Drosophila melanogaster Dis3 N-terminal domains are required for ribonuclease activities, nuclear localization and exosome interactions

Nucleic Acids Research

Volumn 38, Issue 16, 2010, Pages 5507-5517

  Mamolen, Megan ^a   Smith, Alexandra ^a   Andrulis, Erik D ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN ALPHA; RIBONUCLEASE; RIBONUCLEASE P; DIS3 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; EXORIBONUCLEASE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; EXOSOME; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA METABOLISM; TISSUE CULTURE; ANIMAL; CELL CULTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PROTEIN TERTIARY STRUCTURE;

DROSOPHILA MELANOGASTER; EUKARYOTA;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDORIBONUCLEASES; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; MUTATION; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASES;

EID: 77956521590     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq295     Document Type: Article

References (36)

1. Kinoshita,N., Goebl,M. and Yanagida,M. (1991) The fission yeast dis3+ encodes a 110-kDa essential protein implicated in mitotic control. Mol. Cell Biol., 11, 5839-5847.
2. Zuo,Y. and Deutscher,M.P. (2001) Exoribonuclease superfamilies: Structural analysis and phylogenetic distribution. Nucleic Acids Res., 29, 1017-1026.
3. 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.
4. Suzuki,N., Noguchi,E., Nakashima,N., Oki,M., Ohba,T., Tartakoff,A., Ohishi,M. and Nishimoto,T. (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.
5. 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.
6. Lebreton,A., Tomecki,R., Dziembowski,A. and Seraphin,B. (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature, 456, 993-996.
7. 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.
8. 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.
9. Kadowaki,T., Chen,S., Hitomi,M., Jacobs,E., Kumagai,C., Liang,S., Schneiter,R., Singleton,D., Wisniewska,J. and Tartakoff,A.M. (1994) Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J. Cell Biol., 126, 649-659.
10. Kadaba,S., Krueger,A., Trice,T., Krecic,A.M., Hinnebusch,A.G. and Anderson,J. (2004) Nuclear surveillance and degradation of hypomodified initiator tRNA Met in Saccharomyces cerevisiae. Genes Dev., 18, 1227-1240.
11. 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.
12. Graham,A.C., Davis,S.M. and Andrulis,E.D. (2009) Interdependent nucleocytoplasmic trafficking and interactions of Dis3 with Rrp6, the core exosome, and Importin-a3. Traffic, 10, 499-513.
13. Mamolen,M. and Andrulis,E.D. (2009) Characterization of the Drosophila melanogaster Dis3 ribonuclease. Biochem. Biophys. Res. Commun., 390, 529-534.
14. Amblar,M., Barbas,A., Fialho,A.M. and Arraiano,C.M. (2006) Characterization of the functional domains of Escherichia coli RNase II. J. Mol. Biol., 360, 921-933.
15. Vincent,H.A. and Deutscher,M.P. (2009) Insights into how RNase R degrades structured RNA: analysis of the nuclease domain. J. Mol. Biol., 387, 570-583.
16. Lorentzen,E., Basquin,J. and Conti,E. (2008) Structural organization of the RNA-degrading exosome. Curr. Opin. Struct. Biol., 18, 709-713.
17. Schmid,M. and Jensen,T.H. (2008) The exosome: a multipurpose RNA-decay machine. Trends Biochem. Sci., 33, 501-510.
18. 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.
19. Callahan,K.P. and Butler,J.S. (2008) Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6. Nucleic Acids Res., 36, 6645-6655.
20. Graham,A.C., Kiss,D.L. and Andrulis,E.D. (2009) Core exosome-independent roles for Rrp6 in cell cycle progression. Mol. Biol. Cell, 20, 2242-2253.
21. 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 protein recruit the exosome to degrade ARE-containing mRNAs. Cell, 107, 451-464.
22. 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.
23. Noguchi,E., Hayashi,N., Azuma,Y., Seki,T., Nakamura,M., Nakashima,N., Yanagida,M., He,X., Mueller,U., Sazer,S. et al. (1996) Dis3, implicated in mitotic control, binds directly to Ran and enhances the GEF activity of RCC1. EMBO J., 15, 5595-5605.
24. Shiomi,T., Fukushima,K., Suzuki,N., Nakashima,N., Noguchi,E. and Nishimoto,T. (1998) Human Dis3p, which binds to either GTP-or GDP-Ran, complements Saccharomyces cerevisiae Dis3. J. Biochem., 123, 883-890.
25. Gavin,A.C., Aloy,P., Grandi,P., Krause,R., Boesche,M., Marzioch,M., Rau,C., Jensen,L.J., Bastuck,S., Dumpelfeld,B. et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature, 440, 631-636.
26. Gavin,A.C., Bosche,M., Krause,R., Grandi,P., Marzioch,M., Bauer,A., Schultz,J., Rick,J.M., Michon,A.M., Cruciat,C.M. et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature, 415, 141-147.
27. 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.
28. 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.
29. Clissold,P.M. and Ponting,C.P. (2000) PIN domains in nonsense-mediated mRNA decay and RNAi. Curr. Biol., 10, 888-890.
30. Bonneau,F., Basquin,J., Ebert,J., Lorentzen,E. and Conti,E. (2009) The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell, 139, 547-559.
31. Liu,Q., Greimann,J.C. and Lima,C.D. (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell, 127, 1223-1237.
32. 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.
33. 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.
34. 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.
35. Eberle,A.B., Lykke-Andersen,S., Muhlemann,O. and Jensen,T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol., 16, 49-55.
36. Hieronymus,H., Yu,M.C. and Silver,P.A. (2004) Genome wide mRNA surveillance is coupled to mRNA export. Genes Dev., 18, 2652-2662.