Experimental Evolution of Diverse Strains as a Method for the Determination of Biochemical Mechanisms of Action for Novel Pyrrolizidinone Antibiotics

ACS Infectious Diseases

Volumn 3, Issue 11, 2017, Pages 854-865

  Beabout, Kathryn ^a   McCurry, Megan D ^a   Mehta, Heer ^a   Shah, Akshay A ^a   Pulukuri, Kiran Kumar ^a   Rigol, Stephan ^a   Wang, Yanping ^a   Nicolaou, K C ^a   Shamoo, Yousif ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

antibiotic resistance; antibiotics; experimental evolution; mechanism of action; pyrrolizidinone

Indexed keywords

ANTIBIOTIC AGENT; PYRROLIZIDINONE ANTIBIOTIC; UNCLASSIFIED DRUG; 2 PYRROLIDONE DERIVATIVE; AMINOTRANSFERASE; ANTIINFECTIVE AGENT; BCAT1 PROTEIN, MOUSE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; BIOCHEMISTRY; CONTROLLED STUDY; DRUG MECHANISM; ENTEROCOCCUS FAECALIS; GENOME; HUMAN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; WHOLE GENOME SEQUENCING; BACTERIAL GENOME; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; EVOLUTION; GENETIC VARIATION; GENETICS; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; OXYGEN CONSUMPTION; STRUCTURE ACTIVITY RELATION;

ANTI-BACTERIAL AGENTS; BIOLOGICAL EVOLUTION; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; OXYGEN CONSUMPTION; PYRROLIDINONES; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSAMINASES;

EID: 85033569529     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.7b00135     Document Type: Article

References (61)

