Crystal structures of antibiotic-bound complexes of aminoglycoside 2″-phosphotransferase IVa highlight the diversity in substrate binding modes among aminoglycoside kinases

Biochemistry

Volumn 50, Issue 28, 2011, Pages 6237-6244

  Shi, Kun ^a   Houston, Douglas R ^a,b   Berghuis, Albert M ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTICS; AMINOGLYCOSIDES; BACTERIAL ENZYMES; BACTERICIDAL EFFECTS; BINDING MODES; CONFORMATIONAL CHANGE; KANAMYCIN A; KANAMYCINS; PHOSPHOTRANSFERASES; RESISTANCE FACTORS; RESISTANCE TO ANTIBIOTICS; ROTATIONAL SHIFT; STRUCTURAL BASIS; SUBSTRATE BINDING; SUBSTRATE SELECTIVITY; TOBRAMYCIN;

ANTIBIOTICS; BACTERICIDES; BINDING ENERGY; COMPLEXATION; ENZYMES; REFINING;

SUBSTRATES;

AMINOGLYCOSIDE 2'' PHOSPHOTRANSFERASE; AMINOGLYCOSIDE ANTIBIOTIC AGENT; BACTERIAL ENZYME; KANAMYCIN A; TOBRAMYCIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERICIDAL ACTIVITY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG BINDING; DRUG SELECTIVITY; DRUG STRUCTURE; ENTEROCOCCUS; NONHUMAN; PRIORITY JOURNAL;

APOENZYMES; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS; KANAMYCIN; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; TOBRAMYCIN;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS; IVA;

EID: 79960255057     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200747f     Document Type: Article

References (36)

