Identification of inhibitors of PvdQ, an enzyme involved in the synthesis of the siderophore pyoverdine

ACS Chemical Biology

Volumn 9, Issue 7, 2014, Pages 1536-1544

  Wurst, Jacqueline M ^a   Drake, Eric J ^b,c   Theriault, Jimmy R ^a   Jewett, Ivan T ^a   Verplank, Lynn ^a   Perez, Jose R ^a   Dandapani, Sivaraman ^a   Palmer, Michelle ^a   Moskowitz, Samuel M ^d,e   Schreiber, Stuart L ^a   Munoz, Benito ^a   Gulick, Andrew M ^b,c  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b Hauptman Woodward Medical Institute   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; HYDROLASE INHIBITOR; ML 318; NITRILE; PYOVERDINE; SIDEROPHORE; UNCLASSIFIED DRUG; AMIDASE; ANTIINFECTIVE AGENT; ENZYME INHIBITOR; OLIGOPEPTIDE;

ARTICLE; BACTERIAL GROWTH; CRYSTAL STRUCTURE; ENZYME INHIBITION; FEMALE; HELA CELL LINE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HYDROGEN BOND; IC 50; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; PSEUDOMONAS INFECTIONS; X RAY CRYSTALLOGRAPHY;

AMIDOHYDROLASES; ANTI-BACTERIAL AGENTS; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; HUMANS; MODELS, MOLECULAR; OLIGOPEPTIDES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

EID: 84904541042     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb5001586     Document Type: Article

References (39)

