The Mtr4 ratchet helix and arch domain both function to promote RNA unwinding

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages 13861-13872

  Taylor, Lacy L ^a   Jackson, Ryan N ^a   Rexhepaj, Megi ^a   King, Alejandra Klauer ^b   Lott, Lindsey K ^a   Van Hoof, Ambro ^b   Johnson, Sean J ^a  

^a UTAH STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MTR4 PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; MTR4 PROTEIN, S CEREVISIAE; POLYADENYLIC ACID; PROTEIN BINDING; RNA; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DENATURATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MUTAGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RATCHET HELIX; RESIDUE ANALYSIS; RNA STRUCTURE; RNA UNWINDING; SCORING SYSTEM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

DEAD-BOX RNA HELICASES; MODELS, MOLECULAR; MUTATION; POLY A; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RNA; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84927642789     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1208     Document Type: Article

References (62)

1. Bernstein, J. and Toth, E. A. (2012) Yeast nuclear RNA processing. World J. Biol. Chem., 3, 7-26.
2. Lebreton, A. and Seraphin, B. (2008) Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim. Biophys. Acta, 1779, 558-565.
3. Ibrahim, H., Wilusz, J. and Wilusz, C. J. (2008) RNA recognition by 3'-to-5' exonucleases: the substrate perspective. Biochim. Biophys. Acta, 1779, 256-265.
4. Astuti, D., Morris, M. R., Cooper, W. N., Staals, R. H., Wake, N. C., Fews, G. A., Gill, H., Gentle, D., Shuib, S., Ricketts, C. J. et al. (2012) Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nat. Genet., 44, 277-284.
5. Bruserud, O. (2007) Introduction: RNA and the treatment of human cancer. Curr. Pharm. Biotechnol., 8, 318-319.
6. Fabre, A., Charroux, B., Martinez-Vinson, C., Roquelaure, B., Odul, E., Sayar, E., Smith, H., Colomb, V., Andre, N., Hugot, J. P. et al. (2012) SKIV2L mutations cause syndromic diarrhea, or trichohepatoenteric syndrome. Am. J. Hum. Genet., 90, 689-692.
7. Nelson, P. T. and Keller, J. N (2007) RNA in brain disease: no longer just 'the messenger in the middle'. J. Neuropathol. Exp. Neurol, 66, 461-468.
8. Staals, R. H. and Pruijn, G. J. (2011) The human exosome and disease. Adv. Exp. Med. Biol, 702, 132-142.
9. Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D. and Mitchell, P (1999) The yeast exosome and human PM-Scl are related complexes of 3' → 5' exonucleases. Genes Dev., 13, 2148-2158.
10. Lykke-Andersen, S., Tomecki, R., Jensen, TH. and Dziembowski, A. (2011) The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol, 8, 61-66.
11. 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.
12. Wolin, S. L., Sim, S. and Chen, X. (2012) Nuclear noncoding RNA surveillance: is the end in sight? Trends Genet., 28, 306-313.
13. Januszyk, K. and Lima, C. D. (2014) The eukaryotic RNA exosome. Curr. Opin. Cell Biol., 24, 132-140.
14. Schneider, C. and Tollervey, D. (2013) Threading the barrel of the RNA exosome. Trends Biochem. Sci., 38, 485-493.
15. Anderson, J. T. and Wang, X. (2009) Nuclear RNA surveillance: no sign of substrates tailing off. Crit. Rev. Biochem. Mol. Biol, 44, 16-24.
16. Bayne, E. H., White, S. A. and Allshire, R. C. (2007) DegrAAAded into silence. Cell, 129, 651-653.
17. Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell, 136, 763-776.
18. Vanacova, S. and Stefl, R. (2007) The exosome and RNA quality control in the nucleus. EMBO Rep., 8, 651-657.
19. Kong, K. Y., Tang, H. M., Pan, K., Huang, Z., Lee, TH., Hinnebusch, A. G., Jin, D. Y and Wong, C. M. (2013) Cotranscriptional recruitment of yeast TRAMP complex to intronic sequences promotes optimal pre-mRNA splicing. Nucleic Acids Res., 42, 643-660.
20. Sloan, K. E., Bohnsack, M. T., Schneider, C. and Watkins, NJ. (2014) The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. RNA Biol, 20, 540-550.
21. 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.
22. 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.
23. 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.
24. Jia, H., Wang, X., Liu, F., Guenther, U. P., Srinivasan, S., Anderson, J. T and Jankowsky, E. (2011) The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell, 145, 890-901.
25. Wlotzka, W., Kudla, G., Granneman, S. and Tollervey, D. (2011) The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J., 30, 1790-1803.
26. Lykke-Andersen, S., Brodersen, D. E. and Jensen, TH. (2009) Origins and activities of the eukaryotic exosome. J. Cell Sci., 122, 1487-1494.
27. Bernstein, J., Ballin, J. D., Patterson, D. N., Wilson, G. M. and Toth, E. A. (2010) Unique properties of the Mtr4p-poly (A) complex suggest a role in substrate targeting. Biochemistry, 49, 10357-10370.
28. Bernstein, J., Patterson, D. N., Wilson, GM. and Toth, E. A. (2008) Characterization of the essential activities of Saccharomyces cerevisiae Mtr4p, a 3'→5' helicase partner of the nuclear exosome. J. Biol. Chem., 283, 4930-4942.
29. Jia, H., Wang, X., Anderson, J. T and Jankowsky, E. (2012) RNA unwinding by the Trf4/Air2/Mtr4 polyadenylation (TRAMP) complex. Proc. Natl Acad. Sci. U. S. A., 109, 7292-7297.
