Microarray detection of novel nuclear RNA substrates for the exosome

Yeast

Volumn 23, Issue 6, 2006, Pages 439-454

  Houalla, Rym ^a   Devaux, Frédéric ^b   Fatica, Alessandra ^c   Kufel, Joanna ^d   Barrass, David ^a   Torchet, Claire ^e   Tollervey, David ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF WARSAW   (Poland)

^e INSTITUT JACQUES MONOD   (France)

Author keywords

Microarray; mRNA surveillance; RNA degradation; Yeast

Indexed keywords

FUNGAL RNA; MESSENGER RNA; NRD1 PROTEIN; NUCLEAR RNA; RNA BINDING PROTEIN; SMALL NUCLEAR RNA; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; AUTOREGULATION; BINDING SITE; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC HETEROGENEITY; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; NORTHERN BLOTTING; OPEN READING FRAME; PREDICTION; PRIORITY JOURNAL; RNA MICROARRAY; RNA TRANSCRIPTION; TEMPERATURE MEASUREMENT; TRANSCRIPTION REGULATION;

BLOTTING, NORTHERN; EXORIBONUCLEASES; FUNGAL PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RIBONUCLEOPROTEINS; RNA, FUNGAL; RNA, NUCLEAR; YEASTS;

EID: 33744474553     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1369     Document Type: Article

References (61)

