A yeast exosome cofactor, Mpp6, functions in RNA surveillance and in the degradation of noncoding RNA transcripts

Molecular and Cellular Biology

Volumn 28, Issue 17, 2008, Pages 5446-5457

  Milligan, Laura ^c   Decourty, Laurence ^a   Saveanu, Cosmin ^a   Rappsilber, Juri ^c   Ceulemans, Hugo ^b   Jacquier, Alain ^a   Tollervey, David ^c  

^a CNRS   (France)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MPP6 COFACTOR; PROTEIN; RIBOSOME DNA; RIBOSOME RNA; RNA BINDING PROTEIN; SPACER DNA; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; EXOSOME; GENE; GENE INTERACTION; HETEROCHROMATIN; MPP6 GENE; NONHUMAN; PRIORITY JOURNAL; RNA DEGRADATION; RNA METABOLISM; RNA TRANSCRIPTION; RRP47 GENE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CELL NUCLEUS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; RNA, UNTRANSLATED; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 50249112157     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00463-08     Document Type: Article

References (62)

1. Allmang, C., P. Mitchell, E. Petfalski, and D. Tollervey. 2000. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 28:1684-1691.
2. Allmang, C., E. Petfalski, A. Podtelejnikov, M. Mann, D. Tollervey, and P. Mitchell. 1999. The yeast exosome and human PM-Scl are related complexes of 3′→5′ exonucleases. Genes Dev. 13:2148-2158.
3. Araki, Y., S. Takahashi, T. Kobayashi, H. Kajiho, S. Hoshino, and T. Katada. 2001. Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J. 20:4684-4693.
4. Arigo, J. T., D. E. Eyler, K. L. Carroll, and J. L. Corden. 2006. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23:841-851.
5. 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.
6. Berretta, J., M. Pinskaya, and A. Morillon. 2008. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev. 22:615-626.
7. Birney, E., J. A. Stamatoyannopoulos, A. Dutta, R. Guigo, T. R. Gingeras, E. H. Margulies, Z. Weng, M. Snyder, E. T. Dermitzakis, R. E. Thurman, M. S. Kuehn, C. M. Taylor, S. Neph, C. M. Koch, S. Asthana, A. Malhotra, I. Adzhubei, J. A. Greenbaum, R. M. Andrews, P. Flicek, P. J. Boyle, H. Cao, N. P. Carter, G. K. Clelland, S. Davis, N. Day, P. Dhami, S. C. Dillon, M. O. Dorschner, H. Fiegler, P. G. Giresi, J. Goldy, M. Hawrylycz, A. Haydock, R. Humbert, K. D. James, B. E. Johnson, E. M. Johnson, T. T. Frum, E. R. Rosenzweig, N. Karnani, K. Lee, G. C. Lefebvre, P. A. Navas, F. Neri, S. C. Parker, P. J. Sabo, R. Sandstrom, A. Shafer, D. Vetrie, M. Weaver, S. Wilcox, M. Yu, F. S. Collins, J. Dekker, J. D. Lieb, T. D. Tullius, G. E. Crawford, S. Sunyaev, W. S. Noble, I. Dunham, F. Denoeud, A. Reymond, P. Kapranov, J. Rozowsky, D. Zheng, R. Castelo, A. Frankish, J. Harrow, S. Ghosh, A. Sandelin, I. L. Hofacker, R. Baertsch, D. Keefe, S. Dike, J. Cheng, H. A. Hirsch, E. A. Sekinger, J. Lagarde, J. F. Abril, A. Shahab, C. Flamm, C. Fried, J. Hackermuller, J. Hertel, M. Lindemeyer, K. Missal, A. Tanzer, S. Washietl, J. Korbel, O. Emanuelsson, J. S. Pedersen, N. Holroyd, R. Taylor, D. Swarbreck, N. Matthews, M. C. Dickson, D. J. Thomas, M. T. Weirauch, J. Gilbert, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799-816.
8. Bousquet-Antonelli, C., C. Presutti, and D. Tollervey. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102:765-775.
9. Brachmann, C. B., A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, and J. D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
10. Buhler, M., W. Haas, S. P. Gygi, and D. Moazed. 2007. RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129:707-721.
11. Chavez, S., T. Beilharz, A. G. Rondon, H. Erdjument-Bromage, P. Tempst, J. Q. Svejstrup, T. Lithgow, and A. Aguilera. 2000. A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J. 19:5824-5834.
12. Ciais, D., M. Bohnsack, and D. Tollervey. 2008. The mRNA encoding the yeast ARE-binding protein Cth2 is generated by a novel 3′ processing pathway. Nucleic Acids Res. 36:3075-3084.