30. Jackson, R. N., Klauer, A. A., Hintze, B. J., Robinson, H., van Hoof, A. and Johnson, S. J. (2010) The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J., 29, 2205-2216.
31. Buttner, K., Nehring, S. and Hopfner, K. P (2007) Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat. Struct. Mol. Biol, 14, 647-652.
32. Halbach, F., Rode, M. and Conti, E. (2012) The crystal structure of S.cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA, 18, 124-134.
33. He, Y, Andersen, G. R. and Nielsen, K. H. (2011) Structural basis for the function of DEAH helicases. EMBO Rep, 11, 180-186.
34. Oyama, T., Oka, H., Mayanagi, K., Shirai, T., Matoba, K., Fujikane, R., Ishino, Y and Morikawa, K. (2009) Atomic structures and functional implications of the archaeal RecQ-like helicase Hjm. BMC Struct. Biol, 9, 2.
35. Richards, J. D., Johnson, K. A., Liu, H., McRobbie, A. M., McMahon, S., Oke, M., Carter, L., Naismith, J. H. and White, M. F. (2008) Structure of the DNA repair helicase hel308 reveals DNA binding and autoinhibitory domains. J. Biol. Chem., 283, 5118-5126.
36. Walbott, H., Mouffok, S., Capeyrou, R., Lebaron, S., Humbert, O., van Tilbeurgh, H., Henry, Y and Leulliot, N (2010) Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J., 29, 2194-2204.
37. Zhang, X., Nakashima, T., Kakuta, Y., Yao, M., Tanaka, I. and Kimura, M. (2008) Crystal structure of an archaeal Ski2p-like protein from Pyrococcus horikoshii OT3. Protein Sci, 17, 136-145.
38. Weir, J. R., Bonneau, F., Hentschel, J. and Conti, E. (2010) Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc. Natl Acad. Sci. U. S. A., 107, 12139-12144.
39. Mozaffari-Jovin, S., Wandersleben, T., Santos, K. F., Will, CL., Luhrmann, R. and Wahl, M. C. (2013) Inhibition of RNA helicase Brr2 by the C-terminal tail of the spliceosomal protein Prp8. Science, 341, 80-83.
40. Johnson, S. J. and Jackson, RN. (2013) Ski2-like RNA helicase structures common themes and complex assemblies. RNA Biol, 10, 1-12.
41. Singleton, M. R., Dillingham, M. S. and Wigley, D. B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev Biochem., 76, 23-50.
42. Holub, P., Lalakova, J., Cerna, H., Pasulka, J., Sarazova, M., Hrazdilova, K., Arce, M. S., Hobor, F., Stefl, R. and Vanacova, S. (2012) Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res., 40, 5679-5693.
43. Zhang, L., Xu, T., Maeder, C., Bud, L. O., Shanks, J., Nix, J., Guthrie, C., Pleiss, J. A. and Zhao, R. (2009) Structural evidence for consecutive Hel308-like modules in the spliceosomal ATPase Brr2. Nat. Struct. Mol. Biol., 16, 731-739.
44. Hahn, D. and Beggs, J. D. (2010) Brr2p RNA helicase with a split personality: insights into structure and function. Biochem. Soc. Trans., 38, 1105-1109.
45. Liang, S., Hitomi, M., Hu, Y. H., Liu, Y. and Tartakoff, A. M. (1996) A DEAD-box-family protein is required for nucleocytoplasmic transport of yeast mRNA. Mol. Cell. Biol., 16, 5139-5146.
46. Pena, V., Jovin, S. M., Fabrizio, P., Orlowski, J., Bujnicki, J. M., Luhrmann, R. and Wahl, M. C. (2009) Common design principles in the spliceosomal RNA helicase Brr2 and in the Hel308 DNA helicase. Mol. Cell, 35, 454-466.
47. Small, E. C., Leggett, S. R., Winans, A. A. and Staley, J. P. (2006) The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell, 23, 389-399.
48. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
49. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
50. Ashkenazy, H., Erez, E., Martz, E., Pupko, T. and Ben-Tal, N. (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res., 38, W529-W533.
51. Liu, H. and Naismith, J. H. (2008) An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol., 8, 91.
52. Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., de Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E. et al. (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res., 4, W597-W603.
53. 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.
54. Wagner, J. D. O., Jankowsky, E., Company, M., Pyle, A. M. and Abelson, J. N. (1998) The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes. EMBO J., 17, 2926-2937.
55. Sikorski, R. S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
56. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr., D66, 486-501.
57. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., D66, 213-221.
58. Yang, Q. and Jankowsky, E. (2005) ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry, 44, 13591-13601.
59. Kim, J. W., Seo, M. Y., Shelat, A., Kim, C. S., Kwon, T. W., Lu, H. H., Moustakas, D. T., Sun, J. and Han, J. H. (2003) Structurally conserved amino acid W501 is required for RNA helicase activity but is not essential for DNA helicase activity of hepatitis C virus NS3 protein. J. Virol., 77, 571-582.
60. 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.
61. Falk, S., Weir, J. R., Hentschel, J., Reichelt, P., Bonneau, F. and Conti, E. (2014) The molecular architecture of the TRAMP complex reveals the organization and interplay of its two catalytic activities. Mol. Cell, 55, 856-867.
62. Schrodinger, LLC. (2010) The Py MOL Molecular Graphics System, Version 1.3r1.