Structural and functional analysis of the archaeal endonuclease Nob1

Nucleic Acids Research

Volumn 40, Issue 7, 2012, Pages 3259-3274

  Veith, Thomas ^a   Martin, Roman ^a   Wurm, Jan P ^a   Weis, Benjamin L ^a   Duchardt Ferner, Elke ^a   Safferthal, Charlotta ^a   Hennig, Raoul ^a   Mirus, Oliver ^a   Bohnsack, Markus T ^a   Wöhnert, Jens ^a   Schleiff, Enrico ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENDONUCLEASE; ENDONUCLEASE NOB1; MANGANESE; NUCLEASE; PRERIBOSOMAL RNA; RNA; SMALL SUBUNIT RIBOSOMAL RNA; UNCLASSIFIED DRUG;

ARCHAEON; ARTICLE; BIOGENESIS; CATALYSIS; CONTROLLED STUDY; ENZYME STRUCTURE; EUKARYOTE; GENETIC CONSERVATION; MICROBIAL COMMUNITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PYROCOCCUS HORIKOSHII; RIBOSOME; RNA CLEAVAGE; STRUCTURE ANALYSIS; YEAST;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CATALYTIC DOMAIN; ENDORIBONUCLEASES; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PYROCOCCUS HORIKOSHII; RNA; RNA, RIBOSOMAL; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

EID: 84860144395     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1186     Document Type: Article

References (82)

