Cosubstrate tolerance of the aminoglycoside resistance enzyme eis from Mycobacterium tuberculosis

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 11, 2012, Pages 5831-5838

  Chen, Wenjing ^a   Green, Keith D ^a   Garneau Tsodikova, Sylvie ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A; ACYLTRANSFERASE; AMIKACIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; BACTERIAL PROTEIN; MALONYL COENZYME A; MOLECULAR SCAFFOLD; NETILMICIN; PROPIONYL COENZYME A; PROTEIN ENHANCED INTRACELLULAR SURVIVAL; UNCLASSIFIED DRUG;

ACETYLATION; ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; ENZYME SUBSTRATE; MASS SPECTROMETRY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; THIN LAYER CHROMATOGRAPHY;

ACYL COENZYME A; ACYLATION; AMIKACIN; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; CHROMATOGRAPHY, THIN LAYER; FRAMYCETIN; KANAMYCIN RESISTANCE; MASS SPECTROMETRY; MYCOBACTERIUM TUBERCULOSIS; NETILMICIN; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84868028203     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00932-12     Document Type: Article

References (46)

1. Bernhardt P, Usera AR, O'Connor SE. 2010. Biocatalytic asymmetric formation of tetrahydro-beta-carbolines. Tetrahedron Lett. 51:4400-4402.
2. Boehr DD, Daigle DM, Wright GD. 2004. Domain-domain interactions in the aminoglycoside antibiotic resistance enzyme AAC(6')-APH(2′″). Biochemistry 43:9846-9855.
3. Burk DL, Ghuman N, Wybenga-Groot LE, Berghuis AM. 2003. X-ray structure of the AAC(6')-Ii antibiotic resistance enzyme at 1.8 A resolution; examination of oligomeric arrangements in GNAT superfamily members. Protein Sci. 12:426-437.
4. Burk DL, Xiong B, Breitbach C, Berghuis AM. 2005. Structures of aminoglycoside acetyltransferase AAC(6')-Ii in a novel crystal form: structural and normal-mode analyses. Acta Crystallogr. D Biol. Crystal-logr. 61:1273-1279.
5. Busto E, Gotor-Fernandez V, Gotor V. 2010. Hydrolases: catalytically promiscuous enzymes for non-conventional reactions in organic synthesis. Chem. Soc. Rev. 39:4504-4523.
6. Caldwell SJ, Berghuis AM. 2012. Small-angle X-ray scattering analysis of the bifunctional antibiotic resistance enzyme aminoglycoside (6') acetyltransferase-ie/aminoglycoside (2′″) phosphotransferase-ia reveals a rigid solution structure. Antimicrob. Agents Chemother. 56:1899-1906.
7. Caminero JA, Sotgiu G, Zumla A, Migliori GB. 2010. Best drug treatment for multidrug-resistant and extensively drug-resistant tuberculosis. Lancet Infect. Dis. 10:621-629.
8. Campbell PJ, et al. 2011. Molecular detection of mutations associated with first- and second-line drug resistance compared with conventional drug susceptibility testing of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 55:2032-2041.
9. Centron D, Roy PH. 2002. Presence of a group II intron in a multiresistant Serratia marcescens strain that harbors three integrons and a novel gene fusion. Antimicrob. Agents Chemother. 46:1402-1409.
10. Chen W, Biswas T, Porter VR, Tsodikov OV, Garneau-Tsodikova S. 2011. Unusual regioversatility of acetyltransferase Eis, a cause of drug resistance in XDR-TB. Proc. Natl. Acad. Sci. U. S. A. 108:9804-9808.
11. Chen W, Green KD, Tsodikov OV, Garneau-Tsodikova S. 2012. The aminoglycoside multi-acetylating activity of the enhanced intracellular survival (Eis) protein from Mycobacterium smegmatis and its inhibition. Biochemistry 51:4959-4967.
12. Courvalin P, Weisblum B, Davies J. 1977. Aminoglycoside-modifying enzyme of an antibiotic-producing bacterium acts as a determinant of antibiotic resistance in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A 74:999-1003.
13. Dahl JL, Wei J, Moulder JW, Laal S, Friedman RL. 2001. Subcellular localization of the intracellular survival-enhancing Eis protein of Mycobacterium tuberculosis. Infect. Immun. 69:4295-4302.
14. 1 and a fused product of aac3-Ib/aac6'-Ib' gene cassettes in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 46: 638-645.
15. Dye C, Williams BG. 2010. The population dynamics and control of tuberculosis. Science 328:856-861.
16. Fridman M, et al. 2007. Chemoenzymatic formation of novel aminocoumarin antibiotics by the enzymes CouN1 and CouN7. Biochemistry 46: 8462-8471.
17. Georghiou SB, et al. 2012. Evaluation of genetic mutations associated with Mycobacterium tuberculosis resistance to amikacin, kanamycin and capreomycin: a systematic review. PLoS One 7:e33275. doi:10.1371/journal.pone. 0033275.
18. Gillingham DG, Stallforth P, Adibekian A, Seeberger PH, Hilvert D. 2010. Chemoenzymatic synthesis of differentially protected 3-deoxysugars. Nat. Chem. 2:102-105.
19. Green KD, Chen W, Garneau-Tsodikova S. 2011. Effects of altering aminoglycoside structures on bacterial resistance enzyme activities. Antimicrob. Agents Chemother. 55:3207-3213.