1. Blair, J. M. A., Webber, M. A., Baylay, A. J., Ogbolu, D. O., and Piddock, L. J. V. (2015) Molecular mechanisms of antibiotic resistance Nat. Rev. Microbiol. 13 (1) 42-51 10.1038/nrmicro3380
2. CDC. ((2013) Antibiotic resistance threats in the United States, 2013, CDC, Atlanta, GA.
3. The PEW Charitable Trusts. ((2016) Antibiotics Currently in Clinical Development, http://www.pewtrusts.org/~/media/assets/2016/05/antibiotics-currently-in-clinical-development.pdf.
4. Rine, J., Hansen, W., Hardeman, E., and Davis, R. W. (1983) Targeted selection of recombinant clones through gene dosage effects Proc. Natl. Acad. Sci. U. S. A. 80 (22) 6750-6754 10.1073/pnas.80.22.6750
5. Banerjee, A., Dubnau, E., Quemard, A., Balasubramanian, V., Um, K. S., Wilson, T., Collins, D., de Lisle, G., and Jacobs, W. R. (1994) inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis Science 263 (5144) 227-230 10.1126/science.8284673
6. Belanger, A. E., Besra, G. S., Ford, M. E., Mikusová, K., Belisle, J. T., Brennan, P. J., and Inamine, J. M. (1996) The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol Proc. Natl. Acad. Sci. U. S. A. 93 (21) 11919-11924 10.1073/pnas.93.21.11919
7. Sugden, C. J., Roper, J. R., and Williams, J. G. (2005) Engineered gene over-expression as a method of drug target identification Biochem. Biophys. Res. Commun. 334 (2) 555-560 10.1016/j.bbrc.2005.06.117
8. Shi, W., Zhang, X., Jiang, X., Yuan, H., Lee, J. S., Barry, C. E., Wang, H., Zhang, W., and Zhang, Y. (2011) Pyrazinamide Inhibits Trans-Translation in Mycobacterium tuberculosis Science 333 (6049) 1630-1632 10.1126/science.1208813
9. Payne, D. J., Gwynn, M. N., Holmes, D. J., and Rosenberg, M. (2004) Genomic Approaches to Antibacterial Discovery, in Genomics, Proteomics, and Clinical Bacteriology: Methods and Reviews (Woodford, N. and Johnson, A. P., Eds.) pp 231-259, Humana Press, Totowa, NJ, DOI: 10.1385/1-59259-763-7:231.
10. Luesch, H., Wu, T. Y. H., Ren, P., Gray, N. S., Schultz, P. G., and Supek, F. (2005) A Genome-Wide Overexpression Screen in Yeast for Small-Molecule Target Identification Chem. Biol. 12 (1) 55-63 10.1016/j.chembiol.2004.10.015
11. Butcher, R. A., Bhullar, B. S., Perlstein, E. O., Marsischky, G., LaBaer, J., and Schreiber, S. L. (2006) Microarray-based method for monitoring yeast overexpression strains reveals small-molecule targets in TOR pathway Nat. Chem. Biol. 2 (2) 103-109 10.1038/nchembio762
12. Palmer, A. C. and Kishony, R. (2014) Opposing effects of target overexpression reveal drug mechanisms Nat. Commun. 5, 4296 10.1038/ncomms5296
13. Bandow, J. E., Brötz, H., Leichert, L. I. O., Labischinski, H., and Hecker, M. (2003) Proteomic Approach to Understanding Antibiotic Action Antimicrob. Agents Chemother. 47 (3) 948-955 10.1128/AAC.47.3.948-955.2003
14. Brazas, M. D. and Hancock, R. E. W. (2005) Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance Drug Discovery Today 10 (18) 1245-1252 10.1016/S1359-6446(05)03566-X
15. Le, C.-F., Gudimella, R., Razali, R., Manikam, R., and Sekaran, S. D. (2016) Transcriptome analysis of Streptococcus pneumoniae treated with the designed antimicrobial peptides, DM3 Sci. Rep. 6, 26828 10.1038/srep26828
16. Miesel, L., Greene, J., and Black, T. A. (2003) Genetic strategies for antibacterial drug discovery Nat. Rev. Genet. 4 (6) 442-456 10.1038/nrg1086
17. Belanger, A. E., Lai, A., Brackman, M. A., and LeBlanc, D. J. (2002) PCR-Based Ordered Genomic Libraries: a New Approach to Drug Target Identification for Streptococcus pneumoniae Antimicrob. Agents Chemother. 46 (8) 2507-2512 10.1128/AAC.46.8.2507-2512.2002
