Pronounced and extensive microtubule defects in a Saccharomyces cerevisiae DIS3 mutant

Yeast

Volumn 28, Issue 11, 2011, Pages 755-769

  Smith, Sarah B ^a   Kiss, Daniel L ^a   Turk, Edward ^a   Tartakoff, Alan M ^a   Andrulis, Erik D ^a  

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

Author keywords

Dis3; Exosome; Exozyme; Mitosis; Mitotic spindle; Mtr3

Indexed keywords

ANAPHASE; ARTICLE; CELL BUDDING; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXOSOME; FUNGAL STRAIN; FUNGUS MUTANT; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; RNA SEQUENCE; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; YEAST CELL;

CELL CYCLE; EXORIBONUCLEASES; MICROTUBULES; MITOSIS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 80255129233     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1899     Document Type: Article

References (92)

1. Allmang C, Kufel J, Chanfreau G, et al. 1999a. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410.
2. Allmang C, Mitchell P, Petfalski E, Tollervey D. 2000. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 28: 1684-1691.
3. Allmang C, Petfalski E, Podtelejnikov A, et al. 1999b. The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes Dev 13: 2148-2158.
4. Blankenberg D, Gordon A, Von Kuster G, et al. 2010a. Manipulation of FASTQ data with Galaxy. Bioinformatics 26: 1783-1785.
5. Blankenberg D, Von Kuster G, Coraor N, et al. 2010b. Galaxy: a web-based genome analysis tool for experimentalists. In Current Protocols in Molecular Biology, Chapter 19, Unit 19.10, Ausubel FM, et al. (eds). Wiley: New York; 11-21.
6. Bonneau F, Basquin J, Ebert J, et al. 2009. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139: 547-559.
7. Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102: 765-775.
8. Briggs MW, Burkard KT, Butler JS. 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.
9. Burke DJ, Dawson D, Stearns T. 2000. Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
10. Butler JS. 2002. The yin and yang of the exosome. Trends Cell Biol 12: 90-96.
11. Buttner K, Wenig K, Hopfner KP. 2006. The exosome: a macromolecular cage for controlled RNA degradation. Mol Microbiol 61: 1372-1379.
12. Cai T, Aulds J, Gill T, et al. 2002. The Saccharomyces cerevisiae RNase mitochondrial RNA processing is critical for cell cycle progression at the end of mitosis. Genetics 161: 1029-1042.
13. Callahan KP, Butler JS. 2008. Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res 36: 6645-6655.
14. Callahan KP, Butler JS. 2010. TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J Biol Chem 285: 3540-3547.
15. Chekanova JA, Gregory BD, Reverdatto SV, et al. 2007. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340-1353.
16. Ciciarello M, Mangiacasale R, Lavia P. 2007. Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 64: 1891-1914.
17. Daniel JA, Keyes BE, Ng YP, et al. 2006. Diverse functions of spindle assembly checkpoint genes in Saccharomyces cerevisiae. Genetics 172: 53-65.
18. Das B, Butler JS, Sherman F. 2003. Degradation of normal mRNA in the nucleus of Saccharomyces cerevisiae. Mol Cell Biol 23: 5502-5515.
19. Dasso M. 2002. The Ran GTPase: theme and variations. Curr Biol 12: R502-R508.
20. de la Cruz J, Kressler D, Tollervey D, Linder P. 1998. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J 17: 1128-1140.
21. Dziembowski A, Lorentzen E, Conti E, Seraphin B. 2007. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14: 15-22.
22. Eastman A. 2004. Cell cycle checkpoints and their impact on anticancer therapeutic strategies. J Cell Biochem 91: 223-231.
23. Estevez AM, Lehner B, Sanderson CM, et al. 2003. The roles of intersubunit interactions in exosome stability. J Biol Chem 278b: 34943-34951.
24. Evguenieva-Hackenburg E, Walter P, Hochleitner E, et al. 2003. An exosome-like complex in Sulfolobus solfataricus. EMBO Rep 4: 889-893.
25. Gill T, Aulds J, Schmitt ME. 2006. A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J Cell Biol 173: 35-45.
26. Gill T, Cai T, Aulds J, et al. 2004. RNase MRP cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation. Mol Cell Biol 24: 945-953.
27. Goecks J, Nekrutenko A, Taylor J. 2010. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
28. Goodman B, Zheng Y. 2006. Mitotic spindle morphogenesis: Ran on the microtubule cytoskeleton and beyond. Biochem Soc Trans 34: 716-721.