20. Green KD, Chen W, Houghton JL, Fridman M, Garneau-Tsodikova S. 2010. Exploring the substrate promiscuity of drug-modifying enzymes for the chemoenzymatic generation of N-acylated aminoglycosides. Chembiochem 11:119-126.
21. Green KD, Fridman M, Garneau-Tsodikova S. 2009. hChAT: a tool for the chemoenzymatic generation of potential acetyl/butyrylcholinesterase inhibitors. Chembiochem 10:2191-2194.
22. Houghton JL, Green KD, Chen W, Garneau-Tsodikova S. 2010. The future of aminoglycosides: the end or renaissance? Chembiochem 11: 880-902.
23. Hu X, Norris AL, Baudry J, Serpersu EH. 2011. Coenzyme A binding to the aminoglycoside acetyltransferase (3)-IIIb increases conformational sampling of antibiotic binding site. Biochemistry 50:10559-10565.
24. Kim C, Hesek D, Zajicek J, Vakulenko SB, Mobashery S. 2006. Characterization of the bifunctional aminoglycoside-modifying enzyme ANT(3′″)Ii/AAC(6')-IId from Serratia marcescens. Biochemistry 45: 8368-8377.
25. Kim C, Villegas-Estrada A, Hesek D, Mobashery S. 2007. Mechanistic characterization of the bifunctional aminoglycoside-modifying enzyme AAC(3)-Ib/AAC(6')-Ib' from Pseudomonas aeruginosa. Biochemistry 46:5270-5282.
26. Kim KH, et al. 2012. Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7. Proc. Natl. Acad. Sci. U. S. A. 109:7729-7734.
27. Klimecka MM, et al. 2011. Structural analysis of a putative aminoglycoside N-acetyltransferase from Bacillus anthracis. J. Mol. Biol. 410:411-423.
28. Lella RK, Sharma C. 2007. Eis (enhanced intracellular survival) protein of Mycobacterium tuberculosis disturbs the cross regulation of T-cells. J. Biol. Chem. 282:18671-18675.
29. Li S, et al. 2009. Selective oxidation of carbolide C-H bonds by an engineered macrolide P450 mono-oxygenase. Proc. Natl. Acad. Sci. U. S. A 106:18463-18468.
30. Magalhaes ML, Blanchard JS. 2005. The kinetic mechanism of AAC3-IV aminoglycoside acetyltransferase from Escherichia coli. Biochemistry 44: 16275-16283.
31. Magalhaes ML, et al. 2008. Kinetic and structural analysis of bisubstrate inhibition of the Salmonella enterica aminoglycoside 6'-N-acetyltransferase. Biochemistry 47:579-584.
32. Paterson DL, Bonomo RA. 2005. Extended-spectrum beta-lactamases: a clinical update. Clin. Microbiol. Rev. 18:657-686.
33. Piasecki SK, et al. 2011. Employing modular polyketide synthase ketore-ductases as biocatalysts in the preparative chemoenzymatic syntheses of diketide chiral building blocks. Chem. Biol. 18:1331-1340.
34. Porter VR, Green KD, Zolova OE, Houghton JL, Garneau-Tsodikova S. 2010. Dissecting the cosubstrate structure requirements of the Staphylococcus aureus aminoglycoside resistance enzyme ANT(4'). Biochem. Biophys. Res. Commun. 403:85-90.
35. Ramirez MS, Tolmasky ME. 2010. Aminoglycoside modifying enzymes. Drug Resist. Updat. 13:151-171.
36. Samuel LP, et al. 2007. Expression, production and release of the Eis protein by Mycobacterium tuberculosis during infection of macrophages and its effect on cytokine secretion. Microbiology 153:529-540.
37. Shin DM, et al. 2010. Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog. 6:e1001230. doi:10.1371/journal.ppat.1001230.
38. Tsitovich PB, Pushechnikov A, French JM, Disney MD. 2010. A chemoenzymatic route to diversify aminoglycosides enables a microarray-based method to probe acetyltransferase activity. Chembiochem 11:1656-1660.
39. Vetting MW, Hegde SS, Javid-Majd F, Blanchard JS, Roderick SL. 2002. Aminoglycoside 2'-N-acetyltransferase from Mycobacterium tuberculosis in complex with coenzyme A and aminoglycoside substrates. Nat. Struct. Biol. 9:653-658.
40. Vetting MW, Magnet S, Nieves E, Roderick SL, Blanchard JS. 2004. A bacterial acetyltransferase capable of regioselective N-acetylation of antibiotics and histones. Chem. Biol. 11:565-573.
41. Vetting MW, et al. 2008. Mechanistic and structural analysis of amin-oglycoside N-acetyltransferase AAC(6')-Ib and its bifunctional, fluoro-quinolone-active AAC(6')-Ib-cr variant. Biochemistry 47:9825-9835.
42. Wei J, et al. 2000. Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J. Bacteriol. 182:377-384.
43. Wolf E, et al. 1998. Crystal structure of a GCN5-related N-acetyltransferase: Serratia marcescens aminoglycoside 3-N-acetyltransferase. Cell 94:439 - 449.
44. Wybenga-Groot LE, Draker K, Wright GD, Berghuis AM. 1999. Crystal structure of an aminoglycoside 6'-N-acetyltransferase: defining the GCN5-related N-acetyltransferase superfamily fold. Structure 7:497-507.
45. Zaunbrecher MA, Sikes RD, Jr, Metchock B, Shinnick TM, Posey JE. 2009. Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 106:20004-20009.
46. Zhang W, Fisher JF, Mobashery S. 2009. The bifunctional enzymes of antibiotic resistance. Curr. Opin. Microbiol. 12:505-511.