1. Ramirez, M. S. and Tolmasky, M. E. (2010) Aminoglycoside modifying enzymes Drug Resist. Updates 13, 151-171
2. Allison, K. R., Brynildsen, M. P., and Collins, J. J. (2011) Metabolite-enabled eradication of bacterial persisters by aminoglycosides Nature 473, 216-220
3. Burk, D. L. and Berghuis, A. M. (2002) Protein kinase inhibitors and antibiotic resistance Pharmacol. Ther. 93, 10
4. Moazed, D. and Noller, H. F. (197) Interaction of antibiotics with functional sites in 16S ribosomal RNA Nature 327, 389-395
5. Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T., and Ramakrishnan, V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics Nature 407, 340-348
6. Donabedian, S. M., Thal, L. A., Hershberger, E., Perri, M. B., Chow, J. W., Bartlett, P., Jones, R., Joyce, K., Rossiter, S., Gay, K., Johnson, J., Mackinson, C., Debess, E., Madden, J., Angulo, F., and Zervos, M. J. (2003) Molecular characterization of gentamicin-resistant enterococci in the United States: Evidence of spread from animals to humans through food J. Clin. Microbiol. 41, 1109-1113 (Pubitemid 36307114)
7. Smith, C. A. and Baker, E. N. (2002) Aminoglycoside antibiotic resistance by enzymatic deactivation Curr. Drug Targets: Infect. Disord. 2, 143-160 (Pubitemid 34649862)
8. Shaw, K. J., Rather, P. N., Hare, R. S., and Miller, G. H. (1993) Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes Microbiol. Rev. 57, 138-163 (Pubitemid 23078440)
9. Mingeot-Leclercq, M.-P., Glupczynski, Y., and Tulkens, P. M. (1999) Aminoglcyosides: Activity and resistance Antimicrob. Agents Chemother. 43, 11
10. Kao, S. J., You, I., Clewell, D. B., Donabedian, S. M., Zervos, M. J., Petrin, J., Shaw, K. J., and Chow, J. W. (2000) Detection of the high-level aminoglcoside resistance gene aph(2″)-Ib in Enterococcus faecium Antimicrob. Agents Chemother. 44, 4
11. Badarau, A., Shi, Q., Chow, J. W., Zajicek, J., Mobashery, S., and Vakulenko, S. (2008) Aminoglycoside 2″-phosphotransferase type IIIa from Enterococcus J. Biol. Chem. 283, 7638-7647
12. Tsai, S. F., Zervos, M. J., Clewell, D. B., Donabedian, S. M., Sahm, D. F., and Chow, J. W. (1998) A new high-level gentamicin resistance gene, aph(2″)-Id, in Enterococcus spp Antimicrob. Agents Chemother. 42, 1229-1233
13. Alam, M. M., Kobayashi, N., Ishino, M., Sumi, A., Kobayashi, K.-I., Uehara, N., and Watanabe, N. (2005) Detection of a novel aph(2″) Allele (aph[2″ ]-Ie) conferring high-level gentamicin resistance and a spectinomycin resistance gene ant(9)-Ia (aad9) in clinical isolates of Enterococci Microb. Drug Resist. 11, 9
14. Abbassi, M. S., Achour, W., and Hassen, A. B. (2007) High-level gentamicin-resistant Enterococcus faecium strains isolated from bone marrow transplant patients: Accumulation of antibiotic resistance genes, large plasmids and clonal strain dissemination Int. J. Antimicrob. Agents 29, 658-664 (Pubitemid 46722676)
15. Zarrilli, R., Tripodi, M. F., Di Popolo, A., Fortunato, R., Bagattini, M., Crispino, M., Florio, A., Triassi, M., and Utili, R. (2005) Molecular epidemiology of high-level aminoglycoside-resistant enterococci isolated from patients in a university hospital in southern Italy J. Antimicrob. Chemother. 56, 827-835 (Pubitemid 41631904)
16. Toth, M., Frase, H., Antunes, N. T., Smith, C. A., and Vakulenko, S. B. (2010) Crystal structure and kinetic mechanism of aminoglycoside phosphotransferase-2″-IVa Protein Sci. 19, 1565-1576
17. Young, P. G., Walanj, R., Lakshmi, V., Byrnes, L. J., Metcalf, P., Baker, E. N., Vakulenko, S. B., and Smith, C. A. (2009) The crystal structures of substrate and nucleotide complexes of Enterococcus faecium aminoglycoside- 2″-phosphotransferase-IIa [APH(2″)-IIa] provide insights into substrate selectivity in the APH(2″) subfamily J. Bacteriol. 191, 4133-4143
18. Nurizzo, D., Shewry, S. C., Perlin, M. H., Brown, S. A., Dholakia, J. N., Fuchs, R. L., Deva, T., Baker, E. N., and Smith, C. A. (2003) The crystal structure of aminoglycoside-3′-phosphotransferase-IIa, an enzyme responsible for antibiotic resistance J. Mol. Biol. 327, 491-506 (Pubitemid 36298717)
19. Fong, D. H., Lemke, C. T., Hwang, J., Xiong, B., and Berghuis, A. M. (2010) Structure of the antibiotic resistance factor spectinomycin phosphotransferase from Legionella pneumophila J. Biol. Chem. 285, 9545-9555
20. Hon, W. C., McKay, G. A., Thompson, P. R., Sweet, R. M., Yang, D. S. C., Wright, G. D., and Berghuis, A. M. (1997) Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases Cell 89, 887-895 (Pubitemid 27513515)
21. Stogios, P. J., Shakya, T., Evdokimova, E., Savchenko, A., and Wright, G. D. (2011) Structure and function of APH(4)-Ia, a hygromycin B resistance enzyme J. Biol. Chem. 286, 1966-1975
22. Fong, D. H., Xiong, B., Hwang, J., and Berghuis, A. M. (2011) Crystal structures of two aminoglycoside kinases bound with a eukaryotic protein kinase inhibitor PLoS One 6, e19589
23. Toth, M., Chow, J. W., Mobashery, S., and Vakulenko, S. B. (2009) Source of phosphate in the enzymic reaction as a point of distinction among aminoglycoside 2″-phosphotransferases J. Biol. Chem. 284, 6690-6696
24. McKay, G. A., Thompson, P. R., and Wright, G. D. (1994) Broad spectrum aminoglycoside phosphotransferase type III from Enterococcus: Overexpression, purification, and substrate specificity Biochemistry 33, 6936-6944 (Pubitemid 24190818)
25. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. In Methods in Enzymology (Carter, C. W. J. and Sweet, R. M., Eds.) pp 307-326, Academic Press, San Diego. (Pubitemid 27085611)
26. Collaborative Computational Project Number 4 (1994) The CCP4 Suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
27. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 2126-2132
28. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
29. Schuettelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D60, 1355-1363
30. Maviglia, R., Nestorini, R., and Pennisi, M. (2009) Role of old antibiotics in multidrug resistant bacterial infections Curr. Drug Targets 10, 895-905
31. Fong, D. H. and Berghuis, A. M. (2002) Substrate pomiscuity of an aminoglycoside antibiotic resistance enzyme via target mimicry EMBO J. 21, 2323-2331 (Pubitemid 34546705)
32. Fong, D. H. and Berghuis, A. M. (2009) Structural basis of APH(3′)-IIIa-mediated resistance to N1-substituted aminoglycoside antibiotics Antimicrob. Agents Chemother. 53, 3049-3055
33. Vicens, Q. and Westhof, E. (2002) Crystal structure of a complex between the aminoglycoside tobramycin and an oligonucleotide containing the ribosomal decoding A site Chem. Biol. 9, 747-755 (Pubitemid 34656778)
34. Vicens, Q. and Westhof, E. (2003) RNA as a drug target: The case of aminoglycosides ChemBioChem 4, 1018-1023 (Pubitemid 37267590)
35. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
36. The PyMOL Molecular Graphics System, version 1.3 (2008) Schroedinger, LLC, New York.