1. Kanj, S. S. and Kanafani, Z. A. (2011) Current concepts in antimicrobial therapy against resistant gram-negative organisms: Extended-spectrum β-lactamase-producing Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae, and multidrug-resistant Pseudomonas aeruginosa Mayo Clinic Proceedings 86, 250-259
2. Peterson, L. R. (2009) Bad bugs, no drugs: No ESCAPE revisited Clin. Infect. Dis. 49, 992-993
3. Mekalanos, J. J. (1992) Environmental signals controlling expression of virulence determinants in bacteria J. Bacteriol. 174, 1-7
4. Sandy, M. and Butler, A. (2009) Microbial iron acquisition: Marine and terrestrial siderophores Chem. Rev. 109, 4580-4595
5. Miethke, M. and Marahiel, M. A. (2007) Siderophore-based iron acquisition and pathogen control Microbiol Mol. Biol. Rev. 71, 413-451 (Pubitemid 47429279)
6. Ferreras, J. A., Ryu, J. S., Di Lello, F., Tan, D. S., and Quadri, L. E. (2005) Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis Nat. Chem. Biol. 1, 29-32
7. Miethke, M., Bisseret, P., Beckering, C. L., Vignard, D., Eustache, J., and Marahiel, M. A. (2006) Inhibition of aryl acid adenylation domains involved in bacterial siderophore synthesis FEBS J. 273, 409-419
8. Qiao, C., Gupte, A., Boshoff, H. I., Wilson, D. J., Bennett, E. M., Somu, R. V., Barry, C. E., 3rd, and Aldrich, C. C. (2007) 5′-O-[(N-Acyl) sulfamoyl]adenosines as antitubercular agents that inhibit MbtA: An adenylation enzyme required for siderophore biosynthesis of the mycobactins J. Med. Chem. 50, 6080-6094
9. Lun, S., Guo, H., Adamson, J., Cisar, J. S., Davis, T. D., Chavadi, S. S., Warren, J. D., Quadri, L. E., Tan, D. S., and Bishai, W. R. (2013) Pharmacokinetic and in vivo efficacy studies of the mycobactin biosynthesis inhibitor salicyl-AMS in mice Antimicrob. Agents Chemother. 57, 5138-5140
10. Ochsner, U. A., Wilderman, P. J., Vasil, A. I., and Vasil, M. L. (2002) GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: Identification of novel pyoverdine biosynthesis genes Mol. Microbiol. 45, 1277-1287 (Pubitemid 35015352)
11. Visca, P., Imperi, F., and Lamont, I. L. (2007) Pyoverdine siderophores: From biogenesis to biosignificance Trends Microbiol. 15, 22-30 (Pubitemid 46038729)
12. Lamont, I. L., Beare, P. A., Ochsner, U., Vasil, A. I., and Vasil, M. L. (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U. S. A. 99, 7072-7077 (Pubitemid 34526257)
13. Meyer, J. M., Neely, A., Stintzi, A., Georges, C., and Holder, I. A. (1996) Pyoverdin is essential for virulence of Pseudomonas aeruginosa Infect. Immun. 64, 518-523 (Pubitemid 26032823)
14. Nadal Jimenez, P., Koch, G., Papaioannou, E., Wahjudi, M., Krzeslak, J., Coenye, T., Cool, R. H., and Quax, W. J. (2009) Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions Microbiology 156, 49-59
15. Banin, E., Vasil, M. L., and Greenberg, E. P. (2005) Iron and Pseudomonas aeruginosa biofilm formation Proc. Natl. Acad. Sci. U.S.A. 102, 11076-11081 (Pubitemid 41105995)
16. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial biofilms: A common cause of persistent infections Science 284, 1318-1322 (Pubitemid 29289651)
17. Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A., Davies, D. G., and Gilbert, P. (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm J. Bacteriol. 186, 7312-7326 (Pubitemid 39383116)
18. Lehoux, D. E., Sanschagrin, F., and Levesque, R. C. (2000) Genomics of the 35-kb pvd locus and analysis of novel pvdIJK genes implicated in pyoverdine biosynthesis in Pseudomonas aeruginosa FEMS Microbiol. Lett. 190, 141-146 (Pubitemid 30645849)
19. Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T., and Ichinose, Y. (2010) The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection J. Bacteriol. 192, 117-126
20. Papaioannou, E., Wahjudi, M., Nadal-Jimenez, P., Koch, G., Setroikromo, R., and Quax, W. J. (2009) Quorum-quenching acylase reduces the virulence of Pseudomonas aeruginosa in a Caenorhabditis elegans infection model Antimicrob. Agents Chemother. 53, 4891-4897
21. Schalk, I. J. and Guillon, L. (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis Environ. Microbiol. 15, 1661-1673
22. Challis, G. L. and Naismith, J. H. (2004) Structural aspects of non-ribosomal peptide biosynthesis Curr. Opin Struct Biol. 14, 748-756 (Pubitemid 39592586)
