Structure, Regulation, and Inhibition of the Quorum-Sensing Signal Integrator LuxO

PLoS Biology

Volumn 14, Issue 5, 2016, Pages

  Boyaci, Hande ^a   Shah, Tayyab ^a,d   Hurley, Amanda ^a   Kokona, Bashkim ^b   Li, Zhijie ^a,e   Ventocilla, Christian ^a,f   Jeffrey, Philip D ^a   Semmelhack, Martin F ^a   Fairman, Robert ^b   Bassler, Bonnie L ^a,c   Hughson, Frederick M ^a  

^a PRINCETON UNIVERSITY   (United States)

^b HAVERFORD COLLEGE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

^f Hager Biosciences LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZAURACIL; BACTERIAL PROTEIN; REPRESSOR PROTEIN; URACIL;

ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN DOMAINS; REPRESSOR PROTEINS; URACIL;

EID: 84971515143     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002464     Document Type: Article

References (39)

1. Rutherford ST, Bassler BL, Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med. 2012;2(11). Epub 2012/11/06. doi: 10.1101/cshperspect.a01242723125205; PubMed Central PMCID: PMC3543102.
2. Jung SA, Chapman CA, Ng WL, Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoS Pathog. 2015;11(4):e1004837. doi: 10.1371/journal.ppat.100483725874462; PubMed Central PMCID: PMC4398556.
3. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL, Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell. 2002;110(3):303–14. 12176318.
4. Shao Y, Bassler BL, Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol. 2014;92(5):921–30. doi: 10.1111/mmi.1259924698180; PubMed Central PMCID: PMC4038675.
5. Hammer BK, Bassler BL, Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol. 2003;50(1):101–4. 14507367.
6. Clatworthy AE, Pierson E, Hung DT, Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol. 2007;3(9):541–8. Epub 2007/08/22. doi: 10.1038/nchembio.2007.2417710100.
7. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL, The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature. 2007;450(7171):883–6. Epub 2007/11/16. nature06284 [pii] doi: 10.1038/nature0628418004304.
8. Ng WL, Perez L, Cong J, Semmelhack MF, Bassler BL, Broad spectrum pro-quorum-sensing molecules as inhibitors of virulence in vibrios. PLoS Pathog. 2012;8(6):e1002767. Epub 2012/07/05. doi: 10.1371/journal.ppat.100276722761573; PubMed Central PMCID: PMC3386246.
9. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL, The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004;118(1):69–82. 15242645.
10. Rutherford ST, van Kessel JC, Shao Y, Bassler BL, AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev. 2011;25(4):397–408. Epub 2011/02/18. 25/4/397 [pii]. doi: 10.1101/gad.201501121325136.
11. Nadell CD, Xavier JB, Levin SA, Foster KR, The evolution of quorum sensing in bacterial biofilms. PLoS Biol. 2008;6(1):e14. Epub 2008/02/01. doi: 10.1371/journal.pbio.006001418232735; PubMed Central PMCID: PMC2214811.
12. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ, Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A. 2002;99(5):3129–34. 11854465.
13. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17(1):7–15. doi: 10.3201/eid1701.091101p121192848; PubMed Central PMCID: PMC3375761.
14. Bush M, Dixon R, The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription. Microbiol Mol Biol Rev. 2012;76(3):497–529. doi: 10.1128/MMBR.00006-1222933558; PubMed Central PMCID: PMC3429621.
15. Joly N, Zhang N, Buck M, Zhang X, Coupling AAA protein function to regulated gene expression. Biochim Biophys Acta. 2012;1823(1):108–16. doi: 10.1016/j.bbamcr.2011.08.01221906631.
16. Erzberger JP, Berger JM, Evolutionary relationships and structural mechanisms of AAA+ proteins. Ann Rev Biophys Biomol Struct. 2006;35:93–114. Epub 2006/05/13. doi: 10.1146/annurev.biophys.35.040405.10193316689629.
17. Sysoeva TA, Chowdhury S, Guo L, Nixon BT, Nucleotide-induced asymmetry within ATPase activator ring drives sigma54-RNAP interaction and ATP hydrolysis. Genes Dev. 2013;27(22):2500–11. doi: 10.1101/gad.229385.11324240239; PubMed Central PMCID: PMC3841738.
