Plasticity, dynamics, and inhibition of emerging tetracycline resistance enzymes

Nature Chemical Biology

Volumn 13, Issue 7, 2017, Pages 730-736

  Park, Jooyoung ^a   Gasparrini, Andrew J ^a   Reck, Margaret R ^b   Symister, Chanez T ^b   Elliott, Jennifer L ^a   Vogel, Joseph P ^a   Wencewicz, Timothy A ^b   Dantas, Gautam ^a,c   Tolia, Niraj H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; OXIDOREDUCTASE INHIBITOR; TETRACYCLINE DERIVATIVE; ANTIINFECTIVE AGENT; ENZYME INHIBITOR; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME BINDING; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PURIFICATION; IN VITRO STUDY; LEGIONELLA LONGBEACHAE; METAGENOMICS; MOLECULAR DYNAMICS; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; CHEMISTRY; CONFORMATION; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION;

ANTI-BACTERIAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FLAVIN-ADENINE DINUCLEOTIDE; LEGIONELLA LONGBEACHAE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TETRACYCLINE; TETRACYCLINE RESISTANCE;

EID: 85021135851     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2376     Document Type: Article

References (60)

1. Knapp, C.W., Dolfing, J., Ehlert, P.A. & Graham, D.W. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44, 580-587 (2010).
2. Kinch, M.S., Patridge, E., Plummer, M. & Hoyer, D. An analysis of FDA-approved drugs for infectious disease: antibacterial agents. Drug Discov. Today 19, 1283-1287 (2014).
3. Davies, J. Inactivation of antibiotics and the dissemination of resistance genes. Science 264, 375-382 (1994).
4. Allen, H.K. et al. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251-259 (2010).
5. Berendonk, T.U. et al. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13, 310-317 (2015).
6. Benveniste, R. & Davies, J. Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria. Proc. Natl. Acad. Sci. USA 70, 2276-2280 (1973).
7. D'Costa, V.M. et al. Antibiotic resistance is ancient. Nature 477, 457-461 (2011).
8. Forsberg, K.J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107-1111 (2012).
9. Forsberg, K.J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature 509, 612-616 (2014).
10. Yong, D. et al. Characterization of a new metallo-β-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob. Agents Chemother. 53, 5046-5054 (2009).
11. Liu, Y.Y. et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis. 16, 161-168 (2016).
12. Poirel, L., Rodriguez-Martinez, J.M., Mammeri, H., Liard, A. & Nordmann, P. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49, 3523-3525 (2005).
13. Thaker, M., Spanogiannopoulos, P. & Wright, G.D. The tetracycline resistome. Cell. Mol. Life Sci. 67, 419-431 (2010).
14. State of the World's Antibiotics. 2015. (Center for Disease Dynamics, Economics & Policy, Washington, DC, USA, 2015).
15. Kasbekar, N. Tigecycline: a new glycylcycline antimicrobial agent. Am. J. Health Syst. Pharm. 63, 1235-1243 (2006).
16. Sutcliffe, J.A., O'Brien, W., Fyfe, C. & Grossman, T.H. Antibacterial activity of eravacycline (TP-434), a novel fluorocycline, against hospital and community pathogens. Antimicrob. Agents Chemother. 57, 5548-5558 (2013).
17. Macone, A.B. et al. In vitro and in vivo antibacterial activities of omadacycline, a novel aminomethylcycline. Antimicrob. Agents Chemother. 58, 1127-1135 (2014).
18. Chopra, I. & Roberts, M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65, 232-260 (2001).
19. Park, B.H. & Levy, S.B. The cryptic tetracycline resistance determinant on Tn4400 mediates tetracycline degradation as well as tetracycline efflux. Antimicrob. Agents Chemother. 32, 1797-1800 (1988).
20. Speer, B.S. & Salyers, A.A. Characterization of a novel tetracycline resistance that functions only in aerobically grown Escherichia coli. J. Bacteriol. 170, 1423-1429 (1988).
21. Whittle, G., Hund, B.D., Shoemaker, N.B. & Salyers, A.A. Characterization of the 13-kilobase ermF region of the Bacteroides conjugative transposon CTnDOT. Appl. Environ. Microbiol. 67, 3488-3495 (2001).
22. Nonaka, L. & Suzuki, S. New Mg2+-dependent oxytetracycline resistance determinant tet 34 in Vibrio isolates from marine fish intestinal contents. Antimicrob. Agents Chemother. 46, 1550-1552 (2002).
23. Diaz-Torres, M.L. et al. Novel tetracycline resistance determinant from the oral metagenome. Antimicrob. Agents Chemother. 47, 1430-1432 (2003).
24. Ghosh, S., Sadowsky, M.J., Roberts, M.C., Gralnick, J.A. & LaPara, T.M. Sphingobacterium sp. strain PM2-P1-29 harbours a functional tet(X) gene encoding for the degradation of tetracycline. J. Appl. Microbiol. 106, 1336-1342 (2009).
25. Yang, W. et al. TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J. Biol. Chem. 279, 52346-52352 (2004).
26. Moore, I.F., Hughes, D.W. & Wright, G.D. Tigecycline is modified by the flavin-dependent monooxygenase TetX. Biochemistry 44, 11829-11835 (2005).
