Core exosome - Independent roles for Rrp6 in cell cycle progression

Molecular Biology of the Cell

Volumn 20, Issue 8, 2009, Pages 2242-2253

  Graham, Amy C ^a   Kiss, Daniel L ^a   Andrulis, Erik D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CHECKPOINT KINASE 1; EXORIBONUCLEASE; HISTONE H3; PROTEIN SUBUNIT; RIBONUCLEASE; RIBONUCLEASE CONTAINING PROTEIN 40; RIBONUCLEASE CONTAINING PROTEIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CENTROMERE; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXOSOME; MICROARRAY ANALYSIS; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; RNA METABOLISM; TISSUE CULTURE;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CHROMOSOME ABERRATIONS; CHROMOSOME SEGREGATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXOSOMES; GENE EXPRESSION PROFILING; HISTONES; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PHENOTYPE; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

DROSOPHILA MELANOGASTER;

EID: 65349174674     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-08-0825     Document Type: Article

References (68)

1. Abruzzi, K., Denome, S., Olsen, J. R., Assenholt, J., Haaning, L. L., Jensen T. H., and Rosbash, M. (2007). A novel plasmid - based microarray screer identifies suppressors of rrp6Delta in Saccharomyces cerevisiae. Mol. Cell. Biol 27, 1044-1055.
2. Alliegro, M. C., Alliegro, M. A., and Palazzo, R. E. (2006). Centrosome - associated RNA in surf clam oocytes. Proc. Natl. Acad. Sci. USA 103, 9034-9038.
3. 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.
4. 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.
5. Andrulis, E. D., Guzman, E., Doring, P., Werner, J., and Lis, J. T. (2000). High - resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation. Genes Dev. 14, 2635-2649.
6. Andrulis, E. D., Werner, J., Nazarian, A., Erdjument - Bromage, H., Tempst, P., and Lis, J. T. (2002). The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420, 837-841.
7. Baker, R. E., Harris, K., and Zhang, K. (1998). Mutations synthetically lethal with cep1 target S. cerevisiae kinetochore components. Genetics 149, 73-85.
8. Blower, M. D., Nachury, M., Heald, R., and Weis, K. (2005). A Rae1 - containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121, 223-234.
9. Bousquet - Antonelli, C., Presutti, C., and Tollervey, D. (2000). Identification of a regulated pathway for nuclear pre - mRNA turnover. Cell 102, 765-775.
10. 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.
11. Buhler, M., Haas, W., Gygi, S. P., and Moazed, D. (2007). RNAi - dependent and - independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129, 707-721.
12. 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.
13. 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.
14. Callahan, K. P., and Butler, J. S. (2008). Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res. 36, 6645-6655.
15. Canavan, R., and Bond, U. (2007). Deletion of the nuclear exosome component RRP6 leads to continued accumulation of the histone mRNA HTB1 in S-phase of the cell cycle in Saccharomyces cerevisiae. Nucleic Acids Res. 35, 6268-6279.
16. 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.
17. Das, B., Butler, J. S., and Sherman, F. (2003). Degradation of normal mRNA in the nucleus of Saccharomyces cerevisiae. Mol. Cell. Biol. 23, 5502-5515.
18. 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.
19. Dichtl, B., Blank, D., Ohnacker, M., Friedlein, A., Roeder, D., Langen, H., and Keller, W. (2002). A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol. Cell 10, 1139-1150.
20. 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.
21. Estevez, A. M., Lehner, B., Sanderson, C. M., Ruppert, T., and Clayton, C. (2003). The roles of intersubunit interactions in exosome stability. J. Biol. Chem. 278, 34943-34951.
22. Fang, F., Phillips, S., and Butler, J. S. (2005). Rat1p and Rai1p function with the nuclear exosome in the processing and degradation of rRNA precursors. RNA 11, 1571-1578.
23. Fomproix, N., and Hernandez-Verdun, D. (1999). Effects of anti - PM - Scl 100 (Rrp6p exonuclease) antibodies on prenucleolar body dynamics at the end of mitosis. Exp. Cell Res. 251, 452-464.
24. Gavin,A. C.,etal. (2006). Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636.
25. Gavin, A. C., et al. (2002). Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147.
26. Giet, R., McLean, D., Descamps, S., Lee, M. J., Raff, J. W., Prigent, C., and Glover, D. M. (2002). Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J. Cell Biol. 156, 437-451.
27. Gill,T.,Cai,T.,Aulds,J.,Wierzbicki,S.,and Schmitt,M. E. (2004). RNase MRP cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation. Mol. Cell Biol. 24, 945-953.
28. Goshima, G., Wollman, R., Goodwin, S. S., Zhang, N., Scholey, J. M., Vale, R. D., and Stuurman, N. (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421.
29. Graham, A. C., Kiss, D. L., and Andrulis, E. D. (2006). Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol. Biol. Cell 17, 1399-1409.
30. Haile, S., Cristodero, M., Clayton, C., and Estevez, A. M. (2007). The subcel - lular localisation of trypanosome RRP6 and its association with the exosome. Mol. Biochem. Parasitol. 151, 52-58.
31. Hieronymus, H., Yu, M. C., and Silver, P. A. (2004). Genome - wide mRNA surveillance is coupled to mRNA export. Genes Dev. 18, 2652-2662.
