Structural insights into a novel interkingdom signaling circuit by cartography of the ligand-binding sites of the homologous quorum sensing LuxR-family

International Journal of Molecular Sciences

Volumn 14, Issue 10, 2013, Pages 20578-20596

  Covaceuszach, Sonia ^a   Degrassi, Giuliano ^b,c   Venturi, Vittorio ^b   Lamba, Doriano ^a  

^a CNR   (Italy)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c Instituto de Investigación en Biomedicina de Buenos Aires   (Argentina)

Author keywords

Bacterial plant communication; Interkingdom signaling; Ligand binding site; Molecular modeling; Plant Associated Bacteria LuxR solos; Quorum sensing; Structure based multiple alignment

Indexed keywords

N ACYLHOMOSERINE LACTONE; TRANSCRIPTION FACTOR LUXR;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ARTICLE; BINDING SITE; CARTOGRAPHY; COMPARATIVE STUDY; COMPLEX FORMATION; LIGAND BINDING; LIGAND BINDING SITE; PLANT MICROORGANISM INTERACTION; PROTEIN DOMAIN; PROTEIN STRUCTURE; QUORUM SENSING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; LIGANDS; MOLECULAR SEQUENCE DATA; PLANTS; QUORUM SENSING; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 84885923568     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141020578     Document Type: Article

References (52)