27. Volkers, G., Palm, G.J., Weiss, M.S., Wright, G.D. & Hinrichs, W. Structural basis for a new tetracycline resistance mechanism relying on the TetX monooxygenase. FEBS Lett. 585, 1061-1066 (2011).
28. Forsberg, K.J., Patel, S., Wencewicz, T.A. & Dantas, G. The tetracycline destructases: a novel family of tetracycline-inactivating enzymes. Chem. Biol. 22, 888-897 (2015).
29. Drawz, S.M., Papp-Wallace, K.M. & Bonomo, R.A. New β-lactamase inhibitors: a therapeutic renaissance in an MDR world. Antimicrob. Agents Chemother. 58, 1835-1846 (2014).
30. Hornak, V., Okur, A., Rizzo, R.C. & Simmerling, C. HIV-1 protease flaps spontaneously close to the correct structure in simulations following manual placement of an inhibitor into the open state. J. Am. Chem. Soc. 128, 2812-2813 (2006).
31. Pesnot, T., Jørgensen, R., Palcic, M.M. & Wagner, G.K. Structural and mechanistic basis for a new mode of glycosyltransferase inhibition. Nat. Chem. Biol. 6, 321-323 (2010).
32. Cazalet, C. et al. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet. 6, e1000851 (2010).
33. Whiley, H. & Bentham, R. Legionella longbeachae and legionellosis. Emerg. Infect. Dis. 17, 579-583 (2011).
34. Ballou, D.P., Entsch, B. & Cole, L.J. Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases. Biochem. Biophys. Res. Commun. 338, 590-598 (2005).
35. van Berkel, W.J., Kamerbeek, N.M. & Fraaije, M.W. Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J. Biotechnol. 124, 670-689 (2006).
36. Gatti, D.L. et al. The mobile flavin of 4-OH benzoate hydroxylase. Science 266, 110-114 (1994).
37. Massey, V. Activation of molecular oxygen by flavins and flavoproteins. J. Biol. Chem. 269, 22459-22462 (1994).
38. Volkers, G. et al. Putative dioxygen-binding sites and recognition of tigecycline and minocycline in the tetracycline-degrading monooxygenase TetX. Acta Crystallogr. D Biol. Crystallogr. 69, 1758-1767 (2013).
39. Liu, L.K. et al. The structure of the antibiotic deactivating, N-hydroxylating rifampicin monooxygenase. J. Biol. Chem. 291, 21553-21562 (2016).
40. Gibson, M., Nur-e-alam, M., Lipata, F., Oliveira, M.A. & Rohr, J. Characterization of kinetics and products of the Baeyer-Villiger oxygenase MtmOIV, the key enzyme of the biosynthetic pathway toward the natural product anticancer drug mithramycin from Streptomyces argillaceus. J. Am. Chem. Soc. 127, 17594-17595 (2005).
41. Wang, P., Bashiri, G., Gao, X., Sawaya, M.R. & Tang, Y. Uncovering the enzymes that catalyze the final steps in oxytetracycline biosynthesis. J. Am. Chem. Soc. 135, 7138-7141 (2013).
42. Yuen, P.H. & Sokoloski, T.D. Kinetics of concomitant degradation of tetracycline to epitetracycline, anhydrotetracycline, and epianhydrotetracycline in acid phosphate solution. J. Pharm. Sci. 66, 1648-1650 (1977).
43. Palmer, A.C., Angelino, E. & Kishony, R. Chemical decay of an antibiotic inverts selection for resistance. Nat. Chem. Biol. 6, 105-107 (2010).
44. Liu, F. & Myers, A.G. Development of a platform for the discovery and practical synthesis of new tetracycline antibiotics. Curr. Opin. Chem. Biol. 32, 48-57 (2016).
45. Lienhart, W.D., Gudipati, V. & Macheroux, P. The human flavoproteome. Arch. Biochem. Biophys. 535, 150-162 (2013).
46. Leski, T.A. et al. Multidrug-resistant tet(X)-containing hospital isolates in Sierra Leone. Int. J. Antimicrob. Agents 42, 83-86 (2013).
47. Deng, M. et al. Molecular epidemiology and mechanisms of tigecycline resistance in clinical isolates of Acinetobacter baumannii from a Chinese university hospital. Antimicrob. Agents Chemother. 58, 297-303 (2014).
48. Boucher, H.W. et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48, 1-12 (2009).
49. Walsh, C.T. & Wencewicz, T.A. Flavoenzymes: versatile catalysts in biosynthetic pathways. Nat. Prod. Rep. 30, 175-200 (2013).
50. Merriam, J.J., Mathur, R., Maxfield-Boumil, R. & Isberg, R.R. Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect. Immun. 65, 2497-2501 (1997).
51. Feeley, J.C. et al. Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J. Clin. Microbiol. 10, 437-441 (1979).
52. Berger, K.H. & Isberg, R.R. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7, 7-19 (1993).
53. Sexton, J.A. et al. The Legionella pneumophila PilT homologue DotB exhibits ATPase activity that is critical for intracellular growth. J. Bacteriol. 186, 1658-1666 (2004).
54. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
55. Winn, M.D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
56. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
57. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
58. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
59. CLSI. Methods for Dilution Antimicrobial Susceptibility Testing for Bacteria That Grow Aerobically; Approved Standard-Tenth Edition. Vol. M07-A10 (Clinical and Laboratory Standards Institute, 2015).
60. Berenbaum, M.C. A method for testing for synergy with any number of agents. J. Infect. Dis. 137, 122-130 (1978).