Phosphorylation-Induced Activation of the Response Regulator VraR from Staphylococcus aureus: Insights from Hydrogen Exchange Mass Spectrometry

Journal of Molecular Biology

Volumn 391, Issue 1, 2009, Pages 149-163

  Liu, Yu Hong ^a   Belcheva, Antoaneta ^b   Konermann, Lars ^a   Golemi Kotra, Dasantila ^b,c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

antibiotic resistance; conformational dynamics; MRSA VRSA; signal transduction; two component system

Indexed keywords

BACTERIAL PROTEIN; UNCLASSIFIED DRUG; VRAR PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; HYDROGEN BOND; HYDROGEN EXCHANGE MASS SPECTROMETRY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 67651087555     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.06.017     Document Type: Article

References (75)

1. Gao R., Mack T.R., and Stock A.M. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 32 (2007) 225-234
2. Skerker J.M., Prasol M.S., Perchuk B.S., Biondi E.G., and Laub M.T. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol. 3 (2005) 1770-1788
3. Yamamoto K., Hirao K., Oshima T., Aiba H., Utsumi R., and Ishihama A. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280 (2005) 1448-1456
4. Hoch J.A., and Varughese K.I. Keeping signals straight in phosphorelay signal transduction. J. Bacteriol. 183 (2001) 4941-4949
5. Thomas S.A., Brewster J.A., and Bourret R.B. Two variable active site residues modulate response regulator phosphoryl group stability. Mol. Microbiol. 69 (2008) 453-465
6. Utaida S., Dunman P.M., Macapagal D., Murphy E., Projan S.J., Singh V.K., et al. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149 (2003)
7. Mwangi M.M., Wu S.W., Zhou Y., Sieradzki K., de Lencastre H., Richardson P., et al. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc. Natl Acad. Sci. 104 (2007) 9451-9456
8. Walsh C. Where will new antibiotics come from?. Nat. Rev. Microbiol. 1 (2003) 65-70
9. Fuda C.C.S., Fisher J.F., and Mobashery S. β-Lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome. Cell. Mol. Life Sci. 62 (2005) 2617-2633
10. Varughese K.I. Rebuttal: beryllofluoride binding mimics phosphorylation of aspartate in response regulators. J. Bacteriol. 187 (2005) 8231
11. Boyle-Vavra S., Yin S., and Daum R.S. TheVraS/VraR two-component regulatory system required for oxacillin resistance in community-acquired methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 262 (2006) 163-171
12. Kuroda M., Kuroda H., Oshima T., Takeuchi F., Mori H., and Hiramatsu K. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol. Microbiol. 49 (2003) 807-821
13. Kuroda M., Kuwahara-Arai K., and Hiramatsu K. Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem. Biophys. Res. Commun. 269 (2000) 485-490
14. Gardete S., Wu S.W., Gill S., and Tomasz A. Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus. Antimicrob. Agents Chemother. 50 (2006) 3424-3434
15. Belcheva A., and Golemi-Kotra D. A close-up view of the VraSR two-component system: a mediator of Staphylococcus aureus response to cell wall damage. J. Biol. Chem. 283 (2008) 12354-12364
16. Baikalov I., Schrder I., Kaczor-Grzeskowiak M., Cascio D., Gunsalus R.P., and Dickerson R.E. NarL dimerization? Suggestive evidence from a new crystal form. Biochemistry 37 (1998) 3665-3676
17. Lee S.-Y., Cho H.S., Pelton J.G., Yan D., Berry E.A., and Wemmer D.E. Crystal structure of activated CheY comparison with other activated receiver domains. J. Biol. Chem. 276 (2001) 16425-16431
18. - activated response regulator CheY2. J. Mol. Biol. 338 (2004) 287-297
19. Stock A.M., Mottonen J.M., Stock J.B., and Schutt C.E. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature 337 (1989) 745-749
20. Milani M., Leoni L., Rampioni G., Zennaro E., Ascenzi P., and Bolognesi M. An active-like structure in the unphosphorylated StyR response regulator suggests a phosphorylation-dependent allosteric activation mechanism. Structure 13 (2005) 1289-1297
21. Simonovic M., and Volz K. A distinct meta-active conformation in the 1.1 Å resolution structure of wild-type ApoCheY. J. Biol. Chem. 276 (2001) 28637-28640
22. Buckler D.R., Zhou Y., and Stock A.M. Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermotoga maritima. Structure 10 (2002) 153-164
23. Baikalov I., Schrder I., Kaczor-Grzeskowiak M., Grzeskowiak K., Gunsalus R.P., and Dickerson R.E. Structure of the Escherichia coli response regulator NarL. Biochemistry 35 (1996) 11053-11061
