Antimicrobial peptide resistance of Vibrio cholerae results from an LPS modification pathway related to nonribosomal peptide synthetases

ACS Chemical Biology

Volumn 9, Issue 10, 2014, Pages 2382-2392

  Henderson, Jeremy C ^a   Fage, Christopher D ^a   Cannon, Joe R ^b   Brodbelt, Jennifer S ^b   Keatinge Clay, Adrian T ^a   Trent, M Stephen ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b The University of Texas at Austin   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ALME PROTEIN; ALMF PROTEIN; BACTERIAL ENZYME; BACTERIAL PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; CARRIER PROTEIN; GLYCINE; GLYCYLADENYLATE; LIPID A; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; LIPOPOLYSACCHARIDE; PEPTIDE FRAGMENT; PEPTIDE SYNTHASE; POLYMYXIN B;

ANTIBIOTIC RESISTANCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; NONHUMAN; OPERON; VIBRIO CHOLERAE; CHEMISTRY; CHOLERA; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; VIBRIO CHOLERAE O1; X RAY CRYSTALLOGRAPHY;

VIBRIO CHOLERAE;

ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; CHOLERA; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; PEPTIDE FRAGMENTS; PEPTIDE SYNTHASES; POLYMYXIN B; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TANDEM MASS SPECTROMETRY; VIBRIO CHOLERAE O1;

EID: 84908137882     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500438x     Document Type: Article

References (47)