29. Graham AC, Davis SM, Andrulis ED. 2009a. Interdependent nucleocytoplasmic trafficking and interactions of Dis3 with Rrp6, the core exosome and importin-α3. Traffic 10: 499-513.
30. Graham AC, Davis SM, Andrulis ED. 2009b. Interdependent nucleocytoplasmic trafficking and interactions of Dis3 with Rrp6, the core exosome, and importin-α3. Traffic 10: 499-513.
31. Graham AC, Kiss DL, Andrulis ED. 2006. Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol Biol Cell 17: 1399-1409.
32. Graham AC, Kiss DL, Andrulis ED. 2009c. Core exosome-independent roles for Rrp6 in cell cycle progression. Mol Biol Cell 20: 2242-2253.
33. Gruss OJ, Vernos I. 2004. The mechanism of spindle assembly: functions of Ran and its target TPX2. J Cell Biol 166: 949-955.
34. Hieronymus H, Yu MC, Silver PA. 2004. Genome-wide mRNA surveillance is coupled to mRNA export. Genes Dev 18: 2652-2662.
35. Houalla R, Devaux F, Fatica A, et al. 2006. Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23: 439-454.
36. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7: 529-539.
37. Hwang E, Kusch J, Barral Y, Huffaker TC. 2003. Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables. J Cell Biol 161: 483-488.
38. Interthal H, Bellocq C, Bahler J, et al. 1995. A role of Sep1 (= Kem1, Xrn1) as a microtubule-associated protein in Saccharomyces cerevisiae. EMBO J 14: 1057-1066.
39. Kadaba S, Krueger A, Trice T, et al. 2004. Nuclear surveillance and degradation of hypomodified initiator tRNA Met in S. cerevisiae. Genes Dev 18: 1227-1240.
40. Kadowaki T, Chen S, Hitomi M, et al. 1994. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J Cell Biol 126: 649-659.
41. + RNA in Saccharomyces cerevisiae. Mol Biol Cell 6: 1103-1110.
42. + gene encodes a 110-kDa essential protein implicated in mitotic control. Mol Cell Biol 11: 5839-5847.
43. Kiss DL, Andrulis ED. 2010. Genome-wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits. RNA 16: 781-791.
44. Kiss DL, Andrulis ED. 2011. The exozyme model: a continuum of functionally distinct complexes. RNA 17: 1-13.
45. Kusch J, Liakopoulos D, Barral Y. 2003. Spindle asymmetry: a compass for the cell. Trends Cell Biol 13: 562-569.
46. LaCava J, Houseley J, Saveanu C, et al. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
47. Lee L, Klee SK, Evangelista M, et al. 1999. Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p. J Cell Biol 144: 947-961.
48. Li HY, Cao K, Zheng Y. 2003. Ran in the spindle checkpoint: a new function for a versatile GTPase. Trends Cell Biol 13: 553-557.
49. Liang S, Hitomi M, Hu YH, et al. 1996. A DEAD-box-family protein is required for nucleocytoplasmic transport of yeast mRNA. Mol Cell Biol 16: 5139-5146.
50. Liu Q, Greimann JC, Lima CD. 2006. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127: 1223-1237.
51. Malet H, Topf M, Clare DK, et al. 2010. RNA channelling by the eukaryotic exosome. EMBO Rep 11: 936-942.
52. Mamolen M, Andrulis ED. 2009. Characterization of the Drosophila melanogaster Dis3 ribonuclease. Biochem Biophys Res Commun 390: 529-534.
53. Mamolen M, Smith A, Andrulis ED. 2010. Drosophila melanogaster Dis3 N-terminal domains are required for ribonuclease activities, nuclear localization and exosome interactions. Nucleic Acids Res 38: 5507-5517.
54. 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.
55. Mitchell P, Petfalski E, Shevchenko A, et al. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′ → 5′ exoribonucleases. Cell 91: 457-466.
56. Mitchell P, Petfalski E, Tollervey D. 1996. The 3′ end of yeast 5.8S rRNA is generated by an exonuclease processing mechanism. Genes Dev 10: 502-513.
57. Mitchell P, Tollervey D. 2000. Musing on the structural organization of the exosome complex. Nat Struct Biol 7: 843-846.
58. Murakami H, Goto DB, Toda T, et al. 2007. Ribonuclease activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS One 2: e317.
59. Noguchi E, Hayashi N, Azuma Y, et al. 1996. Dis3, implicated in mitotic control, binds directly to Ran and enhances the GEF activity of RCC1. EMBO J 15: 5595-5605.
60. Oeffinger M, Fatica A, Rout MP, Tollervey D. 2007. Yeast Rrp14p is required for ribosomal subunit synthesis and for correct positioning of the mitotic spindle during mitosis. Nucleic Acids Res 35: 1354-1366.