18. Beabout, K., Hammerstrom, T. G., Perez, A. M., Magalhães, B., de, F., Prater, A. G., Clements, T. P., Arias, C. A., Saxer, G., and Shamoo, Y. (2015) The ribosomal S10 protein is a general target for decreased tigecycline susceptibility Antimicrob. Agents Chemother. 59, 5561 10.1128/AAC.00547-15
19. Beabout, K., Hammerstrom, T. G., Wang, T. T., Bhatty, M., Christie, P. J., Saxer, G., and Shamoo, Y. (2015) Rampant Parasexuality Evolves in a Hospital Pathogen during Antibiotic Selection Mol. Biol. Evol. 32 (10) 2585-2597 10.1093/molbev/msv133
20. Hammerstrom, T. G., Beabout, K., Clements, T. P., Saxer, G., and Shamoo, Y. (2015) Acinetobacter baumannii Repeatedly Evolves a Hypermutator Phenotype in Response to Tigecycline That Effectively Surveys Evolutionary Trajectories to Resistance PLoS One 10 (10) e0140489 10.1371/journal.pone.0140489
21. Miller, C., Kong, J., Tran, T. T., Arias, C. A., Saxer, G., and Shamoo, Y. (2013) Adaptation of Enterococcus faecalis to Daptomycin Reveals an Ordered Progression to Resistance Antimicrob. Agents Chemother. 57, 5373 10.1128/AAC.01473-13
22. Sugie, Y., Hirai, H., Kachi-Tonai, H., Kim, Y. J., Kojima, Y., Shiomi, Y., Sugiura, A., Sugiura, A., Suzuki, Y., and Yoshikawa, N. et al. 2001, New pyrrolizidinone antibiotics CJ-16,264 and CJ-16,367 J. Antibiot. 54 (11) 917-925 10.7164/antibiotics.54.917
23. Nicolaou, K. C., Shah, A. A., Korman, H., Khan, T., Shi, L., Worawalai, W., and Theodorakis, E. A. (2015) Total Synthesis and Structural Revision of Antibiotic CJ-16,264 Angew. Chem., Int. Ed. 54 (32) 9203-9208 10.1002/anie.201504337
24. Tanaka, M. M., Bergstrom, C. T., and Levin, B. R. (2003) The evolution of mutator genes in bacterial populations: the roles of environmental change and timing Genetics 164 (3) 843-854
25. Even, S., Burguière, P., Auger, S., Soutourina, O., Danchin, A., and Martin-Verstraete, I. (2006) Global Control of Cysteine Metabolism by CymR in Bacillus subtilis J. Bacteriol. 188 (6) 2184-2197 10.1128/JB.188.6.2184-2197.2006
26. Albanesi, D., Mansilla, M. C., Schujman, G. E., and de Mendoza, D. (2005) Bacillus subtilis Cysteine Synthetase Is a Global Regulator of the Expression of Genes Involved in Sulfur Assimilation J. Bacteriol. 187 (22) 7631-7638 10.1128/JB.187.22.7631-7638.2005
27. Tanous, C., Soutourina, O., Raynal, B., Hullo, M.-F., Mervelet, P., Gilles, A.-M., Noirot, P., Danchin, A., England, P., and Martin-Verstraete, I. (2008) The CymR Regulator in Complex with the Enzyme CysK Controls Cysteine Metabolism in Bacillus subtilis J. Biol. Chem. 283 (51) 35551-35560 10.1074/jbc.M805951200
28. Brooijmans, R., Smit, B., Santos, F., van Riel, J., de Vos, W. M., and Hugenholtz, J. (2009) Heme and menaquinone induced electron transport in lactic acid bacteria Microb. Cell Fact. 8 (1) 28 10.1186/1475-2859-8-28
29. Winstedt, L., Frankenberg, L., Hederstedt, L., and von Wachenfeldt, C. (2000) Enterococcus faecalis V583 Contains a Cytochrome bd-Type Respiratory Oxidase J. Bacteriol. 182 (13) 3863-3866 10.1128/JB.182.13.3863-3866.2000
30. Vik, S. B., Lee, D., and Marshall, P. A. (1991) Temperature-sensitive mutations at the carboxy terminus of the alpha subunit of the Escherichia coli F1F0 ATP synthase J. Bacteriol. 173 (14) 4544-4548 10.1128/jb.173.14.4544-4548.1991
31. Beinert, H., Holm, R. H., and Münck, E. (1997) Iron-Sulfur Clusters: Nature's Modular, Multipurpose Structures Science 277 (5326) 653-659 10.1126/science.277.5326.653