13. Conrad, N. K., S. M. Wilson, E. J. Steinmetz, M. Patturajan, D. A. Brow, M. S. Swanson, and J. L. Corden. 2000. A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II. Genetics 154:557-571.
14. 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 105:5816-5821.
15. Dez, C., M. Dlakic, and D. Tollervey. 2007. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA 13:1516-1527.
16. Dez, C., J. Houseley, and D. Tollervey, 2006. Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 25:1534-1546.
17. Egecioglu, D. E., A. K. Henras, and G. F. Chanfreau. 2006. Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12:26-32.
18. Fatica, A., A. D. Cronshaw, M. Dlakic, and D. Tollervey. 2002. Ssf1p prevents premature processing of an early pre-60S ribosomal particle. Mol. Cell 9:341-351.
19. Ghaemmaghami, S., W. K. Huh, K. Bower, R. W. Howson, A. Belle, N. Dephoure, E. K. O'Shea, and J. S. Weissman. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
20. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K.-D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C.-Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
21. Houseley, J., K. Kotovic, A. El Hage, and D. Tollervey. 2007. Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J. 26:4996-5006.
22. Houseley, J., J. LaCava, and D. Tollervey. 2006. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7:529-539.
23. Houseley, J., and D. Tollervey. 2008. The nuclear RNA surveillance machinery: the link between ncRNAs and genome structure in budding yeast. Biochim. Biophys. Acta 1779:239-246.
24. Houseley, J., and D. Tollervey. 2006. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep. 7:205-211.
25. Ishihama, Y., J. Rappsilber, J. S. Andersen, and M. Mann. 2002. Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A 979:233-239.
26. Jonson, L., J. F. Rehfeld, and A. H. Johnsen. 2004. Enhanced peptide secretion by gene disruption of CYM1, a novel protease in Saccharomyces cerevisiae. Eur. J. Biochem. 271:4788-4797.
27. Kadowaki, T., R. Schneiter, M. Hitomi, and A. M. Tartakoff. 1995. Mutations in nucleolar proteins lead to nucleolar accumulation of polyA+ RNA in Saccharomyces cerevisiae. Mol. Biol. Cell 6:1103-1110.
28. LaCava, J., J. Houseley, C. Saveanu, E. Petfalski, E. Thompson, A. Jacquier, and D. Tollervey. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 21:713-724.
29. Lebreton, A., C. Saveanu, L. Decourty, J. C. Rain, A. Jacquier, and M. Fromont-Racine. 2006. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 173:349-360.
30. Libri, D., K. Dower, J. Boulay, R. Thomsen, M. Rosbash, and T. H. Jensen. 2002. Interactions between mRNA export commitment, 3′-end quality control, and nuclear degradation. Mol. Cell. Biol. 22:8254-8266.
31. Minvielle-Sebastia, L., P. J. Preker, and W. Keller. 1994. RNA14 and RNA15 proteins as components of a yeast pre-mRNA 3′-end processing factor. Science 266:1702-1705.
32. Mitchell, P., E. Petfalski, R. Houalla, A. Podtelejnikov, M. Mann, and D. Tollervey. 2003. Rrp47p is an exosome-associated protein required for the 3′ processing of stable RNAs. Mol. Cell. Biol. 23:6982-6992.
33. Oeffinger, M., M. Dlakic, and D. Tollervey. 2004. A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 18:196-209.
34. Olesen, J. R., D. Libri, and T. H. Jensen. 2005. A link between transcription and mRNP quality in Saccharomyces cerevisiae. RNA Biol. 2:45-48.
35. Peng, W. T., M. D. Robinson, S. Mnaimneh, N. J. Krogan, G. Cagney, Q. Morris, A. P. Davierwala, J. Grigull, X. Yang, W. Zhang, N. Mitsakakis, O. W. Ryan, N. Datta, V. Jojic, C. Pal, V. Canadien, D. Richards, B. Beattie, L. F. Wu, S. J. Altschuler, S. Roweis, B. J. Frey, A. Emili, J. F. Greenblatt, and T. R. Hughes. 2003. A panoramic view of yeast noncoding RNA processing. Cell 113:919-933.
36. Plumpton, M., M. McGarvey, and J. D. Beggs. 1994. A dominant negative mutation in the conserved RNA helicase motif "SAT" causes splicing factor PRP2 to stall in spliceosomes. EMBO J. 13:879-887.