1. Schmeing, T.M. and Ramakrishnan, V. (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature, 461, 1234-1242.
2. Dunkle, J.A. and Cate, J.H. (2010) Ribosome structure and dynamics during translocation and termination. Annu. Rev. Biophys., 39, 227-244.
3. Nierhaus, K.H. (1991) The assembly of prokaryotic ribosomes. Biochimie, 73, 739-755.
4. Kaczanowska, M. and Rydë-Aulin, M. (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev., 71, 477-494. (Pubitemid 47429282)
5. Connolly, K. and Culver, G. (2009) Deconstructing ribosome construction. Trends Biochem. Sci., 34, 256-263.
6. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003) Ribosome assembly in eukaryotes. Gene, 313, 17-42. (Pubitemid 37338237)
7. Tschochner, H. and Hurt, E. (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol., 13, 255-263. (Pubitemid 36556010)
8. Henras, A.K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol. Life Sci., 65, 2334-2359.
9. Venema, J. and Tollervey, D. (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet., 33, 261-311. (Pubitemid 30083125)
10. Thomson, E. and Tollervey, D. (2010) The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol., 30, 976-984.
11. Zemp, I. and Kutay, U. (2007) Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett., 581, 2783-2793. (Pubitemid 46881154)
12. Fatica, A., Oeffinger, M., Dlakic M. and Tollervey, D. (2003) Nob1p is required for cleavage of the 30 end of 18S rRNA. Mol. Cell Biol., 23, 1798-1807. (Pubitemid 36246059)
13. Pertschy, B., Schneider, C., Gnädig, M., Schäfer, T., Tollervey, D. and Hurt, E. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20S to 18S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem., 284, 35079-35091.
14. Bohnsack, M.T., Martin, R., Granneman, S., Ruprecht, M., Schleiff, E. and Tollervey, D. (2009) Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell, 36, 583-592.
15. Lamanna, A.C. and Karbstein, K. (2011) An RNA conformational switch regulates pre-18S rRNA cleavage. J. Mol. Biol., 405, 3-17.
16. Lafontaine, D., Delcour, J., Glasser, A.L., Desgres, J. and Vandenhaute, J. (1994) The DIM1 gene responsible for the conserved m62Am62A dimethylation in the 30-terminal loop of 18 S rRNA is essential in yeast. J. Mol. Biol., 241, 492-497.
17. Fassio, C.A., Schofield, B.J., Seiser, R.M., Johnson, A.W. and Lycan, D.E. (2010) Dominant mutations in the late 40S biogenesis factor Ltv1 affect cytoplasmic maturation of the small ribosomal subunit in Saccharomyces cerevisiae. Genetics, 185, 199-209.
18. Neueder, A., Jakob, S., Pöll, G., Linnemann, J., Deutzmann, R., Tschochner, H. and Milkereit, P. (2010) A local role for the small ribosomal subunit primary binder rpS5 in final 18S rRNA processing in yeast. PLoS One, 5, e10194.
19. Tone, Y., Tanahashi, N., Tanaka, K., Fujimuro, M., Yokosawa, H. and Toh-e, A. (2000) Nob1p, a new essential protein, associates with the 26S proteasome of growing Saccharomyces cerevisiae cells. Gene, 243, 37-45. (Pubitemid 30079703)
20. Lamanna, A.C. and Karbstein, K. (2009) Nob1 binds the single-stranded cleavage site D at the 30-end of 18S rRNA with its PIN domain. Proc. Natl Acad. Sci. USA, 106, 14259-14264.
21. Granneman, S., Petfalski, E., Swiatkowska, A. and Tollervey, D. (2010) Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J., 29, 2026-2036.
22. Arcus, V.L., Bäckbro, K., Roos, A., Daniel, E.L. and Baker, E.N. (2004) Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J. Biol. Chem., 279, 16471-16478. (Pubitemid 38509345)
23. Lebreton, A., Tomecki, R., Dziembowski, A. and Sëaphin, B. (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature, 456, 993-996.
24. Qian, X., Gozani, S.N., Yoon, H., Jeon, C.J., Agarwal, K. and Weiss, M.A. (1993) Novel zinc finger motif in the basal transcriptional machinery: three-dimensional NMR studies of the nucleic acid binding domain of transcriptional elongation factor TFIIS. Biochem., 32, 9944-9959. (Pubitemid 23312420)
25. Woolls, H.A., Lamanna, A.C. and Karbstein, K. (2011) Roles of Dim2 in ribosome assembly. J. Biol. Chem., 286, 2578-2586.
26. Fatica, A., Tollervey, D. and Dlakic M. (2004) PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA, 10, 1698-1701. (Pubitemid 39426368)
27. 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.
28. 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.
29. Huntzinger, E., Kashima, I., Fauser, M., Sauliè re, J. and Izaurralde, E. (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA, 14, 2609-2617.
30. Wild, T., Horvath, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csucs, G., Lund, E. and Kutay, U. (2010) A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol., 8, e1000522.
31. Wyler, E., Zimmermann, M., Widmann, B., Gstaiger, M., Pfannstiel, J., Kutay, U. and Zemp, I. (2011) Tandem affinity purification combined with inducible shRNA expression as a tool to study the maturation of macromolecular assemblies. RNA, 17, 189-200.
