Subunit dynamics and nucleotide-dependent asymmetry of an AAA+ transcription complex

Journal of Molecular Biology

Volumn 426, Issue 1, 2014, Pages 71-83

  Zhang, Nan ^a   Gordiyenko, Yuliya ^b   Joly, Nicolas ^c   Lawton, Edward ^a   Robinson, Carol V ^b   Buck, Martin ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

enhancer binding protein; native mass spectrometry; PspF; sigma 54

Indexed keywords

ADENOSINE TRIPHOSPHATE; MEDIATOR COMPLEX; NUCLEOTIDE; RNA POLYMERASE; TRANSCRIPTION COMPLEX AAA; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; HYDROLYSIS; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE BINDING SITE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TRANSCRIPTION INITIATION;

BACTERIA (MICROORGANISMS);

EID: 84890859658     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.08.018     Document Type: Article

References (65)

1. D. Bose, N. Joly, T. Pape, M Rappas, J. Schumacher, and M. Buck et al. Dissecting the ATP hydrolysis pathway of bacterial enhancer-binding proteins Biochem Soc Trans 36 2008 83 88
2. D.F. Browning, and S.J. Busby The regulation of bacterial transcription initiation Nat Rev Microbiol 2 2004 57 65
3. M. Buck, M.T. Gallegos, D.J. Studholme, Y. Guo, and J.D. Gralla The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor J Bacteriol 182 2000 4129 4136
4. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA + proteins Annu Rev Biophys Biomol Struct 35 2006 93 114
5. A.J. Wolfe, D.S. Millikan, J.M. Campbell, and K.L. Visick Vibrio fischeri sigma54 controls motility, biofilm formation, luminescence, and colonization Appl Environ Microbiol 70 2004 2520 2524
6. A. Mitra, P. Fay, J. Morgan, K. Vendura, S. Versaggi, and J. Riorda Sigma factor N, liaison to an ntrC and rpoS dependent regulatory pathway controlling acid resistance and the LEE in enterohemorrhagic Escherichia coli PLoS One 7 2012 e46288
7. M. Fisher, D. Grimm, A. Henion, A. Elias, P. Stewart, and PA. Rosa et al. Borrelia burgdorferi sigma54 is required for mammalian infection and vector transmission but not for tick colonization Proc Natl Acad Sci USA 102 2005 5162 5167
8. M. Bush, and R. Dixon The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription Microbiol Mol Biol Rev 76 2012 497 529
9. N. Joly, C. Engl, G. Jovanovic, M. Huvet, T. Toni, and X. Sheng et al. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology FEMS Microbiol Rev 34 2010 797 827
10. G. Jovanovic, J. Rakonjac, and P. Model In vivo and in vitro activities of the Escherichia coli sigma54 transcription activator, PspF, and its DNA-binding mutant, PspFDeltaHTH J Mol Biol 285 1999 469 483
11. J. Schumacher, N. Joly, M. Rappas, X. Zhang, and M. Buck Structures and organisation of AAA + enhancer binding proteins in transcriptional activation J Struct Biol 156 2006 190 199
12. H. Xu, B. Gu, B.T. Nixon, and T.R. Hoover Purification and characterization of the AAA + domain of Sinorhizobium meliloti DctD, a sigma54-dependent transcriptional activator J Bacteriol 186 2004 3499 3507
13. P. Bordes, S. Wigneshweraraj, J. Schumacher, and M. Buck The ATP hydrolyzing transcription activator phage shock protein F of Escherichia coli: identifying a surface that binds sigma 54 Proc Natl Acad Sci USA 100 2003 2278 2283
14. D. Bose, T. Pape, P.C. Burrows, M. Rappas, SR. Wigneshweraraj, and M. Buck et al. Organization of an activator-bound RNA polymerase holoenzyme Mol Cell 32 2008 337 346
15. Y. Guo, C.M. Lew, and J.D. Gralla Promoter opening by sigma(54) and sigma(70) RNA polymerases: sigma factor-directed alterations in the mechanism and tightness of control Genes Dev 14 2000 2242 2255
16. N. Zhang, N. Joly, PC. Burrows, M. Jovanovic, SR. Wigneshweraraj, and M. Buck The role of the conserved phenylalanine in the sigma54-interacting GAFTGA motif of bacterial enhancer binding proteins Nucleic Acids Res 37 2009 5981 5992
17. N. Zhang, N. Joly, and M. Buck A common feature from different subunits of a homomeric AAA + protein contacts three spatially distinct transcription elements Nucleic Acids Res 40 2012 9139 9152
