Origins and activities of the eukaryotic exosome

Journal of Cell Science

Volumn 122, Issue 10, 2009, Pages 1487-1494

  Lykke Andersen, Søren ^a   Brodersen, Ditiev E ^a   Jensen, Torben Heick ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Exosome function; Exosome structure; RNA exosome

Indexed keywords

CELL PROTEIN; EXONUCLEASE; MESSENGER RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN RRP44; RNA; RNA HELICASE; UNCLASSIFIED DRUG; BACTERIAL RNA; ENDONUCLEASE; FUNGAL RNA; RRP44 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

CELL FUNCTION; CELL NUCLEUS; CELL STRUCTURE; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; EUKARYOTE; EXOSOME; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; NOTE; PRIORITY JOURNAL; PROKARYOTE; QUALITY CONTROL; RIBOSOME; RNA DEGRADATION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; ANIMAL; ENZYMOLOGY; EUKARYOTIC CELL; GENETIC TRANSCRIPTION; METABOLISM; PROKARYOTIC CELL; REVIEW;

EUKARYOTA; PROKARYOTA;

ANIMALS; CYTOPLASM; ENDONUCLEASES; EUKARYOTIC CELLS; EXONUCLEASES; EXOSOMES; HUMANS; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROKARYOTIC CELLS; RIBOSOMES; RNA; RNA HELICASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 67649910424     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.047399     Document Type: Note

References (124)