23. Mossialos, D., Ochsner, U., Baysse, C., Chablain, P., Pirnay, J. P., Koedam, N., Budzikiewicz, H., Fernandez, D. U., Schafer, M., Ravel, J., and Cornelis, P. (2002) Identification of new, conserved, non-ribosomal peptide synthetases from fluorescent pseudomonads involved in the biosynthesis of the siderophore pyoverdine Mol. Microbiol. 45, 1673-1685 (Pubitemid 35231982)
24. Drake, E. J. and Gulick, A. M. (2011) Structural characterization and high-throughput screening of inhibitors of PvdQ, an NTN hydrolase involved in pyoverdine synthesis ACS Chem. Biol. 6, 1277-1286
25. Hannauer, M., Schafer, M., Hoegy, F., Gizzi, P., Wehrung, P., Mislin, G. L., Budzikiewicz, H., and Schalk, I. J. (2012) Biosynthesis of the pyoverdine siderophore of Pseudomonas aeruginosa involves precursors with a myristic or a myristoleic acid chain FEBS Lett. 586, 96-101
26. Artymiuk, P. J. (1995) A sting in the (N-terminal) tail Nat. Struct. Biol. 2, 1035-1037
27. Bokhove, M., Jimenez, P. N., Quax, W. J., and Dijkstra, B. W. (2010) The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket Proc. Natl. Acad. Sci. U.S.A. 107, 686-691
28. Sio, C. F., Otten, L. G., Cool, R. H., Diggle, S. P., Braun, P. G., Bos, R., Daykin, M., Camara, M., Williams, P., and Quax, W. J. (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1 Infect. Immun. 74, 1673-1682 (Pubitemid 43346800)
29. Theriault, J. R., Wurst, J., Jewett, I., Verplank, L., Perez, J. R., Gulick, A. M., Drake, E. J., Palmer, M., Moskowitz, S., Dasgupta, N., Brannon, M. K., Dandapani, S., Munoz, B., and Schreiber, S. (2013) Identification of a small molecule inhibitor of Pseudomonas aeruginosa PvdQ acylase, an enzyme involved in siderophore pyoverdine synthesis., In Probe Reports from the NIH Molecular Libraries Program [Internet]; National Center for Biotchnology Information (U.S.), Bethesda, MD.
30. Meyer, J. M., Halle, F., Hohnadel, D., Lemanceau, P., and Ratefiarivelo, H. (1987) Siderophores of Pseudomonas -biological properties, In Iron Transport in Microbes, Plants, and Animals (Winkelmann, G., Van der Helm, D., and Neilands, J. B., Eds.), pp 189-205, VCH, Weinheim Germany.
31. Sommer, M. B., Begtrup, M., and Bogeso, K. P. (1990) Displacement of halogen of 2-halogeno-substituted benzonitriles with carbanion. Preparation of (2-cyanoaryl)arylacetonitriles J. Org. Chem. 55, 4817-4821
32. Hino, K., Nagai, Y., and Uno, H. (1988) Agents acting on the central nervous system. Synthesis of 3-phenyl-2-piperazinyl-1-benzazocines, 3-substituted-2-piperazinyl-1-benzazepines, and related compounds Chem. Pharmaceut. Bull. 36, 2386-2400
33. Gutmann, B., Roduit, J. P., Roberge, D., and Kappe, C. O. (2010) Synthesis of 5-substituted 1H-tetrazoles from nitriles and hydrazoic acid by using a safe and scalable high-temperature microreactor approach Angew. Chem., Int. Ed. Engl. 49, 7101-7105
34. Tran, V. H., Kantharaj, R., Roufogalis, B. D., and Duke, C. C. (2006) An efficient and facile synthesis of capsaicin-like compounds as agonists of the TRPV1 receptor Eur. J. Org. Chem. 2006, 2970-2976
35. Clatworthy, A. E., Pierson, E., and Hung, D. T. (2007) Targeting virulence: A new paradigm for antimicrobial therapy Nat. Chem. Biol. 3, 541-548 (Pubitemid 47294400)
36. Lomovskaya, O., Warren, M. S., Lee, A., Galazzo, J., Fronko, R., Lee, M., Blais, J., Cho, D., Chamberland, S., Renau, T., Leger, R., Hecker, S., Watkins, W., Hoshino, K., Ishida, H., and Lee, V. J. (2001) Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: Novel agents for combination therapy Antimicrob. Agents Chemother. 45, 105-116 (Pubitemid 32039101)
37. Pages, J. M. and Amaral, L. (2009) Mechanisms of drug efflux and strategies to combat them: Challenging the efflux pump of Gram-negative bacteria Biochim. Biophys. Acta 1794, 826-833
38. Imperi, F., Massai, F., Facchini, M., Frangipani, E., Visaggio, D., Leoni, L., Bragonzi, A., and Visca, P. (2013) Repurposing the antimycotic drug flucytosine for suppression of Pseudomonas aeruginosa pathogenicity Proc. Natl. Acad. Sci. U.S.A. 110, 7458-7463
39. Clevenger, K. D., Wu, R., Er, J. A., Liu, D., and Fast, W. (2013) Rational design of a transition state analogue with picomolar affinity for Pseudomonas aeruginosa PvdQ, a siderophore biosynthetic enzyme ACS Chem. Biol. 8, 2192-2200