18. K.S. Murakami X-ray crystal structure of Escherichia coli RNA polymerase sigma70 holoenzyme J Biol Chem 288 2013 9126 9134
19. K.S. Murakami, and S.A. Darst Bacterial RNA polymerases: the wholo story Curr Opin Struct Biol 13 2003 31 39
20. S. De Carlo, B. Chen, TR. Hoover, E. Kondrashkina, E. Nogales, and BT. Nixon The structural basis for regulated assembly and function of the transcriptional activator NtrC Genes Dev 20 2006 1485 1495
21. M. Rappas, J. Schumacher, F. Beuron, H. Niwa, P. Bordes, and S. Wigneshweraraj et al. Structural insights into the activity of enhancer-binding proteins Science 307 2005 1972 1975
22. L. Sallai, and P.A. Tucker Crystal structure of the central and C-terminal domain of the sigma(54)-activator ZraR J Struct Biol 151 2005 160 170
23. J. Schumacher, X. Zhang, S. Jones, P. Bordes, and M. Buck ATP-dependent transcriptional activation by bacterial PspF AAA + protein J Mol Biol 338 2004 863 875
24. B. Chen, TA. Sysoeva, S. Chowdhury, L. Guo, S. De Carlo, and JA. Hanson et al. Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA + ATPase for remodeling bacterial RNA polymerase Structure 18 2010 1420 1430
25. SY. Lee, A. De La Torre, D. Yan, S. Kustu, BT Nixon, and DE. Wemmer Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA + ATPase domains Genes Dev 17 2003 2552 2563
26. A. Martin, T.A. Baker, and R.T. Sauer Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines Nature 437 2005 1115 1120
27. N. Joly, J. Schumacher, and M. Buck Heterogeneous nucleotide occupancy stimulates functionality of phage shock protein F, an AAA + transcriptional activator J Biol Chem 281 2006 34997 35007
28. A. Dyachenko, R. Gruber, L. Shimon, A. Horovitz, and M. Sharon Allosteric mechanisms can be distinguished using structural mass spectrometry Proc Natl Acad Sci USA 110 2013 7235 7239
29. N. Morgner, F. Montenegro, N.P. Barrera, and C.V. Robinson Mass spectrometry - from peripheral proteins to membrane motors J Mol Biol 423 2012 1 13
30. R.J. Rose, E. Damoc, E. Denisov, A. Makarov, and A.J. Heck High-sensitivity orbitrap mass analysis of intact macromolecular assemblies Nat Methods 9 2012 1084 1086
31. W.V. Cannon, M.T. Gallegos, and M. Buck Isomerization of a binary sigma-promoter DNA complex by transcription activators Nat Struct Biol 7 2000 594 601
32. M. Chaney, R. Grande, SR. Wigneshweraraj, W. Cannon, P. Casaz, and MT. Gallegos et al. Binding of transcriptional activators to sigma 54 in the presence of the transition state analog ADP-aluminum fluoride: insights into activator mechanochemical action Genes Dev 15 2001 2282 2294
33. L.J. Friedman, and J. Gelles Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation Cell 148 2012 679 689
34. PC Burrows, N. Joly, W. Cannon, BP Camara, M. Rappas, and X. Zhang et al. Coupling sigma factor conformation to RNA polymerase reorganisation for DNA melting J Mol Biol 387 2009 306 319
35. N. Joly, M. Rappas, M. Buck, and X. Zhang Trapping of a transcription complex using a new nucleotide analogue: AMP aluminium fluoride J Mol Biol 375 2008 1206 1211
36. P.C. Burrows, N. Joly, and M. Buck A prehydrolysis state of an AAA + ATPase supports transcription activation of an enhancer-dependent RNA polymerase Proc Natl Acad Sci USA 107 2010 9376 9381
37. B. Chen, M. Doucleff, DE. Wemmer, S. De Carlo, HH. Huang, and E. Nogales et al. ATP ground- and transition states of bacterial enhancer binding AAA + ATPases support complex formation with their target protein, sigma54 Structure 15 2007 429 440
38. RN. Leach, C. Gell, S. Wigneshweraraj, M. Buck, A. Smith, and PG. Stockley Mapping ATP-dependent activation at a sigma54 promoter J Biol Chem 281 2006 33717 33726
39. I. Schlichting, and J. Reinstein pH influences fluoride coordination number of the AlFx phosphoryl transfer transition state analog Nat Struct Biol 6 1999 721 723
40. J.D. Batchelor, H.J. Sterling, E. Hong, E.R. Williams, and D.E. Wemmer Receiver domains control the active-state stoichiometry of Aquifex aeolicus sigma54 activator NtrC4, as revealed by electrospray ionization mass spectrometry J Mol Biol 393 2009 634 643