32. Bandyopadhyay, S., Chandramouli, K., and Johnson, M. K. (2008) Iron-Sulphur Cluster Biosynthesis Biochem. Soc. Trans. 36 (6) 1112-1119 10.1042/BST0361112
33. Udekwu, K. I., Parrish, N., Ankomah, P., Baquero, F., and Levin, B. R. (2009) Functional relationship between bacterial cell density and the efficacy of antibiotics J. Antimicrob. Chemother. 63 (4) 745-757 10.1093/jac/dkn554
34. Brook, I. (1989) Inoculum Effect Clin. Infect. Dis. 11 (3) 361-368 10.1093/clinids/11.3.361
35. Borisov, V. B., Gennis, R. B., Hemp, J., and Verkhovsky, M. I. (2011) The cytochrome bd respiratory oxygen reductases Biochim. Biophys. Acta, Bioenerg. 1807 (11) 1398-1413 10.1016/j.bbabio.2011.06.016
36. Eakins, J., Bauch, C., Woodhouse, H., Park, B., Bevan, S., Dilworth, C., and Walker, P. (2016) A combined in vitro approach to improve the prediction of mitochondrial toxicants Toxicol. In Vitro 34, 161-170 10.1016/j.tiv.2016.03.016
37. Erickson, S. K. (1971) The respiratory system of the aerobic, nitrogen-fixing, Gram-positive bacterium, Mycobacterium flavum 301 Biochim. Biophys. Acta, Bioenerg. 245 (1) 63-69 10.1016/0005-2728(71)90008-9
38. Netrusov, A. and Pestova, E. (1991) Oxidative phosphorylation in membrane vesicles of a gram-positive methylotroph Arch. Microbiol. 156 (2) 115-118 10.1007/BF00290983
39. Garbisu, C., Alkorta, I., Llama, M. J., and Serra, J. L. (1998) Aerobic chromate reduction by Bacillus subtilis Biodegradation 9 (2) 133-141 10.1023/A:1008358816529
40. Frerman, F. E. and White, D. C. (1967) Membrane Lipid Changes During Formation of a Functional Electron Transport System in Staphylococcus aureus J. Bacteriol. 94 (6) 1868-1874
41. Cattoir, V., Isnard, C., Cosquer, T., Odhiambo, A., Bucquet, F., Guérin, F., and Giard, J.-C. (2015) Genomic Analysis of Reduced Susceptibility to Tigecycline in Enterococcus faecium Antimicrob. Agents Chemother. 59 (1) 239-244 10.1128/AAC.04174-14
42. Villa, L., Feudi, C., Fortini, D., García-Fernández, A., and Carattoli, A. (2014) Genomics of KPC-Producing Klebsiella pneumoniae Sequence Type 512 Clone Highlights the Role of RamR and Ribosomal S10 Protein Mutations in Conferring Tigecycline Resistance Antimicrob. Agents Chemother. 58 (3) 1707-1712 10.1128/AAC.01803-13
43. Fiedler, S., Bender, J. K., Klare, I., Halbedel, S., Grohmann, E., Szewzyk, U., and Werner, G. (2016) Tigecycline resistance in clinical isolates of Enterococcus faecium is mediated by an upregulation of plasmid-encoded tetracycline determinants tet(L) and tet(M) J. Antimicrob. Chemother. 71 (4) 871-881 10.1093/jac/dkv420
44. 2+ cleavage of 16S rRNA J. Antimicrob. Chemother. 53 (4) 592-599 10.1093/jac/dkh125
45. Jenner, L., Starosta, A. L., Terry, D. S., Mikolajka, A., Filonava, L., Yusupov, M., Blanchard, S. C., Wilson, D. N., and Yusupova, G. (2013) Structural basis for potent inhibitory activity of the antibiotic tigecycline during protein synthesis Proc. Natl. Acad. Sci. U. S. A. 110 (10) 3812-3816 10.1073/pnas.1216691110
46. Olson, M. W., Ruzin, A., Feyfant, E., Rush, T. S., O'Connell, J., and Bradford, P. A. (2006) Functional, Biophysical, and Structural Bases for Antibacterial Activity of Tigecycline Antimicrob. Agents Chemother. 50 (6) 2156-2166 10.1128/AAC.01499-05
47. Connell, S. R., Tracz, D. M., Nierhaus, K. H., and Taylor, D. E. (2003) Ribosomal Protection Proteins and Their Mechanism of Tetracycline Resistance Antimicrob. Agents Chemother. 47 (12) 3675-3681 10.1128/AAC.47.12.3675-3681.2003