1. Allmang, C., Kufel, J., Chanfreau, G., Mitchell, P., Petfalski, E. and Tollervey, D. (1999a). Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18, 5399-5410.
2. Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D. and Mitchell, P. (1999b). The yeast exosome and human PM-Scl are related complexes of 3′→5′ exonucleases. Genes Dev. 13, 2148-2158.
3. Anderson, J. S. and Parker, R. P. (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.
4. Araki, Y., Takahashi, S., Kobayashi, T., Kajiho, H., Hoshino, S. and Katada, T. (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.
5. Arcus, V. L., Backbro, K., Roos, A., Daniel, E. L. and Baker, E. N. (2004). Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J. Biol. Chem. 279, 16471-16478.
6. Arigo, J. T., Eyler, D. E., Carroll, K. L. and Corden, J. L. (2006). Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23, 841-851.
7. Baillat, D., Hakimi, M. A., Naar, A. M., Shilatifard, A., Cooch, N. and Shiekhattar, R. (2005). Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123, 265-276.
8. Benard, L., Carroll, K., Valle, R. C., Masison, D. C. and Wickner, R. B. (1999). The ski7 antiviral protein is an EF1-alpha homolog that blocks expression of non-Poly(A) mRNA in Saccharomyces cerevisiae. J. Virol. 73, 2893-2900.
9. Briggs, M. W., Burkard, K. T. and Butler, J. S. (1998). Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J. Biol. Chem. 273, 13255-13263.
10. Brown, J. T., Bai, X. and Johnson, A. W. (2000). The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6, 449-457.
11. Burkard, K. T. and Butler, J. S. (2000). A nuclear 3′-5′ exonuclease involved in mRNA degradation interacts with Poly(A) polymerase and the hnRNA protein Npl3p. Mol. Cell. Biol. 20, 604-616.
12. Buttner, K., Wenig, K. and Hopfner, K. P. (2005). Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol. Cell 20, 461-471.
13. Callaghan, A. J., Marcaida, M. J., Stead, J. A., McDowall, K. J., Scott, W. G. and Luisi, B. F. (2005). Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437, 1187-1191.
14. Carpousis, A. J. (2007). The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61, 71-87.
15. Carroll, K. L., Pradhan, D. A., Granek, J. A., Clarke, N. D. and Corden, J. L. (2004). Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol. Cell. Biol. 24, 6241-6252.
16. Carroll, K. L., Ghirlando, R., Ames, J. M. and Corden, J. L. (2007). Interaction of yeast RNA-binding proteins Nrd1 and Nab3 with RNA polymerase II terminator elements. RNA 13, 361-373.
17. Chekanova, J. A., Shaw, R. J., Wills, M. A. and Belostotsky, D. A. (2000). Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8 S rRNA processing and mRNA decay defects of the yeast ski6 mutant and is found in an exosome-sized complex in plant and yeast cells. J. Biol. Chem. 275, 33158-33166.
18. Chekanova, J. A., Gregory, B. D., Reverdatto, S. V., Chen, H., Kumar, R., Hooker, T., Yazaki, J., Li, P., Skiba, N., Peng, Q. et al. (2007). Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131, 1340-1353.
19. Chen, C. Y., Gherzi, R., Ong, S. E., Chan, E. L., Raijmakers, R., Pruijn, G. J., Stoecklin, G., Moroni, C., Mann, M. and Karin, M. (2001). AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107, 451-464.
20. Cheng, Z. F. and Deutscher, M. P. (2002). Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 277, 21624-21629.
21. Cheng, Z. F. and Deutscher, M. P. (2003). Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl. Acad. Sci. USA 100, 6388-6393.
22. Clement, S. L. and Lykke-Andersen, J. (2006). No mercy for messages that mess with the ribosome. Nat. Struct. Mol. Biol. 13, 299-301.
23. Conrad, N. K., Wilson, S. M., Steinmetz, E. J., Patturajan, M., Brow, D. A., Swanson, M. S. and Corden, J. L. (2000). A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II. Genetics 154, 557-571.
24. Davis, C. A. and Ares, M., Jr (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.
25. Deana, A., Celesnik, H. and Belasco, J. G. (2008). The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal. Nature 451, 355-358.
26. Deutscher, M. P. and Reuven, N. B. (1991). Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. USA 88, 3277-3280.
27. Deutscher, M. P., Marshall, G. T. and Cudny, H. (1988). RNase PH: an Escherichia coli phosphate-dependent nuclease distinct from polynucleotide phosphorylase. Proc. Natl. Acad. Sci. USA 85, 4710-4714.
28. Dez, C., Houseley, J. and Tollervey, D. (2006). Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 25, 1534-1546.
29. Doma, M. K. and Parker, R. (2006). Revenge of the NRD: preferential degradation of nonfunctional eukaryotic rRNA. Dev. Cell 11, 757-758.
30. Doma, M. K. and Parker, R. (2007). RNA quality control in eukaryotes. Cell 131, 660-668.
31. Dziembowski, A., Lorentzen, E., Conti, E. and Seraphin, B. (2007). A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 14, 15-22.
32. Eberle, A. B., Lykke-Andersen, S., Mühlemann, O. and Jensen, T. H. (2008). SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16, 49-55.