18. Freeman JA, Bassler BL, A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol. 1999;31(2):665–77. 10027982.
19. Lilley BN, Bassler BL, Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol. 2000;36(4):940–54. 10844680.
20. Batchelor JD, Doucleff M, Lee CJ, Matsubara K, De Carlo S, Heideker J, et al. Structure and regulatory mechanism of Aquifex aeolicus NtrC4: variability and evolution in bacterial transcriptional regulation. J Mol Biol. 2008;384(5):1058–75. doi: 10.1016/j.jmb.2008.10.024WOS:000262016600005.
21. De Carlo S, Chen B, Hoover TR, Kondrashkina E, Nogales E, Nixon BT, The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev. 2006;20(11):1485–95. doi: 10.1101/gad.141830616751184; PubMed Central PMCID: PMC1475761.
22. Lee SY, De La Torre A, Yan D, Kustu S, Nixon BT, Wemmer DE, Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev. 2003;17(20):2552–63. doi: 10.1101/gad.112560314561776; PubMed Central PMCID: PMC218149.
23. Doucleff M, Chen B, Maris AE, Wemmer DE, Kondrashkina E, Nixon BT, 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(2):242–55. doi: 10.1016/j.jmb.2005.08.00316169010.
24. Gao R, Mack TR, Stock AM, Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci. 2007;32(5):225–34. doi: 10.1016/j.tibs.2007.03.00217433693; PubMed Central PMCID: PMC3655528.
25. Galperin MY, Diversity of structure and function of response regulator output domains. Curr Opin Microbiol. 2010;13(2):150–9. doi: 10.1016/j.mib.2010.01.00520226724; PubMed Central PMCID: PMC3086695.
26. Stock AM, Robinson VL, Goudreau PN, Two-component signal transduction. Annu Rev Biochem. 2000;69:183–215. 10966457.
27. Bourret RB, Receiver domain structure and function in response regulator proteins. Curr Opin Microbiol. 2010;13(2):142–9. doi: 10.1016/j.mib.2010.01.01520211578; PubMed Central PMCID: PMC2847656.
28. Gao R, Stock AM, Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr Opin Microbiol. 2010;13(2):160–7. Epub 2010/01/19. doi: 10.1016/j.mib.2009.12.00920080056; PubMed Central PMCID: PMC2859964.
29. Hammer BK, Bassler BL, Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A. 2007. 17556542.
30. Chen B, Sysoeva TA, Chowdhury S, Guo L, De Carlo S, Hanson JA, et al. Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA+ ATPase for remodeling bacterial RNA polymerase. Structure. 2010;18(11):1420–30. doi: 10.1016/j.str.2010.08.01821070941; PubMed Central PMCID: PMC3001195.
31. 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(46):34997–5007. doi: 10.1074/jbc.M60662820016973614.
32. Bose D, Pape T, Burrows PC, Rappas M, Wigneshweraraj SR, Buck M, et al. Organization of an activator-bound RNA polymerase holoenzyme. Mol Cell. 2008;32(3):337–46. doi: 10.1016/j.molcel.2008.09.01518995832; PubMed Central PMCID: PMC2680985.
33. Storoni LC, McCoy AJ, Read RJ, Likelihood-enhanced fast rotation functions. Acta Crystallogr D. 2004;60(Pt 3):432–8. 14993666.
34. Emsley P, Cowtan K, Coot: model-building tools for molecular graphics. Acta Crystallogr D. 2004;60(Pt 12 Pt 1):2126–32. 15572765.
35. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002;58(Pt 11):1948–54. Epub 2002/10/24. S0907444902016657 [pii]. 12393927.
36. Laue TM, Shah BD, Ridgeway TM, Pelletier SL, Harding SE, Rowe AJ, Horton JC, Analytical Ultracentrifugation in Biochemistry and Polymer Science. Cambridge: The Royal Society of Chemistry; 1992. p. 90–125.
37. Schuck P, Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J. 2000;78(3):1606–19. doi: 10.1016/S0006-3495(00)76713-010692345; PubMed Central PMCID: PMC1300758.
38. Philo JS, Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques. Anal Biochem. 2006;354(2):238–46. doi: 10.1016/j.ab.2006.04.05316730633.
39. Cantor CR, Schimmel PR, Biophysical chemistry part II: Techniques for the study of biological structure and function. New York: W.H. Freeman and Company; 1980. p. 618–20.