Engagement of Arginine Finger to ATP Triggers Large Conformational Changes in NtrC1 AAA+ ATPase for Remodeling Bacterial RNA Polymerase

Structure

Volumn 18, Issue 11, 2010, Pages 1420-1430

  Chen, Baoyu ^a   Sysoeva, Tatyana A ^a   Chowdhury, Saikat ^a   Guo, Liang ^b   De Carlo, Sacha ^c   Hanson, Jeffrey A ^d,e   Yang, Haw ^d,e   Nixon, B Tracy ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; BACTERIAL RNA; RNA POLYMERASE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ARGININE; BACTERIA; DNA-DIRECTED RNA POLYMERASES; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; TRANSCRIPTION FACTORS;

AQUIFEX AEOLICUS; BACTERIA (MICROORGANISMS);

EID: 78149460165     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.08.018     Document Type: Article

References (36)

1. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.-W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, D66:213-221.
2. Batchelor J.D., Sterling H.J., Hong E., Williams E.R., Wemmer D.E. Receiver domains control the active-state stoichiometry of Aquifex aeolicus σ54 activator NtrC4, as revealed by electrospray ionization mass spectrometry. J. Mol. Biol. 2009, 393:634-643.
3. Bose D., Pape T., Burrows P.C., Rappas M., Wigneshweraraj S.R., Buck M., Zhang X. Organization of an activator-bound RNA polymerase holoenzyme. Mol. Cell 2008, 32:337-346.
4. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.-S., Kuszewski J., Nilges N., Pannu N.S., et al. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, D54:905-921.
5. Chen V.B., Davis I.W., Richardson D.C. KiNG (Kinmage, Next Generation): a versatile interactive molecular and scientific visualization program. Protein Sci. 2009, 18:2403-2409.
6. Chen B., Doucleff M., Wemmer D.E., De Carlo S., Huang H.C., Nogales E., Hoover T.R., Kondrashkina E., Guo L., Nixon B.T. ATP ground- and transition states of bacterial enhancer binding AAA+ ATPases support complex formation with their target protein, σ54. Structure 2007, 15:429-440.
7. Chen B., Sysoeva T.A., Chowdhury S., Guo L., Nixon B.T. ADPase activity of recombinantly expressed thermotolerant ATPases may be caused by co-purification of adenylate kinase of Escherichia coli. FEBS J. 2009, 276:807-815.
8. Davies J.M., Brunger A.T., Weis W.I. Improved structures of full-length p97, an AAA ATPase: Implications for mechanisms of nucleotide-dependent conformational change. Structure 2008, 16:715-726.
9. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
10. De Carlo S., Chen B., Hoover T.R., Kondrashkina E., Nogales E., Nixon B.T. The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev. 2006, 20:1485-1495.
11. Dekker J.P., Fodor A., Aldrich R.W., Yellen G. A perturbation-based method for calculating explicit likelihood of evolutionary co-variance in multiple sequence alignments. Bioinformatics 2004, 20:1565-1572.
12. Doucleff M., Chen B., Maris A.E., Wemmer D.E., Kondrashkina E., Nixon B.T. Negative regulation of AAA+ ATPase assembly by two component receiver domains: a transcription activation mechanism that is conserved in mesophilic and extremely hyperthermophilic bacteria. J. Mol. Biol. 2005, 353:242-255.
13. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, D60:2126-2132.
14. Fischetti R., Stepanov S., Rosenbaum G., Barrea R., Black E., Gore D., Heurich R., Kondrashkina E., Kropf A.J., Wang S., et al. The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source. J. Synchrotron Radiat. 2004, 11:399-405.
15. Hayward S., Berendsen H.J.C. Systemic analysis of domain motions in proteins from conformational change; new results on citrate synthase and T4 lysozyme. Proteins 1998, 30:144-154.
16. Joly N., Buck M. Engineered interfaces of an AAA+ ATPase reveal a new nucleotide-dependent coordination mechanism. J. Biol. Chem. 2010, 285:15178-15186.
17. Joly N., Burrows P.C., Buck M. An intramolecular route for coupling ATPase activity in AAA+ proteins for transcription activation. J. Biol. Chem. 2008, 283:13725-13735.
18. Joly N., Schumacher J., Buck M. Heterogeneous nucleotide occupancy stimulates functionality of phage shock protein F, an AAA+ transcriptional activator. J. Biol. Chem. 2006, 281:34997-35007.
19. Keegan R.M., Winn M.D. Automated search-model discovery and preparation for structure solution by molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 2007, D63:447-457.
20. Kozin M.B., Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 2001, 34:33-41.
21. Lee S.-Y., DeLaTorre A., Yan D., Kustu S., Nixon B.T., Wemmer D.E. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev. 2003, 17:2552-2563.
22. Mosca R., Schneider T.R. Alignment of protein structures in the presence of domain motions. BMC Bioinformatics 2008, 9:352-368.
23. Mosca R., Schneider T.R. RAPIDO: a web server for the alignment of protein structures in the presence of conformational changes. Nucleic Acids Res. 2008, 36:W42-W46.
24. Neuwald A.F., Aravind L., Spounge J.L., Koonin E.V. AAA+: A class of chaperonin-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 1999, 9:27-43.
25. Radermacher M., Wagenknecht T., Verschoor A., Frank J. Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc. 1987, 146:113-136.
26. Rappas M., Schumacher J., Beuron F., Niwa H., Bordes P., Wigneshweraraj S.R., Keetch C.A., Robinson C.V., Buck M., Zhang X. Structural insights into the activity of enhancer-binding proteins. Science 2005, 307:1972-1975.
27. Rappas M., Schumacher J., Niwa H., Buck M., Zhang X. Structural basis of the nucleotide driven conformational changes in the AAA+ domain of the transcription factor PspF. J. Mol. Biol. 2006, 357:481-492.
28. Rappas M., Bose D., Zhang X. Bacterial enhancer-binding proteins: unlocking σ54-dependent gene transcription. Curr. Opin. Struct. Biol. 2007, 17:110-116.
29. Sallai L., Tucker P.A. Crystal structure of the central and C-terminal domain of the sigma(54)-activator ZraR. J. Struct. Biol. 2005, 151:160-170.
30. Schumacher J., Joly N., Claeys-Bouuaert I.L., Azia S.A., Rappas M., Zhang X., Buck M. Mechanism of homotropic control to coordinate hydrolysis in a hexameric AAA+ ring ATPase. J. Mol. Biol. 2008, 381:1-12.
31. Terwilliger T.C. Maximum likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 2000, D56:965-972.
32. Theobald D.L., Wuttke D.S. Accurate structural correlations from maximum likelihood superpositions. PLoS Comput. Biol. 2008, 4:e43.
33. Thomsen N.D., Berger J.M. Structural framework for considering microbial protein- and nucleic acid-dependent motor ATPases. Mol. Microbiol. 2008, 69:1071-1090.
34. Tucker P.A., Sallai L. The AAA+ superfamily-a myriad of motions. Curr. Opin. Struct. Biol. 2007, 17:641-652.
35. Xu H., Gu B., Nixon B.T., Hoover T.R. Purification and characterization of the AAA+ domain of Sinorhizobium meliloti DctD, a σ54-dependent transcriptional activator. J. Bacteriol. 2004, 186:3499-3507.
36. Zhang X., Wigley D.B. The 'glutamate switch' provides a link between ATPase activity and ligand binding in AAA+ proteins. Nat. Struct. Mol. Biol. 2008, 15:1223-1227.