37. Rappsilber, J., Y. Ishihama, and M. Mann. 2003. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75:663-670.
38. Rexach, M., and G. Blobel. 1995. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83:683-692.
39. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Seraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
40. Rinn, J. L., M. Kertesz, J. K. Wang, S. L. Squazzo, X. Xu, S. A. Brugmann, L. H. Goodnough, J. A. Helms, P. J. Farnham, E. Segal, and H. Y. Chang. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311-1323.
41. Rougemaille, M., R. K. Gudipati, J. R. Olesen, R. Thomsen, B. Seraphin, D. Libri, and T. H. Jensen. 2007. Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J. 26:2317-2326.
42. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Schilders, G., R. Raijmakers, J. M. Raats, and G. J. Pruijn. 2005. MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res. 33:6795-6804.
44. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
45. Stead, J. A., J. L. Costello, M. J. Livingstone, and P. Mitchell. 2007. The PMC2NT domain of the catalytic exosome subunit Rrp6p provides the interface for binding with its cofactor Rrp47p, a nucleic acid-binding protein. Nucleic Acids Res. 35:5556-5567.
46. Steinmetz, E. J., N. K. Conrad, D. A. Brow, and J. L. Corden. 2001. RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413:327-331.
47. Steinmetz, E. J., C. L. Warren, J. N. Kuehner, B. Panbehi, A. Z. Ansari, and D. A. Brow. 2006. Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 24:735-746.
48. Struhl, K. 2007. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat. Struct. Mol. Biol. 14:103-105.
49. Teigelkamp, S., M. McGarvey, M. Plumpton, and J. D. Beggs. 1994. The splicing factor PRP2, a putative RNA helicase, interacts directly with pre-mRNA. EMBO J. 13:888-897.
50. Tollervey, D., and I. W. Mattaj. 1987. Fungal small nuclear ribonucleoproteins share properties with plant and vertebrate U-snRNPs. EMBO J. 6:469-476.
51. Torchet, C., C. Bousquet-Antonelli, L. Milligan, E. Thompson, J. Kufel, and D. Tollervey. 2002. Processing of 3′ extended read-through transcripts by the exosome can generate functional mRNAs. Mol. Cell 9:1285-1296.
52. Vanacova, S., J. Wolf, G. Martin, D. Blank, S. Dettwiler, A. Friedlein, H. Langen, G. Keith, and W. Keller. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3:e189.
53. van Hoof, A., P. Lennertz, and R. Parker. 2000. Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J. 19:1357-1365.
54. van Hoof, A., R. R. Staples, R. E. Baker, and R. Parker. 2000. Function of the Ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol. Cell. Biol. 20:8230-8243.
55. Vasiljeva, L., and S. Buratowski. 2006. Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Mol. Cell 21:239-248.
56. Vasiljeva, L., M. Kim, N. Terzi, L. M. Soares, and S. Buratowski. 2008. Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol. Cell 29:313-323.
57. Venema, J., and D. Tollervey. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33:261-311.
58. Venema, J., and D. Tollervey. 1996. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO J. 15:5701-5714.
59. Wang, S.-W., A. L. Stevenson, S. E. Kearsey, S. Watt, and J. Bähler. 2008. Global role for polyadenylation-assisted nuclear RNA degradation in post-transcriptional gene silencing. Mol. Cell. Biol. 28:656-665.
60. Wu, K., P. Wu, and J. P. Aris. 2001. Nucleolar protein Nop12p participates in synthesis of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res. 29:2938-2949.
61. Wyers, F., M. Rougemaille, G. Badis, J.-C. Rousselle, M.-E. Dufour, J. Boulay, B. Régnault, F. Devaux, A. Namane, B. Séraphin, D. Libri, and A. Jacquier. 2005. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121:725-737.
62. Zenklusen, D., P. Vinciguerra, J. C. Wyss, and F. Stutz. 2002. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol. Cell. Biol. 22:8241-8253.