The Rrp6 C-terminal domain binds RNA and activates the nuclear RNA exosome

Nucleic Acids Research

Volumn 45, Issue 2, 2017, Pages 846-860

  Wasmuth, Elizabeth V ^a   Lima, Christopher D ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXO9 PROTEIN; EXORIBONUCLEASE; NUCLEAR RNA; RIBONUCLEASE; RNA; RRP44 PROTEIN; RRP6 PROTEIN; UNCLASSIFIED DRUG; DIS3 PROTEIN, HUMAN; EXOSC10 PROTEIN, HUMAN; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; PROTEIN BINDING;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME SUBUNIT; EUKARYOTE; EXOSOME; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN RNA BINDING; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; RNA STABILITY;

EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA; RNA STABILITY;

EID: 85013998934     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw1152     Document Type: Article

References (60)

1. Houseley,J., LaCava,J. and Tollervey,D. (2006) RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol., 7, 529-539.
2. Kilchert,C., Wittmann,S. and Vasiljeva,L. (2016) The regulation and functions of the nuclear exosome complex. Nat. Rev. Mol. Cell Biol., 17, 227-239.
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, 1497-506.
4. Allmang,C., Kufel,J., Chanfreau,G., Mitchell,P., Petfalski,E. and Tollervey,D. (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J., 18, 5399-5410.
5. Allmang,C., Mitchell,P., Petfalski,E. and Tollervey,D. (2000) Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res., 28,1684-1691.
6. 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.
7. Wyers,F., Rougemaille,M., Badis,G., Rousselle,J.C., Dufour,M.E., Boulay,J., Régnault,B., Devaux,F., Namane,A., Séraphin,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.
8. 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. U.S.A., 103, 3262-3267.
9. 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.
10. Xu,Z., Wei,W., Gagneur,J., Perocchi,F., Clauder-Münster,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.
11. Bühler,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. Januszyk,K. and Lima,C.D. (2014) The eukaryotic exosome. Curr. Opin. Struct. Biol., 24, 132-140.
13. Wasmuth,E.V. and Lima,C.D. (2012) Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol. Cell, 48, 133-144.
14. 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.
15. Lebreton,A., Tomecki,R., Dziembowski,A. and Séraphin,B. (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature, 456, 993-996.
16. 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.
17. 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.
18. 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. U.S.A., 103, 11898-11903.
19. 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.
20. Feigenbutz,M., Garland,W., Turner,M. and Mitchell,P. (2013) The exosome cofactor Rrp47 is critical for the stability and normal expression of its associated exoribonuclease Rrp6 in Saccharomyces cerevisiae. PLoS One, 8, e80752.
21. Schuch,B., Feigenbutz,M., Makino,D.L., Falk,S., Basquin,C., Mitchell,P. and Conti,E. (2014) The exosome-binding factors Rrp6 and Rrp47 form a composite surface for recruiting the Mtr4 helicase. EMBO J., 33, 2829-2846.
22. Makino,D.L., Baumgärtner,M. and Conti,E. (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature, 495, 70-75.
23. Wasmuth,E.V., Januszyk,K.J. and Lima,C.D. (2014) Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature, 511, 435-439.
24. Makino,D.L., Schuch,B., Stegmann,E., Baumgärtner,M., Basquin,C. and Conti,E. (2015) RNA degradation paths in a 12-subunit nuclear exosome complex. Nature, 524, 54-58.
25. Phillips,S. and Butler,J.S. (2003) Contribution of domain structure to the RNA 3′ end processing and degradation functions of the nuclear exosome subunit Rrp6p. RNA, 9, 1098-1107.
26. Liu,J.J., Bratkowski,M.A., Liu,X., Niu,C.Y., Ke,A. and Wang,H.W. (2013) Visualization of distinct substrate-recruitment pathways in the yeast exosome by EM. Nat. Struct. Mol. Biol., 21, 95-102.
27. Drążkowsak,K., Tomecki,R., Stodus,K., Kowalska,K., Czarnocki-Cieciura,M. and Dziembowski,A. (2013) The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res., 41, 3845-3858.
28. Greimann,J.C. and Lima,C.D. (2008) Reconstitution of RNA exosomes from human and Saccharomyces cerevisiae cloning, expression, purification, and activity assays. Methods Enzymol., 448, 185-210.
29. Liu,Q., Greimann,J.C. and Lima,C.D. (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell, 127, 1223-1237.
30. Senger,B., Despons,L., Walter,P. and Fasiolo,F. (1992) The anticodon triplet is not sufficient to confer methionine acceptance to a transfer RNA. Proc. Natl. Acad. Sci. U.S.A., 89, 10768-10771.