32. 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.
33. Houalla, R., Devaux, F., Fatica, A., Kufel, J., Barrass, D., Torchet, C., and Tollervey, D. (2006). Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23, 439-454.
34. Houseley, J., LaCava, J., and Tollervey, D. (2006). RNA - quality control by the exosome. Nat. Rev. Mol. Cell. Biol. 7, 529-539.
35. Jensen, T. H., Boulay, J., Rosbash, M., and Libri, D. (2001). The DECD box putative ATPase Sub2p is an early mRNA export factor. Curr. Biol. 11, 1711-1715.
36. Johansen, K. M., and Johansen, J. (2006). Regulation of chromatin structure by histone H3S10 phosphorylation. Chromosome Res. 14, 393-404.
37. Kinoshita, N., Goebl, M., and Yanagida, M. (1991). The fission yeast dis3 + gene encodes a 110 - kDa essential protein implicated in mitotic control. Mol. Cell Biol. 11, 5839-5847.
38. Koonin, E. V., Wolf, Y. I., and Aravind, L. (2001). Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative - genomic approach. Genome Res. 11, 240-252.
39. Krogan, N. J., et al (2004). High - definition macromolecular composition of yeast RNA - processing complexes. Mol. Cell 13, 225-239.
40. Kuai, L., Das, B., and Sherman, F. (2005). A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102, 13962-13967.
41. Lambert, J. D., and Nagy, L. M. (2002). Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 420, 682-686.
42. 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.
43. 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.
44. Liu, Q., Greimann, J. C., and Lima, C. D. (2006). Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223-1237.
45. Logarinho, E., Bousbaa, H., Dias, J. M., Lopes, C., Amorim, I., Antunes - Martins, A., and Sunkel, C. E. (2004). Different spindle checkpoint proteins monitor microtubule attachment and tension at kinetochores in Drosophila cells. J. Cell Sci. 117, 1757-1771.
46. Lorentzen, E., and Conti, E. (2005). Structural basis of 3′ end RNA recognition and exoribonucleolytic cleavage by an exosome RNase PH core. Mol. Cell 20, 473-481.
47. Lorentzen, E., and Conti, E. (2006). The exosome and the proteasome: nano- compartments for degradation. Cell 125, 651-654.
48. 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.
49. Luna, R., Jimeno, S., Marin, M., Huertas, P., Garcia - Rubio, M., and Aguilera, A. (2005). Interdependence between transcription and mRNP processing and export, and its impact on genetic stability. Mol. Cell 18, 711-722.
50. 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.
51. Muller, B., Blackburn, J., Feijoo, C., Zhao, X., and Smythe, C. (2007). Are multiple checkpoint mediators involved in a checkpoint linking histone gene expression with DNA replication? Biochem. Soc. Trans. 35, 1369-1371.
52. Murakami, H., Goto, D. B., Toda, T., Chen, E. S., Grewal, S. I., Martienssen, R. A., and Yanagida, M. (2007). Ribonuclease activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS ONE 2, e317.
53. Musacchio, A., and Salmon, E. D. (2007). The spindle - assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393.
54. Nicolas, E., Yamada, T., Cam, H.P., Fitzgerald, P.C., Kobayashi, R., and Grewal, S.I. (2007). Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat. Struct. Mol. Biol.
55. Noguchi, E., et al. (1996). Dis3, implicated in mitotic control, binds directly to Ran and enhances the GEF activity of RCC1. EMBO J. 15, 5595-5605.
56. Ohkura, H., Adachi, Y., Kinoshita, N., Niwa, O., Toda, T., and Yanagida, M. (1988). Cold - sensitive and caffeine - supersensitive mutants of the Schizosaccha - romyces pombe dis genes implicated in sister chromatid separation during mitosis. EMBO J. 7, 1465-1473.
57. Reis, C. C., and Campbell, J. L. (2007). Contribution of Trf4/5 and the nuclear exosome to genome stability through regulation of histone mRNA levels in Saccharomyces cerevisiae. Genetics 175, 993-1010.
58. Roth, K. M., Wolf, M. K., Rossi, M., and Butler, J. S. (2005). The nuclear exosome contributes to autogenous control of NAB2 mRNA levels. Mol. Cell Biol. 25, 1577-1585.
59. Sullivan, W., Ashburner, M., and Hawley, R. S. (2000). Drosophila Protocols, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Thomsen, R., Libri, D., Boulay, J., Rosbash, M., and Jensen, T. H. (2003). Localization of nuclear retained mRNAs in Saccharomyces cerevisiae. RNA 9, 1049-1057.
61. van Hoof, A., Staples, R. R., Baker, R. E., and Parker, R. (2000). Function of the ski4p (Csl4p) and Ski7p proteins in 3′ - to - 5′ degradation of mRNA. Mol. Cell. Biol. 20, 8230-8243.
62. Van Hooser, A. A., Yuh, P., and Heald, R. (2005). The perichromosomal layer. Chromosoma 114, 377-388.
63. 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.
64. Vidanes, G. M., Bonilla, C. Y., and Toczyski, D. P. (2005). Complicated tails: histone modifications and the DNA damage response. Cell 121, 973-976.
65. Vodala, S., Abruzzi, K. C., and Rosbash, M. (2008). The nuclear exosome and adenylation regulate posttranscriptional tethering of yeast GAL genes to the nuclear periphery. Mol. Cell 31, 104-113.
66. Wyers, F., 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.
67. Zenklusen, D., Vinciguerra, P., Wyss, J. C., and Stutz, F. (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.
68. Zhao, J. (2004). Coordination of DNA synthesis and histone gene expression during normal cell cycle progression and after DNA damage. Cell Cycle 3, 695-697.