1. Fuqua, W.C.; Winans, S.C.; Greenberg, E.P. Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 1994, 176, 269-275.
2. Patankar, A.V.; Gonzalez, J.E. An orphan LuxR homolog of Sinorhizobium meliloti affects stress adaptation and competition for nodulation. Appl. Environ. Microbiol. 2009, 75, 946-955.
3. Subramoni, S.; Venturi, V. LuxR-family "solos": Bachelor sensors/regulators of signalling molecules. Microbiology 2009, 155, 1377-1385.
4. González, J.F.; Venturi, V. A novel widespread interkingdom signalling circuit. Trends Plant Sci. 2013, 18, 167-174.
5. Venturi, V.; Fuqua, W.C. Chemical signaling between plants and plant-pathogenic bacteria. Annu. Rev. Phytopathol. 2013, 51, 17-37.
6. Fuqua, C.; Greenberg, E.P. Listening in on bacteria: Acylhomoserine lactone signalling. Nat. Rev. Mol. Cell. Biol. 2002, 3, 685-695.
7. Slock, J.; VanRiet, D.; Kolibachuk, D.; Greenberg, E.P. Critical regions of the Vibrio fischeri LuxR protein defined by mutational analysis. J. Bacteriol. 1990, 172, 3974-3979.
8. Ferluga, S.; Bigirimana, J.; Hofte, M.; Venturi, V. A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol. Plant. Pathol. 2007, 8, 529-538.
9. Ferluga, S.; Venturi, V. OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas. oryzae pv. oryzae and rice. J. Bacteriol. 2009, 191, 890-897.
10. Zhang, L.; Jia, Y.; Wang, L.; Fang, R. A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas. campestris pv. campestris. Mol. Microbiol. 2007, 65, 121-136.
11. Subramoni, S.; Gonzalez, J.F.; Johnson, A.; Pechy-Tarr, M.; Rochat, L.; Paulsen, I.; Loper, J.E.; Keel, C.; Venturi, V. Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 2011, 77, 4579-4588.
12. Chatnaparat, T.; Prathuangwong, S.; Ionescu, M.; Lindow, S.E. XagR, a LuxR homolog, contributes to the virulence of Xanthomonas. axonopodis pv. glycines to soybean. Mol. Plant Microbe Interact. 2012, 25, 1104-1117.
13. Shadel, G.S.; Young, R.; Baldwin, T.O. Use of regulated cell lysis in a lethal genetic selection in Escherichia coli: Identification of the autoinducer-binding region of the LuxR protein from Vibrio fischeri ATCC 7744. J. Bacteriol. 1990, 172, 3980-3987.
14. Choi, S.H.; Greenberg, E.P. Genetic dissection of DNA binding and luminescence gene activation by the Vibrio fischeri LuxR protein. J. Bacteriol. 1992, 174, 4064-4069.
15. Choi, S.H.; Greenberg, E.P. The C-terminal region of the Vibrio fischeri LuxR protein contains an inducer-independent lux gene activating domain. Proc. Natl. Acad. Sci. USA 1991, 88, 11115-11119.
16. Zhu, J.; Winans, S.C. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc. Natl. Acad. Sci. USA 2001, 98, 1507-1512.
17. Welch, M.; Todd, D.E.; Whitehead, N.A.; McGowan, S.J.; Bycroft, B.W.; Salmond, G.P.C. N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J. 2000, 19, 631-641.
18. Nasser, W.; Reverchon, S. New insights into the regulatory mechanisms of the LuxR family of quorum sensing regulators. Anal. Bioanal. Chem. 2007, 387, 381-390.
19. Whitehead, N.A.; Barnard, A.M.; Slater, H.; Simpson, N.J.; Salmond, G.P. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 2001, 25, 365-404.
20. Fuqua, C.; Winans, S.C.; Greenberg; E.P. Census and consensus in bacterial ecosystems: The LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 1996, 50, 727-751.
21. Soulère, L.; Frezza, M.; Queneau, Y.; Doutheau, A. Exploring the active site of acyl homoserine lactones-dependent transcriptional regulators with bacterial quorum sensing modulators using molecular mechanics and docking studies. J. Mol. Graph. Model. 2007, 26, 581-590.
22. Ahumedo, M.; Díaz, A.; Vivas-Reyes, R. Theoretical and structural analysis of the active site of the transcriptional regulators LasR and TraR, using molecular docking methodology for identifying potential analogues of acyl homoserine lactones (AHLs) with anti-quorum sensing activity. Eur. J. Med. Chem. 2010, 45, 608-615.
23. Zhang, R.G.; Pappas, K.M.; Brace, J.L.; Miller, P.C.; Oulmassov, T.; Molyneaux, J.M.; Anderson, J.C.; Bashkin, J.K.; Winans, S.C.; Joachimiak, A. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 2002, 417, 971-974.
24. Vannini, A.; Volpari, C.; Gargioli, C.; Muraglia, E.; Cortese, R.; De Francesco, R.; Neddermann, P.; Marco, S.D. The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 2002, 21, 4393-4401.
25. Chen, G.; Jeffrey, P.D.; Fuqua, C.; Shi, Y.; Chen, L. Structural basis for antiactivation in bacterial quorum sensing. Proc. Natl. Acad. Sci. USA 2007, 104, 16474-16479.
26. Bottomley, M.J.; Muraglia, E.; Bazzo, R.; Carfì, A. 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. 2007, 282, 13592-13600.
27. Zou, Y.; Nair, S.K. Molecular basis for the recognition of structurally distinct autoinducer mimics by the Pseudomonas aeruginosa LasR quorum-sensing signaling receptor. Chem. Biol. 2009, 16, 961-970.
28. Lintz, M.J.; Oinuma, K.; Wysoczynski, C.L.; Greenberg, E.P.; Churchill, M.E. Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc. Natl. Acad. Sci. USA 2011, 108, 15763-15768.
29. Chen, G.; Swem, L.R.; Swem, D.L.; Stauff, D.L.; O'Loughlin, C.T.; Jeffrey, P.D.; Bassler, B.L.; Hughson, F.M. A strategy for antagonizing quorum sensing. Mol. Cell. 2011, 42, 199-209.
30. Yao, Y.; Martinez-Yamout, M.A.; Dickerson, T.J.; Brogan, A.P.; Wright, P.E.; Dyson, H.J. Structure of the Escherichia coli quorum sensing protein SdiA: Activation of the folding switch by acyl homoserine lactones. J. Mol. Biol. 2006, 355, 262-273.
31. Armougom, F.; Moretti, S.; Poirot, O.; Audic, S.; Dumas, P.; Schaeli, B.; Keduas, V.; Notredame, C. Expresso: Automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 2006, 34, W604-W608.
32. Berman, H.M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T.N.; Weissig, H.; Shindyalov, I.N.; Bourne, P.E. The Protein Data Bank. Nucleic Acids Res. 2000, 28, 235-242.
33. The PyMOL Molecular Graphics System, Version 1.5.0.4, Schrödinger, LLC: Palo Alto, CA, USA, 2002.
34. Krissinel, E.; Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372, 774-797.
35. Patankar, A.V.; González, J.E. Orphan LuxR regulators of quorum sensing. FEMS Microbiol. Rev. 2009, 33, 739-756.
36. Zhang, Y. I-TASSER server for protein 3D structure prediction. BMC Bioinforma. 2008, 9, 40-47.
37. Hernandez, M.; Ghersi, D.; Sanchez, R. SITEHOUND-web: A server for ligand binding site identification in protein structures. Nucleic Acids Res. 2009, 37, W413-W416.
38. Taylor, W.R. Protein structure comparison using SAP. Methods Mol. Biol. 2000, 143, 19-32.
39. Zhang, Y.; Skolnick, J. TM-align: A protein structure alignment algorithm based on TM-score. Nucleic Acids Res. 2005, 33, 2302-2309.
40. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 2006, 22, 195-201.
41. Huang, X.; Miller W. A time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 1991, 12, 337-357.
42. Eswar, N.; John, B.; Mirkovic, N.; Fiser, A.; Ilyin, V.A.; Pieper, U.; Stuart, A.C.; Marti-Renom, M.A.; Madhusudhan, M.S.; Yerkovich, B.; et al. Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 2003, 31, 3375-3380.
43. Martí-Renom, M.A.; Stuart, A.C.; Fiser, A.; Sánchez, R.; Melo, F.; Sali, A. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325.
44. Pieper, U.; Eswar, N.; Stuart, A.C.; Ilyin, V. A; Sali, A. MODBASE, a database of annotated comparative protein structure models. Nucleic Acids Res. 2002, 30, 255-259.
45. Sanchez, R.; Sali, A. Large-scale protein structure modeling of the Saccharomyces cerevisiae genome. Proc. Natl. Acad. Sci. USA 1998, 95, 13597-13602.
46. Fernandez-Fuentes, N.; Madrid-Aliste, C.J.; Rai, B.K.; Fajardo, J.E.; Fiser, A. M4T: A comparative protein structure modeling server. Nucleic Acids Res. 2007, 35, 363-368.
47. Rai, B. K; Fiser, A. Multiple mapping method: A novel approach to the sequence-to-structure alignment problem in comparative protein structure modeling. Proteins 2006, 63, 644-661.
48. Biegert, A.; Mayer, C.; Remmert, M.; Soding, J.; Lupas, A.N. The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res. 2006, 34, W335-W339.
49. Wallner, B.; Elofsson, A. Can correct protein models be identified? Protein Sci. 2003, 12, 1073-1086.
50. Mereghetti, P.; Ganadu, M.L.; Papaleo, E.; Fantucci, P.; De Gioia, L. Validation of protein models by a neural network approach. BMC Bioinforma. 2008, 9, 66-76.
51. Dolinsky, T.J.; Nielsen, J.E.; McCammon, J.A.; Baker, N.A. PDB2PQR: An automated pipeline for the setup, execution, and analysis of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 2004, 32, W665-W667.
52. Black, S.D.; Mould, D.R. Amino acid scale: Hydrophobicity of physiological L-alpha amino acids. Anal. Biochem. 1991, 193, 72-82.