32. Oehler, V.G., Yeung, K.Y., Choi, Y.E., Bumgarner, R.E., Raftery, A.E. and Radich, J.P. (2009) The derivation of diagnostic markers of chronic myeloid leukemia progression from microarray data. Blood, 114, 3292-3298.
33. Lin, Y., Peng, S., Yu, H., Teng, H. and Cui, M. (2011) RNAi-mediated downregulation of NOB1 suppresses the growth and colony-formation ability of human ovarian cancer cells. Med. Oncol., February 2 (doi:10.1007/s12032-010- 9808-5; epub ahead of print).
34. Han, Y., Hong, L., Chen, Y., Zhong, C., Wang, Y., Zhao, D., Xue, T., Qiao, L. and Qiu, J. (2011) Up-regulation of Nob1 in the rat auditory system with noise-induced hearing loss. Neurosci. Lett., 491, 79-82.
35. LaRonde-LeBlanc, N. and Wlodawer, A. (2004) Crystal structure of A. fulgidus Rio2 defines a new family of serine protein kinases. Structure, 12, 1585-1594. (Pubitemid 39200512)
36. Coltri, P.P., Guimarães, B.G., Granato, D.C., Luz, J.S., Teixeira, E.C., Oliveira, C.C. and Zanchin, N.I. (2007) Structural insights into the interaction of the Nip7 PUA domain with polyuridine RNA. Biochemistry, 46, 14177-14787.
37. Taylor, A.B., Meyer, B., Leal, B.Z., Kötter, P., Schirf, V., Demeler, B., Hart, P.J., Entian, K.D. and Wöhnert, J. (2008) The crystal structure of Nep1 reveals an extended SPOUT-class methyltransferase fold and a pre-organized SAM-binding site. Nucleic Acids Res., 36, 1542-1554. (Pubitemid 351426107)
38. Ng, C.L., Waterman, D.G., Koonin, E.V., Walters, A.D., Chong, J.P., Isupov, M.N., Lebedev, A.A., Bunka, D.H., Stockley, P.G. and Ortiz-Lombard, M. (2009) Conformational flexibility and molecular interactions of an archaeal homologue of the Shwachman-Bodian-Diamond syndrome protein. BMC Struct. Biol., 9, 32.
39. Pulicherla, N., Pogorzala, L.A., Xu, Z.O., Farrell, H.C., Musayev, F.N., Scarsdale, J.N., Sia, E.A., Culver, G.M. and Rife, J.P. (2009) Structural and functional divergence within the Dim1/KsgA family of rRNA methyltransferases. J. Mol. Biol., 391, 884-893.
40. Jia, M.Z., Horita, S., Nagata, K. and Tanokura, M. (2010) An archaeal Dim2-like protein, aDim2p, fo, rms a ternary complex with a/eIF2 alpha and the 30 end fragment of 16S rRNA. J. Mol. Biol., 398, 774-785.
41. Finn, R.D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J.E., Gavin, O.L., Gunasekaran, P., Ceric, G., Forslund, K. et al. (2010) The Pfam protein families database. Nucleic Acids Res., 38, D211-D222.
42. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402. (Pubitemid 27359211)
43. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. and Sayers, E.W. (2009) GenBank. Nucleic Acids Res., 37, D26-D31.
44. Whelan, S. and Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol., 18, 691-699. (Pubitemid 32372940)
45. Stamatakis, A., Hoover, P. and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol., 57, 758-771.
46. Katoh, K. and Toh, H. (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics, 26, 1899-1900.
47. Leulliot, N., Bohnsack, M.T., Graille, M., Tollervey, D. and Van Tilbeurgh, H. (2008) The yeast ribosome synthesis factor Emg1 is a novel member of the superfamily of alpha/beta knot fold methyltransferases. Nucleic Acids Res., 36, 629-639. (Pubitemid 351255435)
48. Veith, T., Wurm, J.P., Duchardt-Ferner, E., Weis, B., Hennig, R., Martin, R., Safferthal, C., Bohnsack, M.T., Schleiff, E. and Wöhnert, J. (2011) NMR resonance assignments for an archaeal homolog of the endonuclease Nob1 involved in ribosome biogenesis. Biomol., NMR Assign, July 6 (doi:10.1007/s12104-011-9323-4; epub ahead of print).
49. Wurm, J.P., Duchardt, E., Meyer, B., Leal, B.Z., Kötter, P., Entian, K.D. and Wöhnert, J. (2009) Backbone resonance assignments of the 48 kDa dimeric putative 18S rRNA-methyltransferase Nep1 from Methanocaldococcus jannaschii. Biomol. NMR Assign., 3, 251-254.
50. Farrow, N.A., Muhandiram, R., Singer, A.U., Pascal, S.M., Kay, C.M., Gish, G., Shoelson, S.E., Pawson, T., Forman-Kay, J.D. and Kay, L.E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochem., 33, 5984-6003. (Pubitemid 24184605)
51. Keller, R. (2004) The Computer Aided Resonance Tutorial. CANTINA Verlag, Goldau, Switzerland.
52. Shen, Y., Delaglio, F., Cornilescu, G. and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 44, 213-223.
53. Cordier, F. and Grzesiek, S. (1999) Direct observation of hydrogen bonds in proteins by interresidue 3hJNC 0 scalar couplings. J. Am. Chem Soc., 121, 1601-1602. (Pubitemid 29108715)
54. Herrmann, T., Güntert, P. and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR, 24, 171-189. (Pubitemid 36113646)
55. Fiorito, F., Damberger, F., Herrmann, T. and Wüthrich, K. (2008) Automated amino acid side-chain NMR assignment of proteins using (13)C-and (15)N-resolved 3D [(1)H, (1)H]-NOESY. J. Biomol. NMR, 42, 23-33.