48. Keeney, D., Ruzin, A., McAleese, F., Murphy, E., and Bradford, P. A. (2007) MarA-mediated overexpression of the AcrAB efflux pump results in decreased susceptibility to tigecycline in Escherichia coli J. Antimicrob. Chemother. 61 (1) 46-53 10.1093/jac/dkm397
49. McAleese, F., Petersen, P., Ruzin, A., Dunman, P. M., Murphy, E., Projan, S. J., and Bradford, P. A. (2005) A Novel MATE Family Efflux Pump Contributes to the Reduced Susceptibility of Laboratory-Derived Staphylococcus aureus Mutants to Tigecycline Antimicrob. Agents Chemother. 49 (5) 1865-1871 10.1128/AAC.49.5.1865-1871.2005
50. Miller, W. R., Bayer, A. S., and Arias, C. A. (2016) Mechanism of Action and Resistance to Daptomycin in Staphylococcus aureus and Enterococci Cold Spring Harbor Perspect. Med. 6, a026997 10.1101/cshperspect.a026997
51. Arias, C. A., Panesso, D., McGrath, D. M., Qin, X., Mojica, M. F., Miller, C., Diaz, L., Tran, T. T., Rincon, S., and Barbu, E. M. et al. 2011, Genetic Basis for In Vivo Daptomycin Resistance in Enterococci N. Engl. J. Med. 365 (10) 892-900 10.1056/NEJMoa1011138
52. Hachmann, A.-B., Angert, E. R., and Helmann, J. D. (2009) Genetic Analysis of Factors Affecting Susceptibility of Bacillus subtilis to Daptomycin Antimicrob. Agents Chemother. 53 (4) 1598-1609 10.1128/AAC.01329-08
53. Hachmann, A.-B., Sevim, E., Gaballa, A., Popham, D. L., Antelmann, H., and Helmann, J. D. (2011) Reduction in Membrane Phosphatidylglycerol Content Leads to Daptomycin Resistance in Bacillus subtilis Antimicrob. Agents Chemother. 55 (9) 4326-4337 10.1128/AAC.01819-10
54. Davlieva, M., Zhang, W., Arias, C. A., and Shamoo, Y. (2013) Biochemical Characterization of Cardiolipin Synthase Mutations Associated with Daptomycin Resistance in Enterococci Antimicrob. Agents Chemother. 57 (1) 289-296 10.1128/AAC.01743-12
55. Friedman, L., Alder, J. D., and Silverman, J. A. (2006) Genetic Changes That Correlate with Reduced Susceptibility to Daptomycin in Staphylococcus aureus Antimicrob. Agents Chemother. 50 (6) 2137-2145 10.1128/AAC.00039-06
56. Schäberle, T. F. and Hack, I. M. (2014) Overcoming the current deadlock in antibiotic research Trends Microbiol. 22 (4) 165-167 10.1016/j.tim.2013.12.007
57. Silver, L. L. (2011) Challenges of Antibacterial Discovery Clin. Microbiol. Rev. 24 (1) 71-109 10.1128/CMR.00030-10
58. Nicolaou, K. C., Hale, C. R. H., Nilewski, C., Ioannidou, H. A., ElMarrouni, A., Nilewski, L. G., Beabout, K., Wang, T. T., and Shamoo, Y. (2014) Total Synthesis of Viridicatumtoxin B and Analogues Thereof: Strategy Evolution, Structural Revision, and Biological Evaluation J. Am. Chem. Soc. 136 (34) 12137-12160 10.1021/ja506472u
59. Deatherage, D. E. and Barrick, J. E. (2014) Identification of mutations in laboratory evolved microbes from next-generation sequencing data using breseq Methods Mol. Biol. 1151, 165-188 10.1007/978-1-4939-0554-6-12
60. Diaz, L., Tran, T. T., Munita, J. M., Miller, W. R., Rincon, S., Carvajal, L. P., Wollam, A., Reyes, J., Panesso, D., and Rojas, N. L. et al. 2014, Whole-genome analyses of Enterococcus faecium isolates with diverse daptomycin MICs Antimicrob. Agents Chemother. 58 (8) 4527-4534 10.1128/AAC.02686-14
61. Pace, J. L., Krause, K., Johnston, D., Debabov, D., Wu, T., Farrington, L., Lane, C., Higgins, D. L., Christensen, B., and Judice, J. K. et al. 2003, In vitro activity of TD-6424 against Staphylococcus aureus Antimicrob. Agents Chemother. 47 (11) 3602-3604 10.1128/AAC.47.11.3602-3604.2003