1. Li, J., Nation, R. L., Turnidge, J. D., Milne, R. W., Coulthard, K., Rayner, C. R., and Paterson, D. L. (2006) Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect. Dis. 6, 589-601.
2. Falagas, M. E., Rafailidis, P. I., Ioannidou, E., Alexiou, V. G., Matthaiou, D. K., Karageorgopoulos, D. E., Kapaskelis, A., Nikita, D., and Michalopoulos, A. (2010) Colistin therapy for microbiologically documented multidrug-resistant Gram-negative bacterial infections: a retrospective cohort study of 258 patients. Int. J. Antimicrob. Agents 35, 194-199.
3. Guilhelmelli, F., Vilela, N., Albuquerque, P., Derengowski, L. da S., Silva-Pereira, I., and Kyaw, C. M. (2013) Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Front. Microbiol. 4, 1-12.
4. Falagas, M. E., Rafailidis, P. I., and Matthaiou, D. K. (2010) Resistance to polymyxins: Mechanisms, frequency and treatment options. Drug Resist. Updates 13, 132-138.
5. Roy, H. (2009) Tuning the properties of the bacterial membrane with aminoacylated phosphatidylglycerol. IUBMB Life 61, 940-953.
6. Neuhaus, F. C., and Baddiley, J. (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 686-723.
7. Needham, B. D., and Trent, M. S. (2013) Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11, 467-481.
8. Raetz, C. R. H., Reynolds, C. M., Trent, M. S., and Bishop, R. E. (2007) Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329.
9. Hankins, J. V., Madsen, J. A., Giles, D. K., Brodbelt, J. S., and Trent, M. S. (2012) Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in gram-positive and gram-negative bacteria. Proc. Natl. Acad. Sci. U.S.A. 109, 8722-7.
10. Gangarosa, E. J., Bennett, J. V., and Boring, J. R. (1967) Differentiation between vibrio cholerae and Vibrio cholerae biotype El Tor by the polymyxin B disc test: comparative results with TCBS, Monsur's, Mueller-Hinton and nutrient agar media. Bull. W. H. O. 36, 987.
11. Hankins, J. V., Madsen, J. A., Giles, D. K., Childers, B. M., Klose, K. E., Brodbelt, J. S., and Trent, M. S. (2011) Elucidation of a novel Vibrio cholerae lipid A secondary hydroxy-acyltransferase and its role in innate immune recognition. Mol. Microbiol. 81, 1313-1329.
12. LaRocque, R. C., Harris, J. B., Dziejman, M., Li, X., Khan, A. I., Faruque, A. S. G., Faruque, S. M., Nair, G. B., Ryan, E. T., Qadri, F., Mekalanos, J. J., and Calderwood, S. B. (2005) Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection. Infect. Immun. 73, 4488-4493.
13. Mandlik, A., Livny, J., Robins, W. P., Ritchie, J. M., Mekalanos, J. J., and Waldor, M. K. (2011) RNA-Seq-based monitoring of infectionlinked changes in Vibrio cholerae gene expression. Cell Host Microbe 10, 165-174.
14. Crosby, J., and Crump, M. P. (2012) The structural role of the carrier protein - active controller or passive carrier. Nat. Prod. Rep. 29, 1111.
15. Beld, J., Sonnenschein, E. C., Vickery, C. R., Noel, J. P., and Burkart, M. D. (2014) The phosphopantetheinyl transferases: catalysis of a post-translational modification crucial for life. Nat. Prod. Rep. 31, 61.
16. Fischbach, M. A., and Walsh, C. T. (2009) Antibiotics for emerging pathogens. Science 325, 1089-1093.
17. Masoudi, A., Raetz, C. R. H., Zhou, P., and Pemble, C. W., IV (2013) Chasing acyl carrier protein through a catalytic cycle of lipid A production. Nature 505, 422-426.
18. Agarwal, V., Lin, S., Lukk, T., Nair, S. K., and Cronan, J. E. (2012) Structure of the enzyme-acyl carrier protein (ACP) substrate gatekeeper complex required for biotin synthesis. Proc. Natl. Acad. Sci. U.S.A. 109, 17406-17411.
19. Rock, C. O., Cronan, J. E., and Armitage, I. M. (1981) Molecular properties of acyl carrier protein derivatives. J. Biol. Chem. 256, 2669-2674.
20. Alberts, A. W., and Vagelos, P. R. (1966) Acyl carrier protein VIII. Studies of acyl carrier protein and coenzyme A in Escherichia coli pantothenate or B-alanine auxotrophs. J. Biol. Chem. 241, 5201-5204.
21. Kelly, W. L., Boyne, M. T., Yeh, E., Vosburg, D. A., Galonić, D. P., Kelleher, N. L., and Walsh, C. T. (2007) Characterization of the aminocarboxycyclopropane-forming enzyme CmaC. Biochemistry (Moscow) 46, 359-368.
22. Geladopoulos, T. P., Sotiroudis, T. G., and Evangelopoulos, A. E. (1991) A malachite green colorimetric assay for protein phosphatase activity. Anal. Biochem. 192, 112-116.
23. Osman, K. T., Du, L., He, Y., and Luo, Y. (2009) Crystal structure of Bacillus cereus d-alanyl carrier protein ligase (DltA) in complex with ATP. J. Mol. Biol. 388, 345-355.
24. Trauger, J. W., and Walsh, C. T. (2000) Heterologous expression in Escherichia coli of the first module of the nonribosomal peptide synthetase for chloroeremomycin, a vancomycin-type glycopeptide antibiotic. Proc. Natl. Acad. Sci. U.S.A. 97, 3112-3117.