1. Abou Elela S, Ares M Jr. 1998. Depletion of yeast RNase III blocks correct U2 3′ end formation and results in polyadenylated but functional U2 snRNA. EMBO J 17: 3738-3746.
2. Abou Elela S, Igel H, Ares M Jr. 1996. RNase III cleaves eukaryotic preribosomal RNA at a U3 snoRNP-dependent site. Cell 85: 115-124.
3. Allmang C, Kufel J, Chanfreau G et al. 1999. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410.
4. Anderson JSJ, Parker RP. 1998. The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J 17: 1497-1506.
5. Andrulis ED, Werner J, Nazarian A et al. 2002. The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420: 837-841.
6. Baudin A, Ozier-Kalogeropoulos O, Denouel A et al. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21: 3329-3330.
7. Beltrame M, Tollervey D. 1992. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J 11: 1531-1542.
8. Benard L, Carroll K, Valle RC, Wickner RB. 1998. Ski6p is a homolog of RNA-processing enzymes that affects translation of non-poly(A) mRNAs and 60S ribosomal subunit biogenesis. Mol Cell Biol 18: 2688-2696.
9. Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102: 765-775.
10. Briggs MW, Burkard KT, Butler JS. 1998. Rrp6p, the yeast homologue of the human PM-Sc1 100 kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J Biol Chem 273: 13255-13263.
11. Chanfreau G, Elela SA, Ares M Jr, Guthrie C. 1997. Alternative 3′ end processing of U5 snRNA by RNase III. Genes Dev 11: 2741-2751.
12. Chanfreau G, Legrain P, Jacquier A. 1998a. Yeast RNase III as a key processing enzyme in small nucleolar RNAs metabolism. J Mol Biol 284: 975-988.
13. Chanfreau G, Rotondo G, Legrain P, Jacquier A. 1998b. Processing of a dicistronic small nucleolar RNA precursor by the RNA endonuclease Rnt1. EMBO J 17: 3726-3737.
14. Chen CY, Gherzi R, Ong SE et al. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464.
15. Connelly S, Manley JL. 1989. RNA polymerase II transcription termination is mediated specifically by protein binding to a CCAAT box sequence. Mol Cell Biol 9: 5254-5259.
16. Conrad NK, Wilson SM, Steinmetz EJ, et al. 2000. A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II. Genetics 154: 557-571.
17. Das B, Butler JS, Sherman F. 2003. Degradation of normal mRNA in the nucleus of Saccharomyces cerevisiae. Mol Cell Biol 23: 5502-5515.
18. Davis CA, Ares MJ. 2006. Accumulation of unstable promoter-associated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 103: 3262-3267.
19. Dheur S, Vole TA, Voisinet-Hakil F et al. 2003. Pti1p and Ref2p found in association with the mRNA 3′ end formation complex direct snoRNA maturation. EMBO J 22: 2831-2840.
20. Dichtl B, Blank D, Ohnacker M et al. 2002. A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol Cell 10: 1139-1150.
21. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
22. Ganem C, Devaux F, Torchet C et al. 2003. Ssu72 is a phosphatase essential for transcription termination of snoRNAs and specific mRNAs in yeast. EMBO J 22: 1588-1598.
23. Gavin AC, Bosche M, Krause R, et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
24. Gietz D, St Jean A, Woods RA, Schiestl RH. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20: 1425.
25. Golfier G, Tran Dang M, Dauphinot L et al. 2004. VARAN: a web server for VARiability ANalysis of DNA microarray experiments. Bioinformatics (e-publication ahead of print).
26. Haile S, Estevez AM, Clayton C. 2003. A role for the exosome in the in viro degradation of unstable mRNAs. RNA 9: 1491-1501.
27. Hilleren P, McCarthy T, Rosbash M, Parker R, Jensen TH. 2001. Quality control of mRNA 3′-end processing is linked to the nuclear exosome. Nature 413: 538-542.
28. Hughes TR, Marton MJ, Jones AR, et al. 2000. Functional discovery via a compendium of expression profiles. Cell 102: 109-126.
29. Kadowaki T, Schneiter R, Hitomi M, Tartakoff AM. 1995. Mutations in nucleolar proteins lead to nucleolar accumulation of polyA RNA in Saccharomyces cerevisiae. Mol Biol Cell 6: 1103-1110.
30. Krogan NJ, Peng WT, Cagney G et al. 2004. High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell 13: 225-239.
31. Kuai L, Das B, Sherman F. 2005. A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102: 13962-13967.
32. Kufel J, Dichtl B, Tollervey D. 1999. Yeast Rnt1p is required for cleavage of the pre-ribosomal RNA in the 3′ ETS but not the 5′ ETS. RNA 5: 909-917.
33. Lafontaine D, Tollervey D. 1996. One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins. Nucleic Acids Res 24: 3469-3472.
34. Lai WS, Carballo E, Strum JR et al. 1999. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311-4323.
35. Lee JM, Greenleaf AL. 1991. CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr 1: 149-167.
36. Mitchell P, Petfalski E, Houalla R et al. 2003. Rrp47p is an exosome-associated protein required for the 3′ processing of stable RNAs. Mol Cell Biol 23: 6982-6992.
37. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′ 5′ exoribonuclease activities. Cell 91: 457-466.
38. Mnaimneh S, Davierwala AP, Haynes J et al. 2004. Exploration of essential gene functions via titratable promoter alleles. Cell 118: 31-44.
39. Mukherjee D, Gao M, O'Connor JP et al. 2002. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J 21: 165-174.
40. Nedea E, He X, Kim M et al. 2003. Organization and function of APT, a subcomplex of the yeast cleavage and polyadenylation factor involved in the formation of mRNA and small nucleolar RNA 3′-ends. J Biol Chem 278: 33000-33010.
41. Olivas WM, Muhlrad D, Parker R. 1997. Analysis of the yeast genome: identification of new non-coding and small ORF-containing RNAs. Nucleic Acids Res 25: 4619-4625.
42. Peng WT, Robinson MD, Mnaimneh S et al. 2003. A panoramic view of yeast noncoding RNA processing. Cell 113: 919-933.
43. Proudfoot NJ. 1989. How RNA polymerase II terminates transcription in higher eukaryotes. Trends Biochem Sci 14: 105-110.
44. Proudfoot NJ, Furger A, Dye MJ. 2002. Integrating mRNA processing with transcription. Cell 108: 501-512.
45. Roth KM, Wolf MK, Rossi M, Butler JS. 2005. The nuclear exosome contributes to autogenous control of NAB2 mRNA levels. Mol Cell Biol 25: 1577-1585.
46. Seipelt RL, Zheng B, Asuru A, Rymond BC. 1999. U1 snRNA is cleaved by RNase III and processed through an Sm site-dependent pathway. Nucleic Acids Res 27: 587-595.
47. Steinmetz EJ, Brow DA. 1996. Repression of gene expression by an exogenous sequence element acting in concert with a heterogeneous nuclear ribonucleoprotein-like protein, Nrd1, and the putative helicase Sen1. Mol Cell Biol 16: 6993-7003.
48. Steinmetz EJ, Brow DA. 1998. Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc Natl Acad Sci USA 95: 6699-6704.
49. Steinmetz EJ, Brow DA. 2003. Ssu72 protein mediates both poly(A)-coupled and poly(A)-independent termination of RNA polymerase II transcription. Mol Cell Biol 23: 6339-6349.
50. Steinmetz EJ, Conrad NK, Brow DA, Corden JL. 2001. RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413: 327-331.
51. Tollervey D. 1987. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J 6: 4169-4175.
52. Torchet C, Bousquet-Antonelli C, Milligan L et al. 2002. Processing of 3′ extended read-through transcripts by the exosome can generate functional mRNAs. Mol Cell 9: 1285-1296.
53. Tran H, Schilling M, Wirbelauer C, Hess D, Nagamine Y. 2004. Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Mol Cell 13: 101-111.
54. Ursic D, Chinchilla K, Finkel JS, Culbertson MR. 2004. Multiple protein/ protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic Acids Res 32: 2441-2452.
55. Ursic D, Himmel KL, Gurley KA, Webb F, Culbertson MR. 1997. The yeast SEN1 gene is required for the processing of diverse RNA classes. Nucleic Acids Res 25: 4778-4785.
56. van Helden J, Andre B, Collado-Vides J. 2000. A web site for the computational analysis of yeast regulatory sequences. Yeast 16: 177-187.
57. van Hoof A, Lennertz P, Parker R. 2000. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 20: 441-452.
58. Vasiljeva L, Buratowski S. 2006. Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Mol Cell 21: 239-248.
59. Wyers F, Rougemaille M, Badis G et al. 2005. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
60. Yuryev A, Patturajan M, Litingtung Y et al. 1996. The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc Natl Acad Sci USA 93: 6975-6980.
61. Zanchin NI, Goldfarb DS. 1999. The exosome subunit Rrp43p is required for the efficient maturation of 5.8S, 18S and 25S rRNA. Nucleic Acids Res 27: 1283-1288.