31. 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.
32. Zearfoss,N. R. and Ryder,S. P. (2012) End-labeling oligonucleotides with chemical tags after synthesis. Methods Mol. Biol., 941, 181-193.
33. Abruzzi,K., Denome,S., Olsen,J.R., Assenholt,J., Haaning,L.L, Jensen,T.H. and Rosbash,M. (2007) A novel plasmid-based microarray screen identifies suppressors of rrp6Delta in Saccharomyces cerevisiae. Mol. Cell. Biol., 27, 1044-1055.
34. 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.
35. Met in S. cerevisiae. Genes Dev., 18, 1224-1240.
36. Basavappa,R. and Sigler,B.P. (1991) The 3 Å crystal structure of yeast initiator tRNA: functional implications in initiator/elongator discrimination. EMBO J., 10, 3105-3111.
37. 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.
38. 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.
39. Klauer,A.A. and van Hoof,A. (2013) Genetic interactions suggest multiple distinct roles of the arch and core helicase domains of Mtr4 in Rrp6 and exosome function. Nucleic Acids Res., 41, 533-541.
40. Castelnuovo,M., Rahman,S., Guffanti,E., Infantino,V., Stutz,F. and Zenklusen,D. (2013) Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nat. Struct. Mol. Biol., 20, 851-858.
41. Ming-Hsiu,H., Mittmann,M., Dong,H., Wodicka,L. and Lockhart,D.J. (1997) Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat. Biotech., 15, 1359-1367.
42. Feigenbutz,M., Jones,R., Besong,T.M., Harding,S.E. and Mitchell,P. (2013) Assembly of the yeast exoribonuclease Rrp6 with its associated cofactor Rrp47 occurs in the nucleus and is critical for the controlled expression of Rrp47. J Biol Chem, 288, 15959-15970.
43. Assenholt,J., Mouaikel,J., Andersen,K.R., Brodersen,D.E., Libri,D. and Jensen,T.H. (2008) Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA, 14, 2305-2313.
44. 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.
45. 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.
46. LaCasse,E.C. and Lefebvre,Y.A. (1995) Nuclear localization signals overlap DNA- or RNA-binding domains in nucleic acid-binding proteins. Nucleic Acids Res., 23, 1647-1656.
47. Yao,K., Wu,Y., Chen,Q., Zhang,Z., Chen,X. and Zhang,Y. (2016) The Arginine/Lysine-rich element within the DNA-binding domain is essential for nuclear localization and function of the intracellular pathogen resistance 1. PLoS One, 11, e0162832.
48. Castello,A., Fischer,B., Frese,C.K., Horos,R., Alleaume,A.M., Foehr,S., Curk,T., Krijgsveld,J. and Hentze,M.W. (2016) Comprehensive identification of RNA-Binding domains in human cells. Mol .Cell, 63, 696-710.
49. Filarsky,M., Zillner,K., Araya,I., Villar-Garea,A., Merkl,R., Langst,G. and Nemeth,A. (2015) The extended AT-hook is a novel RNA binding motif. RNA Biol., 12, 864-876.
50. Melnikov,S., Ben-Shem,A., Yusupova,G. and Yusupov,M. (2015) Insights into the origin of the nuclear localization signals in conserved ribosomal proteins. Nat. Commun., 6, 7382.
51. Tomko,R.J. Jr and Hochstrasser,M. (2014) The intrinsically disordered Sem1 protein functions as a molecular tether during proteasome lid biogenesis. Mol. Cell, 53, 433-443.
52. Kucera,N.J., Hodsdon,M.E. and Wolin,S.L. (2011) An intrinsically disordered C terminus allows the La protein to assist the biogenesis of diverse noncoding RNA precursors. Proc. Natl. Acad. Sci. U.S.A., 108, 1308-1313.
53. Varadi,M., Zsolyomi,F., Guharoy,M. and Tompa,P. (2015) Functional advantages of conserved intrinsic disorder in RNA-Binding proteins. PLoS One, 10, e0139731.
54. Calabretta,S. and Richard,S. (2015) Emerging roles of disordered sequences in RNA-Binding proteins. Trends Biochem Sci., 40, 662-72.
55. Castello,A., Fischer,B., Eichelbaum,K., Horos,R., Beckmann,B.M., Strein,C., Davey,N.E., Humphreys,D.T., Preiss,T., Steinmetz,L.M. et al. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell, 149, 1393-1406.
56. Jonas,S. and Izaurralde,E. (2013) The role of disordered protein regions in the assembly of decapping complexes and RNP granules. Genes Dev., 27, 2628-2641.
57. Tompa,P. and Csermely,P. (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J., 18,1169-1175.
58. Larkin,M.A. et al. ClustalW and ClustalX Version 2. (2007) Bioinformatics, 23, 2947-2948.
59. Gasteiger,E., Hoogland,C., Gattiker,A., Duvaud,S., Wilkins,M.R., Appel,R.D. and Bairoch,A. (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker,JM (ed). The Proteomics Protocols Handbook. Humana Press, Totowa, pp. 571-607.
60. Baker,N.A., Sept,D., Joseph,S., Holst,M.J. and McCammon,J.A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A., 98, 10037-10041.