25. McQuade, T. J., Shallop, A. D., Sheoran, A., DelProposto, J. E., Tsodikov, O. V., and Garneau-Tsodikova, S. (2009) A nonradioactive high-throughput assay for screening and characterization of adenylation domains for nonribosomal peptide combinatorial biosynthesis. Anal. Biochem. 386, 244-250.
26. Conti, E., Stachelhaus, T., Marahiel, M. A., and Brick, P. (1997) Structural basis for the activation of phenylalanine in the nonribosomal biosynthesis of gramicidin S. EMBO J. 16, 4174-4183.
27. Jogl, G., and Tong, L. (2004) Crystal structure of yeast acetylcoenzyme A synthetase in complex with AMP. Biochemistry (Moscow) 43, 1425-1431.
28. Gulick, A. M., Starai, V. J., Horswill, A. R., Homick, K. M., and Escalante-Semerena, J. C. (2003) The 1.75 A˚ crystal structure of acetyl-CoA synthetase bound to adenosine-5′-propylphosphate and coenzyme A. Biochemistry (Moscow) 42, 2866-2873.
29. Conti, E., Franks, N. P., and Brick, P. (1996) Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4, 287-298.
30. Wu, R., Reger, A. S., Lu, X., Gulick, A. M., and Dunaway-Mariano, D. (2009) The mechanism of domain alternation in the acyladenylate forming ligase superfamily member 4-chlorobenzoate: coenzyme A ligase. Biochemistry (Moscow) 48, 4115-4125.
31. Yonus, H., Neumann, P., Zimmermann, S., May, J. J., Marahiel, M. A., and Stubbs, M. T. (2008) Crystal structure of DltA: implications for the reaction mechanism of non-ribosomal peptide synthetase adenylation domains. J. Biol. Chem. 283, 32484-32491.
32. Du, L., He, Y., and Luo, Y. (2008) Crystal structure and enantiomer selection by D-alanyl carrier protein ligase DltA from Bacillus cereus. Biochemistry (Moscow) 47, 11473-11480.
33. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
34. Hughes, A. J., and Keatinge-Clay, A. (2011) Enzymatic extender unit generation for in vitro polyketide synthase reactions: structural and func-tional showcasing of Streptomyces coelicolor MatB. Chem. Biol. 18, 165-176.
35. Sundlov, J. A., Shi, C., Wilson, D. J., Aldrich, C. C., and Gulick, A. M. (2012) Structural and functional investigation of the intermolecular interaction between NRPS adenylation and carrier protein domains. Chem. Biol. 19, 188-198.
36. Reichmann, N. T., Cassona, C. P., and Grundling, A. (2013) Revised mechanism of D-alanine incorporation into cell wall polymers in Gram-positive bacteria. Microbiology 159, 1868-1877.
37. Goudenège, D., Labreuche, Y., Krin, E., Ansquer, D., Mangenot, S., Calteau, A., Médigue, C., Mazel, D., Polz, M. F., and Le Roux, F. (2013) Comparative genomics of pathogenic lineages of Vibrio nigripulchritudo identifies virulence-associated traits. ISME J. 7, 1985-1996.
38. Dzieciatkowska, M., Brochu, D., van Belkum, A., Heikema, A. P., Yuki, N., Houliston, R. S., Richards, J. C., Gilbert, M., and Li, J. (2007) Mass spectrometric analysis of intact lipooligosaccharide: direct evidence for O-acetylated sialic acids and discovery of O-linked glycine expressed by Campylobacter jejuni. Biochemistry (Moscow) 46, 14704-14714.
39. Engskog, M. K. R., Deadman, M., Li, J., Hood, D. W., and Schweda, E. K. H. (2011) Detailed structural features of lipopolysaccharide glycoforms in nontypeable Haemophilus influenzae strain 2019. Carbohydr. Res. 346, 1241-1249.
40. Molinaro, A., Silipo, A., Castro, C. D., Sturiale, L., Nigro, G., Garozzo, D., Bernardini, M. L., Lanzetta, R., and Parrilli, M. (2007) Full structural characterization of Shigella flexneri M90T serotype 5 wild-type R-LPS and its galU mutant: glycine residue location in the inner core of the lipopolysaccharide. Glycobiology 18, 260-269.
41. Scheich, C., Kummel, D., Soumailakakis, D., Heinemann, U., and Bussow, K. (2007) Vectors for co-expression of an unrestricted number of proteins. Nucleic Acids Res. 35, e43-e43.
42. Shaw, J. B., Li, W., Holden, D. D., Zhang, Y., Griep-Raming, J., Fellers, R. T., Early, B. P., Thomas, P. M., Kelleher, N. L., and Brodbelt, J. S. (2013) Complete protein characterization using topdown mass spectrometry and ultraviolet photodissociation. J. Am. Chem. Soc. 135, 12646-12651.
43. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
44. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G. W., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP 4 suite and current developments. Acta Crystallogr., Sect. D 67, 235-242.
45. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179.
46. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D 66, 213-221.
47. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D 60, 2126-2132.