Unusual, dual endo- and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1

Structure

Volumn 19, Issue 9, 2011, Pages 1241-1251

  Newman, Joseph A ^a   Hewitt, Lorraine ^a   Rodrigues, Cecilia ^a   Solovyova, Alexandra ^a   Harwood, Colin R ^a   Lewis, Richard J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; EXONUCLEASE; METALLO BETA LACTAMASE; RIBONUCLEASE; RNASE J1 ENZYME; RNASE J2 ENZYME; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; PRIORITY JOURNAL; RNA BINDING;

AMINO ACID MOTIFS; BACILLUS SUBTILIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RIBONUCLEASES; RNA; STRUCTURAL HOMOLOGY, PROTEIN;

BACILLUS SUBTILIS;

EID: 80052458661     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.06.017     Document Type: Article

References (37)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. R.A. Britton, T. Wen, L. Schaefer, O. Pellegrini, W.C. Uicker, N. Mathy, C. Tobin, R. Daou, J. Szyk, and C. Condon Maturation of the 5′ end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1 Mol. Microbiol. 63 2007 127 138 (Pubitemid 44968114)
3. J.V. Bugrysheva, and J.R. Scott The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes Mol. Microbiol. 75 2010 731 743
4. I. Callebaut, D. Moshous, J.P. Mornon, and J.P. de Villartay Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family Nucleic Acids Res. 30 2002 3592 3601 (Pubitemid 34919215)
5. V.B. Chen, W.B.I.I.I. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
6. B. Clouet-d'Orval, D. Rinaldi, Y. Quentin, and A.J. Carpousis Euryarchaeal beta-CASP proteins with homology to bacterial RNase J have 5′- to 3′-exoribonuclease activity J. Biol. Chem. 285 2010 17574 17583
7. F.M. Commichau, F.M. Rothe, C. Herzberg, E. Wagner, D. Hellwig, M. Lehnik-Habrink, E. Hammer, U. Völker, and J. Stülke Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing Mol. Cell. Proteomics 8 2009 1350 1360
8. C. Condon What is the role of RNase J in mRNA turnover? RNA Biol. 7 2010 316 321
9. R. Daou-Chabo, and C. Condon RNase J1 endonuclease activity as a probe of RNA secondary structure RNA 15 2009 1417 1425
10. R. Daou-Chabo, N. Mathy, L. Bénard, and C. Condon Ribosomes initiating translation of the hbs mRNA protect it from 5′-to-3′ exoribonucleolytic degradation by RNase J1 Mol. Microbiol. 71 2009 1538 1550
11. G. Deikus, C. Condon, and D.H. Bechhofer Role of Bacillus subtilis RNase J1 endonuclease and 5′-exonuclease activities in trp leader RNA turnover J. Biol. Chem. 283 2008 17158 17167
12. A. Dorléans, I.L. de la Sierra-Gallay, J. Piton, L. Zig, L. Winieski, H. Putzer, and C. Condon Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′-3′ exo-endoribonuclease RNase J Structure 19 2011 1252 1261 this issue
13. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
14. N. Eswar, B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M. Shen, U. Pieper, and A. Sali Comparative protein structure modeling using Modeller Curr. Protoc. Bioinformatics 15 2006 5.6.1 5.6.30
15. S. Even, O. Pellegrini, L. Zig, V. Labas, J. Vinh, D. Bréchemmier-Baey, and H. Putzer Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E Nucleic Acids Res. 33 2005 2141 2152 (Pubitemid 41439882)
16. J. García De La Torre, M.L. Huertas, and B. Carrasco Calculation of hydrodynamic properties of globular proteins from their atomic-level structure Biophys. J. 78 2000 719 730 (Pubitemid 30211830)
17. J.F. Gibrat, T. Madej, and S.H. Bryant Surprising similarities in structure comparison Curr. Opin. Struct. Biol. 6 1996 377 385 (Pubitemid 26197439)
18. H. Ishikawa, N. Nakagawa, S. Kuramitsu, and R. Masui Crystal structure of TTHA0252 from Thermus thermophilus HB8, a RNA degradation protein of the metallo-beta-lactamase superfamily J. Biochem. 140 2006 535 542 (Pubitemid 44870918)
19. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
20. K. Kobayashi, S.D. Ehrlich, A. Albertini, G. Amati, K.K. Andersen, M. Arnaud, K. Asai, S. Ashikaga, S. Aymerich, and P. Bessieres Essential Bacillus subtilis genes Proc. Natl. Acad. Sci. USA 100 2003 4678 4683 (Pubitemid 36457789)
21. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268 (Pubitemid 41742778)
22. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
23. T. Laue, B. Shah, T. Ridgeway, and S. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S.E. Harding, A.J. Rowe, J.C. Horton, In Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 Royal Society of Chemistry Cambridge 90 125
24. M. Lehnik-Habrink, H. Pförtner, L. Rempeters, N. Pietack, C. Herzberg, and J. Stülke The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex Mol. Microbiol. 77 2010 958 971
25. I. Li de la Sierra-Gallay, L. Zig, A. Jamalli, and H. Putzer Structural insights into the dual activity of RNase J Nat. Struct. Mol. Biol. 15 2008 206 212 (Pubitemid 351207513)
26. U. Mäder, L. Zig, J. Kretschmer, G. Homuth, and H. Putzer mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale Mol. Microbiol. 70 2008 183 196
27. C.R. Mandel, S. Kaneko, H. Zhang, D. Gebauer, V. Vethantham, J.L. Manley, and L. Tong Polyadenylation factor CPSF-73 is the pre-mRNA 3′-end- processing endonuclease Nature 444 2006 953 956 (Pubitemid 46025011)
28. N. Mathy, L. Bénard, O. Pellegrini, R. Daou, T. Wen, and C. Condon 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA Cell 129 2007 681 692 (Pubitemid 46802375)
29. N. Mathy, A. Hébert, P. Mervelet, L. Bénard, A. Dorléans, I. Li de la Sierra-Gallay, P. Noirot, H. Putzer, and C. Condon Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour Mol. Microbiol. 75 2010 489 498
30. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674 (Pubitemid 47080256)
31. Y. Nishida, H. Ishikawa, S. Baba, N. Nakagawa, S. Kuramitsu, and R. Masui Crystal structure of an archaeal cleavage and polyadenylation specificity factor subunit from Pyrococcus horikoshii Proteins 78 2010 2395 2398
32. G.P. Poornam, A. Matsumoto, H. Ishida, and S. Hayward A method for the analysis of domain movements in large biomolecular complexes Proteins 76 2009 201 212
33. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619 (Pubitemid 30141584)
34. K. Shahbabian, A. Jamalli, L. Zig, and H. Putzer RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis EMBO J. 28 2009 3523 3533
35. S. Yao, and D.H. Bechhofer Initiation of decay of Bacillus subtilis rpsO mRNA by endoribonuclease RNase Y J. Bacteriol. 192 2010 3279 3286
36. S. Yao, J.B. Blaustein, and D.H. Bechhofer Processing of Bacillus subtilis small cytoplasmic RNA: evidence for an additional endonuclease cleavage site Nucleic Acids Res. 35 2007 4464 4473 (Pubitemid 47244597)
37. S. Yao, J.S. Sharp, and D.H. Bechhofer Bacillus subtilis RNase J1 endonuclease and 5′ exonuclease activities in the turnover of DeltaermC mRNA RNA 15 2009 2331 2339