41. H.J. Sterling, J.D. Batchelor, D.E. Wemmer, and E.R. Williams Effects of buffer loading for electrospray ionization mass spectrometry of a noncovalent protein complex that requires high concentrations of essential salts J Am Soc Mass Spectrom 21 2010 1045 1049
42. S.N. Wanasundara, and M. Thachuk Theoretical investigations of the dissociation of charged protein complexes in the gas phase J Am Soc Mass Spectrom 18 2007 2242 2253
43. J.C. Jurchen, D.E. Garcia, and E.R. Williams Gas-phase dissociation pathways of multiply charged peptide clusters J Am Soc Mass Spectrom 14 2003 1373 1386
44. --dependent complexes between an AAA + ATPase and s54 FEBS Open Bio 2 2012 89 92
45. N. Joly, N. Zhang, and M. Buck ATPase site architecture is required for self-assembly and remodeling activity of a hexameric AAA + transcriptional activator Mol Cell 47 2012 484 490
46. M. Rappas, J. Schumacher, H. Niwa, M. Buck, and X. Zhang Structural basis of the nucleotide driven conformational changes in the AAA + domain of transcription activator PspF J Mol Biol 357 2006 481 492
47. N. Joly, P.C. Burrows, and M. Buck An intramolecular route for coupling ATPase activity in AAA + proteins for transcription activation J Biol Chem 283 2008 13725 13735
48. X. Zhang, and D.B. Wigley The "glutamate switch" provides a link between ATPase activity and ligand binding in AAA + proteins Nat Struct Mol Biol 15 2008 1223 1227
49. N. Joly, M. Rappas, S.R. Wigneshweraraj, X. Zhang, and M. Buck Coupling nucleotide hydrolysis to transcription activation performance in a bacterial enhancer binding protein Mol Microbiol 66 2007 583 595
50. N. Joly, and M. Buck Single chain forms of the enhancer binding protein PspF provide insights into geometric requirements for gene activation J Biol Chem 286 2011 12734 12742
51. N. Joly, and M. Buck Engineered interfaces of an AAA + ATPase reveal a new nucleotide-dependent coordination mechanism J Biol Chem 285 2010 15178 15186
52. C. Bieniossek, T. Schalch, M. Bumann, M. Meister, R. Meier, and U. Baum The molecular architecture of the metalloprotease FtsH Proc Natl Acad Sci USA 103 2006 3066 3071
53. M. Bochtler, C. Hartmann, HK. Song, GP Bourenkov, HD. Bartunik, and R. ĆHuber The structures of HsIU and the ATP-dependent protease HsIU-HsIV Nature 403 2000 800 805
54. G.L. Hersch, R.E. Burton, D.N. Bolon, T.A. Baker, and R.T. Sauer Asymmetric interactions of ATP with the AAA + ClpX6 unfoldase: allosteric control of a protein machine Cell 121 2005 1017 1027
55. R. Suno, H. Niwa, D. Tsuchiya, X. Zhang, M. Yoshida, and K. Morikawa Structure of the whole cytosolic region of ATP-dependent protease FtsH Mol Cell 22 2006 575 585
56. J.A. Yakamavich, T.A. Baker, and R.T. Sauer Asymmetric nucleotide transactions of the HslUV protease J Mol Biol 380 2008 946 957
57. A. Costa, I. IIves, N. Tamberg, T. Petojevic, E. Nogales, and MR. Botchan et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45 Nat Struct Mol Biol 18 2011 471 477
58. S.E. Glynn, A. Martin, A.R. Nager, T.A. Baker, and R.T. Sauer Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA + protein-unfolding machine Cell 139 2009 744 756
59. G. Meinke, P.A. Bullock, and A. Bohm Crystal structure of the simian virus 40 large T-antigen origin-binding domain J Virol 80 2006 4304 4312
60. E. Skordalakes, and J.M. Berger Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading Cell 114 2003 135 146
61. R.M. Story, I.T. Weber, and T.A. Steitz The structure of the E. coli recA protein monomer and polymer Nature 355 1992 318 325
62. F. Sobott, H. Hernandez, M.G. McCammon, M.A. Tito, and C.V. Robinson A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies Anal Chem 74 2002 1402 1407
63. I.V. Chernushevich, and B.A. Thomson Collisional cooling of large ions in electrospray mass spectrometry Anal Chem 76 2004 1754 1760
64. EJ. Nettleton, M. Sunde, Z. Lai, JW. Kelly, CM. Dobson, and CV. Robinson Protein subunit interactions and structural integrity of amyloidogenic transthyretins: evidence from electrospray mass spectrometry J Mol Biol 281 1998 553 564
65. +-ATPase activity Methods Enzymol 156 1988 116 119