61. Ohkura H, Adachi Y, Kinoshita N, et al. 1988. Cold-sensitive and caffeine-supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis. EMBO J 7: 1465-1473.
62. Oliveira CC, Gonzales FA, Zanchin NI. 2002. Temperature-sensitive mutants of the exosome subunit Rrp43p show a deficiency in mRNA degradation and no longer interact with the exosome. Nucleic Acids Res 30: 4186-4198.
63. Palmer RE, Sullivan DS, Huffaker T, Koshland D. 1992. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 119: 583-593.
64. Pathak R, Bogomolnaya LM, Guo J, Polymenis M. 2005. A role for KEM1 at the START of the cell cycle in Saccharomyces cerevisiae. Curr Genet 48: 300-309.
65. Preker P, Nielsen J, Kammler S, et al. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
66. Proudfoot N. 2004. New perspectives on connecting messenger RNA 3′ end formation to transcription. Curr Opin Cell Biol 16: 272-278.
67. San Paolo S, Vanacova S, Schenk L, et al. 2009. Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet 5: e1000555.
68. Schaeffer D, Tsanova B, Barbas A, et al. 2009. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16: 56-62.
69. Schaeffer D, van Hoof A. 2011. Different nuclease requirements for exosome-mediated degradation of normal and nonstop mRNAs. Proc Natl Acad Sci USA (in press).
70. Schilders G, van Dijk E, Pruijn GJ. 2007. C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res 35(8): 2564-2572.
71. Schlegel R, Pardee AB. 1986. Caffeine-induced uncoupling of mitosis from the completion of DNA replication in mammalian cells. Science 232: 1264-1266.
72. Schneider C, Anderson JT, Tollervey D. 2007. The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol Cell 27: 324-331.
73. Shaw SL, Yeh E, Maddox P, et al. 1997. Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J Cell Biol 139: 985-994.
74. + involved in cell shape control and mitosis. Mol Biol Cell 4: 303-313.
75. Shiomi T, Fukushima K, Suzuki N, et al. 1998. Human dis3p, which binds to either GTP- or GDP-Ran, complements Saccharomyces cerevisiae dis3. J Biochem (Tokyo) 123: 883-890.
76. + gene, encoding a putative nuclear 5′ → 3′ exoribonuclease, is required for proper chromosome segregation in fission yeast. Nucleic Acids Res 29: 1326-1333.
77. Smeets MF, Segal M. 2002. Spindle polarity in S. cerevisiae: MEN can tell. Cell Cycle 1: 308-311.
78. 2/M transition. Mol Biotechnol 32: 227-248.
79. Straight AF, Marshall WF, Sedat JW, Murray AW. 1997. Mitosis in living budding yeast: anaphase A but no metaphase plate. Science 277: 574-578.
80. Sullivan DS, Huffaker TC. 1992. Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae. J Cell Biol 119: 379-388.
81. Suzuki N, Noguchi E, Nakashima N, et al. 2001. The Saccharomyces cerevisiae small GTPase, Gsp1p/Ran, is involved in 3′ processing of 7S-to-5.8S rRNA and in degradation of the excised 5′-A0 fragment of 35S pre-rRNA, both of which are carried out by the exosome. Genetics 158: 613-625.
82. Szankasi P, Smith GR. 1996. Requirement of Sz. pombe exonuclease II, a homologue of S. cerevisiae Sep1, for normal mitotic growth and viability. Curr Genet 30: 284-293.
83. 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.
84. Trinkle-Mulcahy L, Lamond AI. 2006. Mitotic phosphatases: no longer silent partners. Curr Opin Cell Biol 18: 623-631.
85. van Dijk EL, Schilders G, Pruijn GJ. 2007. Human cell growth requires a functional cytoplasmic exosome, which is involved in various mRNA decay pathways. RNA 13: 1027-1035.
86. van Hoof A, Lennertz P, Parker R. 2000a. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 20: 441-452.
87. van Hoof A, Staples RR, Baker RE, Parker R. 2000b. Function of the ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol Cell Biol 20: 8230-8243.
88. Vanacova S, Wolf J, Martin G, et al. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3: e189.
89. Wang SW, Asakawa K, Win TZ, et al. 2005. Inactivation of the pre-mRNA cleavage and polyadenylation factor Pfs2 in fission yeast causes lethal cell cycle defects. Mol Cell Biol 25: 2288-2296.
90. Wilson RB, Brenner AA, White TB, et al. 1991. The Saccharomyces cerevisiae SRK1 gene, a suppressor of bcy1 and ins1, may be involved in protein phosphatase function. Mol Cell Biol 11: 3369-3373.
91. Win TZ, Draper S, Read RL, et al. 2006. Requirement of fission yeast Cid14 in polyadenylation of rRNAs. Mol Cell Biol 26: 1710-1721.
92. 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.