Structural and mechanistic roles of novel chemical ligands on the SdiA quorum-sensing transcription regulator

mBio

Volumn 6, Issue 2, 2015, Pages

  Nguyen, Y ^a   Nguyen, Nam X ^a   Rogers, Jamie L ^a   Liao, Jun ^a   Macmillan, John B ^a   Jiang, Youxing ^a,b   Sperandio, Vanessa ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; N ACYLHOMOSERINE LACTONE; PROTEIN SDIA; UNCLASSIFIED DRUG; DIACYLGLYCEROL; ESCHERICHIA COLI PROTEIN; GAMMA BUTYROLACTONE DERIVATIVE; SDIA PROTEIN, E COLI; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; BIOGENESIS; CARBONYLATION; CONTROLLED STUDY; DIMERIZATION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; HYDROPHOBICITY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; QUORUM SENSING; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; BOVINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BOS; ESCHERICHIA COLI;

ACYL-BUTYROLACTONES; ANIMALS; CATTLE; CRYSTALLOGRAPHY, X-RAY; DIGLYCERIDES; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STABILITY; QUORUM SENSING; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84928816647     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02429-14     Document Type: Article

References (30)

1. Schuster M, Sexton DJ, Diggle SP, Greenberg E. 2013. Acylhomoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 67:43-63. http://dx.doi.org/10.1146/annurev-micro-092412-155635.
2. Fuqua C, Greenberg E. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685-695. http://dx.doi.org/10.1038/nrm907.
3. Nealson KH, Platt T, Hastings J. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313-322.
4. Lee JH, Lequette Y, Greenberg E. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59:602-609. http://dx.doi.org/10.1111/j.1365-2958.2005.04960.x.
5. Hughes DT, Terekhova DA, Liou L, Hovde CJ, Sahl JW, Patankar AV, Gonzalez JE, Edrington TS, Rasko DA, Sperandio V. 2010. Chemical sensing in mammalian host-bacterial commensal associations. Proc Natl Acad Sci U S A 107:9831-9836. http://dx.doi.org/10.1073/pnas.1002551107.
6. Dyszel JL, Soares JA, Swearingen MC, Lindsay A, Smith JN, Ahmer B. 2010. E. coli K-12 and EHEC genes regulated by SdiA. PLoS One 5:e8946. http://dx.doi.org/10.1371/journal.pone.0008946.
7. Ryan GT, Wei Y, Winans S. 2013. A LuxR-type repressor of Burkholderia cenocepacia inhibits transcription via antiactivation and is inactivated by its cognate acylhomoserine lactone. Mol Microbiol 87:94-111. http://dx.doi.org/10.1111/mmi.12085.
8. Vannini A, Volpari C, Gargioli C, Muraglia E, Cortese R, De Francesco R, Neddermann P, Marco S. 2002. The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21:4393-4401. http://dx.doi.org/10.1093/emboj/cdf459.
9. Zhang RG, Pappas KM, Brace JL, Miller PC, Oulmassov T, Molyneaux JM, Anderson JC, Bashkin JK, Winans SC, Joachimiak A. 2002. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971-974. http://dx.doi.org/10.1038/nature00833.
10. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill M. 2011. Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci U S A 108: 15763-15768. http://dx.doi.org/10.1073/pnas.1112398108.
11. Chen G, Swem LR, Swem DL, Stauff DL, O’Loughlin CT, Jeffrey PD, Bassler BL, Hughson F. 2011. A strategy for antagonizing quorum sensing. Mol Cell 42:199-209. http://dx.doi.org/10.1016/j.molcel.2011.04.003.
12. Kim T, Duong T, Wu CA, Choi J, Lan N, Kang SW, Lokanath NK, Shin D, Hwang HY, Kim K. 2014. Structural insights into the molecular mechanism of Escherichia coli SdiA, a quorum-sensing receptor. Acta Crystallogr D Biol Crystallogr 70:694-707. http://dx.doi.org/10.1107/S1399004713032355.
13. Bottomley MJ, Muraglia E, Bazzo R, Carfì A. 2007. Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa from the structure of the virulence regulator LasR bound to its autoinducer. J Biol Chem 282:13592-13600. http://dx.doi.org/10.1074/jbc.M700556200.
14. Yao Y, Martinez-Yamout MA, Dickerson TJ, Brogan AP, Wright PE, Dyson H. 2006. Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J Mol Biol 355:262-273. http://dx.doi.org/10.1016/j.jmb.2005.10.041.
15. Zhu J, Winans S. 1999. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc Natl Acad Sci U S A 96:4832-4837. http://dx.doi.org/10.1073/pnas.96.9.4832.
16. Zhu J, Winans S. 2001. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci U S A 98:1507-1512. http://dx.doi.org/10.1073/pnas.98.4.1507.
17. Michael B, Smith JN, Swift S, Heffron F, Ahmer B. 2001. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183:5733-5742. http://dx.doi.org/10.1128/JB.183.19.5733-5742.2001.
18. Yamamoto K, Yata K, Fujita N, Ishihama A. 2001. Novel mode of transcription regulation by SdiA, an Escherichia coli homologue of the quorum-sensing regulator. Mol Microbiol 41:1187-1198. http://dx.doi.org/10.1046/j.1365-2958.2001.02585.x.
19. Mellies JL, Barron AM, Carmona A. 2007. Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun 75:4199-4210. http://dx.doi.org/10.1128/IAI.01927-06.
20. Sheng H, Lim JY, Knecht HJ, Li J, Hovde C. 2006. Role of Escherichia coli O157:H7 virulence factors in colonization at the bovine terminal rectal mucosa. Infect Immun 74:4685-4693. http://dx.doi.org/10.1128/IAI.00406-06.
21. Brameyer S, Kresovic D, Bode HB, Heermann R. 2015. Dialkylresorcinols as bacterial signaling molecules. Proc Natl Acad SciUSA112:572-577. http://dx.doi.org/10.1073/pnas.1417685112.
22. Brachmann AO, Brameyer S, Kresovic D, Hitkova I, Kopp Y, Manske C, Schubert K, Bode HB, Heermann R. 2013. Pyrones as bacterial signaling molecules. Nat Chem Biol 9:573-578. http://dx.doi.org/10.1038/nchembio.1295.
23. Tsai CS, Winans S. 2011. The quorum-hindered transcription factor YenR of Yersinia enterocolitica inhibits pheromone production and promotes motility via a small non-coding RNA. Mol Microbiol 80:556-571. http://dx.doi.org/10.1111/j.1365-2958.2011.07595.x.
24. Alvarez HM, Steinbüchel A. 2002. Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367-376. http://dx.doi.org/10.1007/s00253-002-1135-0.
25. Liu Q, Siloto RM, Lehner R, Stone SJ, Weselake R. 2012. Acyl-CoA: diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog Lipid Res 51:350-377. http://dx.doi.org/10.1016/j.plipres.2012.06.001.
26. Smith JN, Dyszel JL, Soares JA, Ellermeier CD, Altier C, Lawhon SD, Adams LG, Konjufca V, Curtiss R, III, Slauch JM, Ahmer B. 2008. SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One 3:e2826. http://dx.doi.org/10.1371/journal.pone.0002826.
27. Sambrook JFE, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.
28. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98: 15264-15269. http://dx.doi.org/10.1073/pnas.261348198.
29. Datsenko KA, Wanner B. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
30. Walters M, Sperandio V. 2006. Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 74:5445-5455. http://dx.doi.org/10.1128/IAI.00099-06.