of the budding yeast A49 subunit of RNA polymerase I and required for maximizing transcription of ribosomal DNA. Genes Genet. Syst. 78:199-209. doi:10.1266/ggs.78.199
30. 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. doi:10.1073/pnas.88.9.3962 (Pubitemid 21916744)
31. 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. doi:10.1083/jcb.143.1.23
32. Osheim, Y.N., S.L. French, M.L. Sikes, and A.L. Beyer. 2009. Electron microscope visualization of RNA transcription and processing in Saccharomyces cerevisiae by Miller chromatin spreading. Methods Mol. Biol. 464: 55-69. doi:10.1007/978-1-60327-461-6-4
33. Panov, K.I., T.B. Panova, O. Gadal, K. Nishiyama, T. Saito, J. Russell, and J.C. Zomerdijk. 2006. RNA polymerase I-specific subunit CAST/hPAF49 has a role in the activation of transcription by upstream binding factor. Mol. Cell. Biol. 26:5436-5448. doi:10.1128/MCB.00230-06
34. Pettersen, E.F., T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612. doi:10.1002/jcc.20084
35. Reimer, G., I. Raska, E.M. Tan, and U. Scheer. 1987. Human autoantibodies: probes for nucleolus structure and function. Virchows. Arch. B Cell Pathol. Incl. Mol. Pathol. 54:131-143. doi:10.1007/BF02899205
36. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Séraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032. doi:10.1038/13732
37. Samkurashvili, I., and D.S. Luse. 1998. Structural changes in the RNA polymerase II transcription complex during transition from initiation to elongation. Mol. Cell. Biol. 18:5343-5354.
38. Schneider, D.A., A. Michel, M.L. Sikes, L. Vu, J.A. Dodd, S. Salgia, Y.N. Osheim, A.L. Beyer, and M. Nomura. 2007. Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol. Cell. 26:217-229. doi:10.1016/j.molcel.2007.04.007
39. Sikorski, R.S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
40. Trumtel, S., I. Léger-Silvestre, P.E. Gleizes, F. Teulières, and N. Gas. 2000. Assembly and functional organization of the nucleolus: ultrastructural analysis of Saccharomyces cerevisiae mutants. Mol. Biol. Cell. 11:2175-2189.
41. Van Mullem, V., M. Wery, X. De Bolle, and J. Vandenhaute. 2003. Construction of a set of Saccharomyces cerevisiae vectors designed for recombinational cloning. Yeast. 20:739-746. doi:10.1002/yea.999
42. Wai, H.H., L. Vu, M. Oakes, and M. Nomura. 2000. Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo. Nucleic Acids Res. 28:3524-3534. doi:10.1093/nar/28.18.3524
43. Wang, D., D.A. Bushnell, K.D. Westover, C.D. Kaplan, and R.D. Kornberg. 2006. Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell. 127:941-954. doi:10.1016/j.cell.2006.11.023
44. Yamamoto, K., M. Yamamoto, K. Hanada, Y. Nogi, T. Matsuyama, and M. Muramatsu. 2004. Multiple protein-protein interactions by RNA polymerase I-associated factor PAF49 and role of PAF49 in rRNA transcription. Mol. Cell. Biol. 24:6338-6349. doi:10.1128/MCB.24.14.6338-6349.2004
45. Yamazaki, T., Y. Hamano, H. Tashiro, K. Itoh, H. Nakano, S. Miyatake, and T. Saito. 1999. CAST, a novel CD3epsilon-binding protein transducing activation signal for interleukin-2 production in T cells. J. Biol. Chem. 274:18173-18180. doi:10.1074/jbc.274.26.18173