24. Donaldson L.W. The NMR structure of the Staphylococcus aureus response regulator VraR DNA binding domain reveals a dynamic relationship between it and its associated receiver domain. Biochemistry 47 (2008) 3379-3388
25. Maris A.E., Kaczor-Grzeskowiak M., Ma Z., Kopka M.L., Gunsalus R.P., and Dickerson R.E. Primary and secondary modes of DNA recognition by the NarL two-component response regulator. Biochemistry 44 (2005) 14538-14552
26. Zhang J.H., Xiao G., Gunsalus R.P., and Hubbell W.L. Phosphorylation triggers domain separation in the DNA binding response regulator NarL. Biochemistry 42 (2003) 2552-2559
27. Maris A.E., Sawaya M.R., Kaczor-Grzeskowiak M., Jarvis M.R., Bearson S.M.D., Kopka M.L., et al. Dimerization allows DNA target site recognition by the NarL response regulator. Nat. Struct. Biol. 9 (2002) 771-778
28. Eldridge A.M., Kang H.-S., Johnson E., Gunsalus R., and Dahlquist F.W. Effect of phosphorylation on the interdomain interaction of the response regulator, NarL. Biochemistry 41 (2002) 15173-15180
29. Arnold K., Bordoli L., Kopp J., and Schwede T. The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 (2006) 195-201
30. Robinson V.L., Buckler D.R., and Stock A.M. A tale of two components: a novel kinase and a regulatory switch. Nat. Struct. Biol. 7 (2000) 626-633
31. Hastings C.A., Lee S.-Y., Cho H.S., Yan D., Kustu S., and Wemmer D.E. High-resolution solution structure of the beryllofluoride-activated NtrC receiver domain. Biochemistry 42 (2003) 9081-9090
32. Katta V., and Chait B.T. Conformational changes in proteins probed by hydrogen-exchange electrospray-ionisation mass spectrometry. Rapid Commun. Mass Spectrom. 5 (1991) 214-217
33. Ghaemmaghami S., Fitzgerald M.C., and Oas T.G. A quantitative, high-throughput screen for protein stability. Proc. Natl Acad. Sci. USA 97 (2000) 8296-8301
34. Englander S.W. Hydrogen exchange and mass spectrometry: a historical perspective. J. Am. Soc. Mass Spectrom. 17 (2006) 1481-1489
35. Eyles S.J., and Kaltashov I.A. Methods to study protein dynamics and folding by mass spectrometry. Methods 34 (2004) 88-99
36. Pan J.X., Rintala-Dempsey A., Li Y., Shaw G.S., and Konermann L. Folding kinetics of the S100A11 protein dimer studied by time-resolved electrospray mass spectrometry and pulsed hydrogen-deuterium exchange. Biochemistry 45 (2006) 3005-3013
37. Lanman J., Lam T.T., Barnes S., Sakalian M., Emmett M.R., Marshall A.G., et al. Identification of novel interactions in HIV-capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325 (2003) 759-772
38. Lu X., Wintrode P.L., and Surewicz W.K. β-Sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proc. Natl Acad. Sci. USA 104 (2007) 1510-1515
39. Wales T.E., and Engen J.R. Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25 (2006) 158-170
40. Zhu M.M., Rempel D.L., Du Z., and Gross M.L. Quantification of protein-ligand interactions by mass spectrometry, titration, and H/D exchange: PLIMSTEX. J. Am. Chem. Soc. 125 (2003) 5252-5253
41. Huzil J.T., Chik J.K., Slysz G.W., Freedman H., Tuszynski J., Taylor R.E., et al. A unique mode of microtubule stabilization induced by peloruside A. J. Mol. Biol. 378 (2008) 1016-1030
42. Chalmers M.J., Busby S.A., Pascal B.D., He Y., Hendrickson C.L., Marshall A.G., et al. Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 78 (2006) 1005-1014
43. Rand K.D., Adams C.M., Zubarev R.A., and Jorgensen T.J.D. Electron capture dissociation proceeds with a low degree of intramolecular migration of peptide amide hydrogens. J. Am. Chem. Soc. 130 (2008) 1341-1349
44. Rist W., Rodriguez F., Jorgensen T.J.D., and Mayer M.P. Analysis of subsecond protein dynamics by amide hydrogen exchange and mass spectrometry using a quench-flow setup. Protein Sci. 14 (2005) 626-632
45. Smith D.L., Deng Y., and Zhang Z. Probing the noncovalent structure of proteins by amide hydrogen exchange mass spectrometry. J. Mass Spectrom. 32 (1997) 135-146
46. Maier C.S., and Deinzer M.L. Protein conformations, interactions, and H/D exchange. Methods Enzymol. 402 (2005) 312-360
47. Uzawa T., Nishimura C., Akiyama S., Ishimori K., Takahashi S., Dyson H.J., et al. Hierarchical folding mechanism of apomyoglobin revealed by ultra-fast H/D exchange coupled with 2D NMR. Proc. Natl Acad. Sci. USA 105 (2008) 13859-13864
48. Krishna M.M.G., Hoang L., Lin Y., and Englander S.W. Hydrogen exchange methods to study protein folding. Methods 34 (2004) 51-64
49. Hughson F.M., Wright P.E., and Baldwin R.L. Structural characterisation of a partly folded apomyoglobin intermediate. Science 249 (1990) 1544-1548