33. Egecioglu, D. E., Henras, A. K. and Chanfreau, G. F. (2006). Contributions of Trf4p-and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12, 26-32.
34. Evguenieva-Hackenberg, E., Walter, P., Hochleitner, E., Lottspeich, F. and Klug, G. (2003). An exosome-like complex in Sulfolobus solfataricus. EMBO Rep. 4, 889-893.
35. Fatica, A., Tollervey, D. and Dlakic, M. (2004). PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 10, 1698-1701.
36. Frazao, C., McVey, C. E., Amblar, M., Barbas, A., Vonrhein, C., Arraiano, C. M. and Carrondo, M. A. (2006). Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110-114.
37. Frischmeyer, P. A., van Hoof, A., O'Donnell, K., Guerrerio, A. L., Parker, R. and Dietz, H. C. (2002). An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295, 2258-2261.
38. Gatfield, D. and Izaurralde, E. (2004). Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429, 575-578.
39. Glavan, F., Behm-Ansmant, I., Izaurralde, E. and Conti, E. (2006). Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25, 5117-5125.
40. Grishin, N. V. (2001). KH domain: one motif, two folds. Nucleic Acids Res. 29, 638-643.
41. Guo, X., Ma, J., Sun, J. and Gao, G. (2007). The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc. Natl. Acad. Sci. USA 104, 151-156.
42. Hernandez, H., Dziembowski, A., Taverner, T., Seraphin, B. and Robinson, C. V. (2006). Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 7, 605-610.
43. Hilleren, P., McCarthy, T., Rosbash, M., Parker, R. and Jensen, T. H. (2001). Quality control of mRNA 3′-end processing is linked to the nuclear exosome. Nature 413, 538-542.
44. Houseley, J. and Tollervey, D. (2006). Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep. 7, 205-211.
45. Houseley, J., Kotovic, K., El Hage, A. and Tollervey, D. (2007). Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J. 26, 4996-5006.
46. Huntzinger, E., Kashima, I., Fauser, M., Sauliere, J. and Izaurralde, E. (2008). SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14, 2609-2617.
47. Ishii, R., Nureki, O. and Yokoyama, S. (2003). Crystal structure of the tRNA processing enzyme RNase PH from Aquifex aeolicus. J. Biol. Chem. 278, 32397-32404.
48. Kadaba, S., Krueger, A., Trice, T., Krecic, A. M., Hinnebusch, A. G. and Anderson, J. (2004). Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 18, 1227-1240.
49. Kadaba, S., Wang, X. and Anderson, J. T. (2006). Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. RNA 12, 508-521.
50. Kiss, T., Fayet, E., Jady, B. E., Richard, P. and Weber, M. (2006). Biogenesis and intranuclear trafficking of human box C/D and H/ ACA RNPs. Cold Spring Harb. Symp. Quant. Biol. 71, 407-417.
51. Kopcewicz, K. A., O'Rourke, T. W. and Reines, D. (2007). Metabolic regulation of IMD2 transcription and an unusual DNA element that generates short transcripts. Mol. Cell. Biol. 27, 2821-2829.
52. Kuai, L., Fang, F., Butler, J. S. and Sherman, F. (2004). Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101, 8581-8586.
53. Kuehner, J. N. and Brow, D. A. (2008). Regulation of a eukaryotic gene by GTP-dependent start site selection and transcription attenuation. Mol. Cell 31, 201-211.
54. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A. and Tollervey, D. (2005). RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121, 713-724.
55. Lebreton, A., Tomecki, R., Dziembowski, A. and Seraphin, B. (2008). Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456, 993-996.
56. Lehner, B. and Sanderson, C. M. (2004). A protein interaction framework for human mRNA degradation. Genome Res. 14, 1315-1323.
57. Lejeune, F., Li, X. and Maquat, L. E. (2003). Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12, 675-687.
58. Leszczyniecka, M., Kang, D. C., Sarkar, D., Su, Z. Z., Holmes, M., Valerie, K. and Fisher, P. B. (2002). Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc. Natl. Acad. Sci. USA 99, 16636-16641.
59. Leszczyniecka, M., DeSalle, R., Kang, D. C. and Fisher, P. B. (2004). The origin of polynucleotide phosphorylase domains. Mol. Phylogenet. Evol. 31, 123-130.
60. Li, Z., Pandit, S. and Deutscher, M. P. (1998). 3′ exoribonucleolytic trimming is a common feature of the maturation of small, stable RNAs in Escherichia coli. Proc. Natl. Acad. Sci. USA 95, 2856-2861.
61. Li, Z., Reimers, S., Pandit, S. and Deutscher, M. P. (2002). RNA quality control: degradation of defective transfer RNA. EMBO J. 21, 1132-1138.
62. Libri, D., Dower, K., Boulay, J., Thomsen, R., Rosbash, M. and Jensen, T. H. (2002). Interactions between mRNA export commitment, 3′-end quality control, and nuclear degradation. Mol. Cell. Biol. 22, 8254-8266.
63. Littauer, U. Z. and Kornberg, A. (1957). Reversible synthesis of polyribonucleotides with an enzyme from Escherichia coli. J. Biol. Chem. 226, 1077-1092.
64. Liu, Q., Greimann, J. C. and Lima, C. D. (2006). Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223-1237.