56. Güntert, P., Mumenthaler, C. and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-293.
57. Ohlenschläger, O., Seiboth, T., Zengerling, H., Briese, L., Marchanka, A., Ramachandran, R., Baum, M., Korbas, M. and Meyer-Klaucke, W. (2006) Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7. Oncogene, 25, 5953-5959. (Pubitemid 44477289)
58. Luginbühl, P., Güntert, P., Billeter, M. and Wüthrich, K. (1996) The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules. J. Biomol. NMR, 8, 136-146. (Pubitemid 126706783)
59. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51-54.
60. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
61. Murzin, A.G., Brenner, S.E., Hubbard, T. and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol., 247, 536-540.
62. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The protein data bank. Nucleic Acids Res., 28, 235-242. (Pubitemid 30047768)
63. Konagurthu, A.S., Whisstock, J.C., Stuckey, P.J. and Lesk, A.M. (2006) MUSTANG: a multiple structural alignment algorithm. Proteins, 64, 559-574. (Pubitemid 44100724)
64. Stamatakis, A. (2006) "RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic analyses with Thousands of Taxa and Mixed Models". Bioinformatics, 22, 2688-2690. (Pubitemid 44642609)
65. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance and Maximum Parsimony Methods. Mol. Biol. Evol., 28, 2731-2739.
66. Schägger, H. (2006) Tricin-SDS-PAGE. Nat. Prot., 1, 16-22.
67. Huber, H., Hohn, M.J., Stetter, K.O. and Rachel, R. (2003) The phylum Nanoarchaeota: present knowledge and future perspectives of a unique form of life. Res. Microbiol., 154, 165-171. (Pubitemid 36428705)
68. Waters, E., Hohn, M.J., Ahel, I., Graham, D.E., Adams, M.D., Barnstead, M., Beeson, K.Y., Bibbs, L., Bolanos, R., Keller, M. et al. (2003) The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA, 100, 12984-12988. (Pubitemid 37340012)
69. Fahrni, C.J. and O'Halloran, T.V. (1999) Aqueous coordination chemistry of quinoline-based fluorescence probes for the biological chemistry of zinc. J. Am. Chem. Soc., 121, 11448-11458.
70. Eghbalnia, H.R., Wang, L., Bahrami, A., Assadi, A. and Markley, J.L. (2005) Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements. J. Biomol. NMR, 32, 71-81. (Pubitemid 41086469)
71. Kornhaber, G.J., Snyder, D., Moseley, H.N. and Montelione, G.T. (2006) Identification of zinc-ligated cysteine residues based on 13Calpha and 13Cbeta chemical shift data. J. Biomol. NMR, 34, 259-269.
72. 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. (Pubitemid 44658529)
73. Takeshita, D., Zenno, S., Lee, W.C., Saigo, K. and Tanokura, M. (2007) Crystal structure of the PIN domain of human telomerase-associated protein EST1A. Proteins, 68, 980-989. (Pubitemid 47434719)
74. Levin, I., Schwarzenbacher, R., Page, R., Abdubek, P., Ambing, E., Biorac, T., Brinen, L.S., Campbell, J., Canaves, J.M., Chiu, H.J. et al. (2004) Crystal structure of a PIN (PilT N-terminus) domain (AF0591) from Archaeoglobus fulgidus at 1.90 A resolution. Proteins, 56, 404-408. (Pubitemid 38850176)
75. Okuda, M., Tanaka, A., Arai, Y., Satoh, M., Okamura, H., Nagadoi, A., Hanaoka, F., Ohkuma, Y. and Nishimura, Y. (2004) A novel zinc finger structure in the large subunit of human general transcription factor TFIIE. J. Biol. Chem., 279, 51395-51403. (Pubitemid 40017887)
76. Nguyen, C.D., Mansfield, R.E., Leung, W., Vaz, P.M., Loughlin, F.E., Grant, R.P. and Mackay, J.P. (2011) Characterization of a family of RanBP2-type zinc fingers that can recognize single-stranded RNA. J. Mol. Biol., 407, 273-283.
77. Loughlin, F.E., Mansfield, R.E., Vaz, P.M., McGrath, A.P., Setiyaputra, S., Gamsjaeger, R., Chen, E.S., Morris, B.J., Guss, J.M. and Mackay, J.P. (2009) The zinc fingers of the SR-like protein ZRANB2 are single-stranded RNA-binding domains that recognize 50 splice site-like sequences. Proc. Natl Acad. Sci. USA, 106, 5581-5586.
78. Karow, A.R. and Klostermeier, D. (2010) A structural model for the DEAD box helicase YxiN in solution: localization of the RNA binding domain. J. Mol. Biol., 402, 629-642.
79. Hardin, J.W., Hu, Y.X. and McKay, D.B. (2010) Structure of the RNA binding domain of a DEAD-box helicase bound to its ribosomal RNA target reveals a novel mode of recognition by an RNA recognition motif. J. Mol. Biol., 402, 412-427.
80. Rudolph, M.G. and Klostermeier, D. (2009) The Thermus thermophilus DEAD box helicase Hera contains a modified RNA recognition motif domain loosely connected to the helicase core. RNA, 15, 1993-2001.
81. Macrae, I.J., Zhou, K., Li, F., Repic, A., Brooks, A.N., Cande, W.Z., Adams, P.D. and Doudna, J.A. (2006) Structural basis for double-stranded RNA processing by Dicer. Science, 311, 195-198. (Pubitemid 43108178)
82. Ben-Shem, A., Jenner, L., Yusupova, G. and Yusupov, M. (2010) Crystal structure of the eukaryotic ribosome. Science, 330, 1203-1209.