50. Konermann L., Tong X., and Pan Y. Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches. J. Mass Spectrom. 43 (2008) 1021-1036
51. Woodward C. Advances in protein hydrogen exchange by mass spectrometry. J. Am. Soc. Mass Spectrom. 10 (1999) 672-674
52. Poliakov A., Jardine P., and Prevelige P.E. Hydrogen/deuterium exchange on protein solutions containing nucleic acids: utility of protamine sulfate. Rapid Commun. Mass Spectrom. 22 (2008) 2423-2428
53. Gonzalez de Peredo A., Saint-Pierre C., Latour J.-M., Michaud-Soret I., and Forest E. Conformational changes of the ferric uptake regulation protein upon metal activation and DNA binding; first evidence of structural homologies with the diphtheria toxin repressor. J. Mol. Biol. 310 (2001) 83-91
54. Sperry J.B., Wilcox J.M., and Gross M.L. Strong anion exchange for studying protein-DNA interactions by H/D exchange mass spectrometry. J. Am. Soc. Mass Spectrom. 19 (2008) 886-890
55. Sours K.M., Kwok S.C., Rachidi T., Lee T., Ring A., Hoofnagle A.N., et al. Hydrogen-exchange mass spectrometry reveals activation-induced changes in the conformational mobility of p38a MAP kinase. J. Mol. Biol. 379 (2008) 1075-1093
56. Marcoux J., Manb P., Castellan M., Vives C., Forest E., and Fieschi F. Conformational changes in p47phox upon activation highlighted by mass spectrometry coupled to hydrogen/deuterium exchange and limited proteolysis. FEBS Lett. 583 (2009) 835-840
57. Chen S., O'Reilly L.P., Smithgall T.E., and Engen J.R. Tyrosine phosphorylation in the SH3 domain disrupts negative regulatory interactions within the c-Abl kinase core. J. Mol. Biol. 383 (2008) 414-423
58. Hoofnagle A.N., Resing K.A., Goldsmith E.J., and Ahn N.G. Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl Acad. Sci. USA 98 (2001) 956-961
59. Hamuro Y., Wong L., Shaffer J., Kim J.S., Stranz D.D., Jennings P.A., et al. Phosphorylation driven motions in the COOH-terminal Src -deuterium exchange and mass spectrometry (DXMS). J. Mol. Biol. 323 (2002) 871-881
60. Hughes C.A., Mandell J.G., Anand G.S., Stock A.M., and Komives E.A. Phosphorylation causes subtle changes in solvent accessibility at the interdomain interface of methylesterase CheB. J. Mol. Biol. 307 (2001) 967-976
61. Feher V.A., and Cavanagh J. Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F. Nature 400 (1999) 289-293
62. Volkman B.F., Lipson D., Wemmer D.E., and Kern D. Two-state allosteric behavior in a single-domain signaling protein. Science 291 (2001) 2429-2433
63. Zhang H., Zhang C., Lajoie G.A., and Yeung K.K.-C. Selective sampling of phosphopeptides for detection by MALDI mass spectrometry. Anal. Chem. 77 (2005) 6078-6084
64. Miranker A., Robinson C.V., Radford S.E., and Dobson C.M. Investigation of protein folding by mass spectrometry. FASEB J. 10 (1996) 93-101
65. Kaltashov I.A., and Eyles S.J. Studies of biomolecular conformations and conformational dynamics by mass spectrometry. Mass Spectrom. Rev. 21 (2002) 37-71
66. Liu Y.-H., and Konermann L. Conformational dynamics of free and catalytically active thermolysin are indistinguishable by hydrogen/deuterium exchange mass spectrometry. Biochemistry 47 (2008) 6342-6351
67. Creighton T.E. Proteins (1993), W. H. Freeman, New York
68. Eliezer D., Yao J., Dyson H.J., and Wright P.E. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding. Nat. Struct. Biol. 5 (1998) 148-155
69. Wright P.E., and Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293 (1999) 321-331
70. Kern D., Volkman B.F., Luginbuhl P., Nohaile M.J., Kustu S., and Wemmer D.E. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 402 (1999) 894-898
71. Stock A.M., and Guhaniyogi J. A new perspective on response regulator activation. J. Bacteriol. 188 (2006) 7328-7330
72. Bai Y., Sosnick T.R., Mayne L., and Englander S.W. Protein folding intermediates: native state hydrogen exchange. Science 269 (1995) 192-197
73. Ulijasz A.T., Kay B.K., and Weisblum B. Peptide analogues of the vans catalytic center inhibit VanR binding to its cognate promoter. Biochemistry 39 (2000) 11417-11424
74. Weis D.D., Engen J.R., and Kass I.J. Semi-automated data processing of hydrogen exchange mass spectra using HDX-Express. J. Am. Soc. Mass Spectrom. 17 (2006) 1700-1703
75. Codreanu S.G., Ladner J.E., Xiao G., Stourman N.V., Hachey D.L., Gilliland G.L., et al. Local protein dynamics and catalysis: detection of segmental motion associated with rate-limiting product release by a glutathione transferase. Biochemistry 41 (2002) 15161-15172