65. Liu, Z., Macias, M. J., Bottomley, M. J., Stier, G., Linge, J. P., Nilges, M., Bork, P. and Sattler, M. (1999). The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure 7, 1557-1566.
66. Lorentzen, E., Walter, P., Fribourg, S., Evguenieva-Hackenberg, E., Klug, G. and Conti, E. (2005). The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat. Struct. Mol. Biol. 12, 575-581.
67. Lorentzen, E., Dziembowski, A., Lindner, D., Seraphin, B. and Conti, E. (2007). RNA channelling by the archaeal exosome. EMBO Rep. 8, 470-476.
68. Lorentzen, E., Basquin, J., Tomecki, R., Dziembowski, A. and Conti, E. (2008). Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol. Cell 29, 717-728.
69. Lykke-Andersen, J. and Wagner, E. (2005). Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19, 351-361.
70. Lykke-Andersen, S. and Jensen, T. H. (2007). Overlapping pathways dictate termination of RNA polymerase II transcription. Biochimie 89, 1177-1182.
71. Martens, J. A., Laprade, L. and Winston, F. (2004). Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429, 571-574.
72. Martens, J. A., Wu, P. Y. and Winston, F. (2005). Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes Dev. 19, 2695-2704.
73. Martin, G. and Keller, W. (2007). RNA-specific ribonucleotidyl transferases. RNA 13, 1834-1849.
74. Mathy, N., Benard, L., Pellegrini, O., Daou, R., Wen, T. and Condon, C. (2007). 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129, 681-692.
75. Midtgaard, S. F., Assenholt, J., Jonstrup, A. T., Van, L. B., Jensen, T. H. and Brodersen, D. E. (2006). Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc. Natl. Acad. Sci. USA 103, 11898-11903.
76. Milligan, L., Decourty, L., Saveanu, C., Rappsilber, J., Ceulemans, H., Jacquier, A. and Tollervey, D. (2008). A yeast exosome cofactor, Mpp6, functions in RNA surveillance and in the degradation of noncoding RNA transcripts. Mol. Cell. Biol. 28, 5446-5457.
77. Mitchell, P. and Tollervey, D. (2003). An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′→5′ degradation. Mol. Cell 11, 1405-1413.
78. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. and Tollervey, D. (1997). The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91, 457-466.
79. Mitchell, P., Petfalski, E., Houalla, R., Podtelejnikov, A., Mann, M. and Tollervey, D. (2003). Rrp47p is an exosome-associated protein required for the 3′ processing of stable RNAs. Mol. Cell. Biol. 23, 6982-6992.
80. Mukherjee, D., Gao, M., O'Connor, J. P., Raijmakers, R., Pruijn, G., Lutz, C. S. and Wilusz, J. (2002). The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21, 165-174.
81. Mullen, T. E. and Marzluff, W. F. (2008). Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev. 22, 50-65.
82. Neil, H., Malabat, C., d'Aubenton-Carafa, Y., Xu, Z., Steinmetz, L. M. and Jacquier, A. (2009). Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457, 1038-1042.
83. Peng, W. T., Robinson, M. D., Mnaimneh, S., Krogan, N. J., Cagney, G., Morris, Q., Davierwala, A. P., Grigull, J., Yang, X., Zhang, W. et al. (2003). A panoramic view of yeast noncoding RNA processing. Cell 113, 919-933.
84. Piwowarski, J., Grzechnik, P., Dziembowski, A., Dmochowska, A., Minczuk, M. and Stepien, P. P. (2003). Human polynucleotide phosphorylase, hPNPase, is localized in mitochondria. J. Mol. Biol. 329, 853-857.
85. Preker, P., Nielsen, J., Kammler, S., Lykke-Andersen, S., Christensen, M. S., Mapendano, C. K., Schierup, M. H. and Jensen, T. H. (2008). RNA exosome depletion reveals transcription upstream of active human promoters. Science 322, 1851-1854.
86. Py, B., Causton, H., Mudd, E. A. and Higgins, C. F. (1994). A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14, 717-729.
87. Py, B., Higgins, C. F., Krisch, H. M. and Carpousis, A. J. (1996). A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381, 169-172.
88. Raynal, L. C. and Carpousis, A. J. (1999). Poly(A) polymerase I of Escherichia coli: characterization of the catalytic domain, an RNA binding site and regions for the interaction with proteins involved in mRNA degradation. Mol. Microbiol. 32, 765-775.
89. Rougemaille, M., Gudipati, R. K., Olesen, J. R., Thomsen, R., Seraphin, B., Libri, D. and Jensen, T. H. (2007). Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J. 26, 2317-2326.
90. Saguez, C., Schmid, M., Olesen, J. R., Ghazy, M. A., Qu, X., Poulsen, M. B., Nasser, T., Moore, C. and Jensen, T. H. (2008). Nuclear mRNA surveillance in THO/sub2 mutants is triggered by inefficient polyadenylation. Mol. Cell 31, 91-103.
91. Schaeffer, D., Tsanova, B., Barbas, A., Reis, F. P., Dastidar, E. G., Sanchez-Rotunno, M., Arraiano, C. M. and van Hoof, A. (2009). The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat. Struct. Mol. Biol. 16, 56-62.
92. Schilders, G., Raijmakers, R., Raats, J. M. and Pruijn, G. J. (2005). MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res. 33, 6795-6804.
93. Schilders, G., van Dijk, E. and Pruijn, G. J. (2007). C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res. 35, 2564-2572.
94. Schmid, M. and Jensen, T. H. (2008). The exosome: a multipurpose RNA-decay machine. Trends Biochem. Sci. 33, 501-510.
95. Schneider, C., Anderson, J. T. and Tollervey, D. (2007). The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol. Cell 27, 324-331.
96. Schneider, C., Leung, E., Brown, J. and Tollervey, D. (2009). The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res. 37, 1127-1140.
97. Shi, Z., Yang, W. Z., Lin-Chao, S., Chak, K. F. and Yuan, H. S. (2008). Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 14, 2361-2371.
98. Stead, J. A., Costello, J. L., Livingstone, M. J. and Mitchell, P. (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.
99. Steinmetz, E. J. and Brow, D. A. (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.
100. Steinmetz, E. J., Conrad, N. K., Brow, D. A. and Corden, J. L. (2001). RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413, 327-331.
101. Steinmetz, E. J., Warren, C. L., Kuehner, J. N., Panbehi, B., Ansari, A. Z. and Brow, D. A. (2006). Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 24, 735-746.
102. Suryanarayana, T. and Subramanian, A. R. (1984). Function of the repeating homologous sequences in nucleic acid binding domain of ribosomal protein S1. Biochemistry 23, 1047-1051.
103. Symmons, M. F., Jones, G. H. and Luisi, B. F. (2000). A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 8, 1215-1226.
104. Takahashi, S., Araki, Y., Sakuno, T. and Katada, T. (2003). Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast. EMBO J. 22, 3951-3959.
105. Thiebaut, M., Kisseleva-Romanova, E., Rougemaille, M., Boulay, J. and Libri, D. (2006). Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Mol. Cell 23, 853-864.
106. Thiebaut, M., Colin, J., Neil, H., Jacquier, A., Seraphin, B., Lacroute, F. and Libri, D. (2008). Futile cycle of transcription initiation and termination modulates the response to nucleotide shortage in S. cerevisiae. Mol. Cell 31, 671-682.
107. Torchet, C., Bousquet-Antonelli, C., Milligan, L., Thompson, E., Kufel, J. and Tollervey, D. (2002). Processing of 3′-extended read-through transcripts by the exosome can generate functional mRNAs. Mol. Cell 9, 1285-1296.
108. van Dijk, E. L., Schilders, G. and Pruijn, G. J. (2007). Human cell growth requires a functional cytoplasmic exosome, which is involved in various mRNA decay pathways. RNA 13, 1027-1035.
109. van Hoof, A., Lennertz, P. and 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.
110. van Hoof, A., Frischmeyer, P. A., Dietz, H. C. and Parker, R. (2002). Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295, 2262-2264.
111. Vanacova, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G. and Keller, W. (2005). A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189.
112. Vasiljeva, L. and Buratowski, S. (2006). Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Mol. Cell 21, 239-248.
113. Vasiljeva, L., Kim, M., Terzi, N., Soares, L. M. and Buratowski, S. (2008). Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol. Cell 29, 313-323.
114. Wall, D. and Kaiser, D. (1999). Type IV pili and cell motility. Mol. Microbiol. 32, 1-10.
115. Wang, X., Jia, H., Jankowsky, E. and Anderson, J. T. (2008). Degradation of hypomodified tRNA(iMet) in vivo involves RNA-dependent ATPase activity of the DExH helicase Mtr4p. RNA 14, 107-116.
116. Wang, Z., Day, N., Trifillis, P. and Kiledjian, M. (1999). An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol. Cell. Biol. 19, 4552-4560.
117. West, S., Gromak, N., Norbury, C. J. and Proudfoot, N. J. (2006). Adenylation and exosome-mediated degradation of cotranscriptionally cleaved pre-messenger RNA in human cells. Mol. Cell 21, 437-443.
118. Wormington, M., Searfoss, A. M. and Hurney, C. A. (1996). Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J. 15, 900-909.
119. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J. C., Dufour, M. E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Seraphin, B. 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.
120. Xu, F. and Cohen, S. N. (1995). RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374, 180-183.
121. Xu, Z., Wei, W., Gagneur, J., Perocchi, F., Clauder-Munster, S., Camblong, J., Guffanti, E., Stutz, F., Huber, W. and Steinmetz, L. M. (2009). Bidirectional promoters generate pervasive transcription in yeast. Nature 457, 1033-1037.
122. Zhu, B., Zheng, Y., Pham, A. D., Mandal, S. S., Erdjument-Bromage, H., Tempst, P. and Reinberg, D. (2005). Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 20, 601-611.
123. Zuo, Y., Wang, Y. and Malhotra, A. (2005). Crystal structure of Escherichia coli RNase D, an exoribonuclease involved in structured RNA processing. Structure 13, 973-984.
124. Zuo, Y., Vincent, H. A., Zhang, J., Wang, Y., Deutscher, M. P. and Malhotra, A. (2006). Structural basis for processivity and single-strand specificity of RNase II. Mol. Cell 24, 149-156.