Molecular Determinants of Antibiotic Recognition and Resistance by Aminoglycoside Phosphotransferase (3′)-IIIa: A Calorimetric and Mutational Analysis

Journal of Molecular Biology

Volumn 369, Issue 1, 2007, Pages 142-156

  Kaul, Malvika ^a   Barbieri, Christopher M ^a   Srinivasan, Annankoil R ^a   Pilch, Daniel S ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

enzyme binding linked drug protonation; isothermal titration calorimetry; kanamycin B; neomycin; pyruvate kinase lactate dehydrogenase coupled detection of aminoglycoside phosphorylation

Indexed keywords

AMINOGLYCOSIDE PHOSPHOTRANSFERASE; KANAMYCIN B; NEOMYCIN; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; CALORIMETRY; CATALYSIS; DRUG SENSITIVITY; ENZYME BINDING; ENZYME CHEMISTRY; ENZYME PHOSPHORYLATION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE; PHENOTYPE; PKA; PRIORITY JOURNAL; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS;

EID: 34247397853     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.103     Document Type: Article

References (27)

1. Moazed D., and Noller H.F. Interaction of antibiotics with functional sites in 16 S ribosomal RNA. Nature 327 (1987) 389-394
2. Puglisi J.D., Blanchard S.C., Dahlquist K.D., Eason R.G., Fourmy D., Lynch S.R., et al. Aminoglycoside antibiotics and decoding. In: Garrett R.A., Douthwaite S.R., Liljas A., Matheson A.T., Moore P.B., and Noller H.F. (Eds). The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions (2000), ASM Press, Washington, DC 419-429
3. Magnet S., and Blanchard J.S. Molecular insights into aminoglycoside action and resistance. Chem. Rev. 105 (2005) 477-498
4. Shaw K.J., Rather P.N., Hare R.S., and Miller G.H. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Mol. Biol. Rev. 57 (1993) 138-163
5. Wright G.D., and Thompson P.R. Aminoglycoside phosphotransferases: proteins, structure, and mechanism. Front. Biosci. 4 (1999) D9-D21
6. Kim C., and Mobashery S. Phosphoryl transfer by aminoglycoside 3′-phosphotransferases and manifestation of antibiotic resistance. Bioorg. Chem. 33 (2005) 149-158
7. McKay G.A., Thompson P.R., and Wright G.D. Broad spectrum aminoglycoside phosphotransferase type III from Enterococcus: overexpression, purification, and substrate specificity. Biochemistry 33 (1994) 6936-6944
8. Hon W.C., McKay G.A., Thompson P.R., Sweet R.M., Yang D.S., Wright G.D., and Berghuis A.M. Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases. Cell 89 (1997) 887-895
9. Thompson P.R., Schwartzenhauer J., Hughes D.W., Berghuis A.M., and Wright G.D. The COOH terminus of aminoglycoside phosphotransferase (3′)-IIIa is critical for antibiotic recognition and resistance. J. Biol. Chem. 274 (1999) 30697-30706
10. Boehr D.D., Thompson P.R., and Wright G.D. Molecular mechanism of aminoglycoside antibiotic kinase APH(3′)-IIIa: roles of conserved active site residues. J. Biol. Chem. 276 (2001) 23929-23936
11. Fong D.H., and Berghuis A.M. Substrate promiscuity of an aminoglycoside antibiotic resistance enzyme via target mimicry. EMBO J. 21 (2002) 2323-2331
12. Roestamadji J., Grapsas I., and Mobashery S. Loss of individual electrostatic interactions between aminoglycoside antibiotics and resistance enzymes as an effective means to overcoming bacterial drug resistance. J. Am. Chem. Soc. 117 (1995) 11060-11069
13. Fukada H., and Takahashi K. Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride. Proteins: Struct. Funct. Genet. 33 (1998) 159-166
14. Kaul M., Barbieri C.M., Kerrigan J.E., and Pilch D.S. Coupling of drug protonation to the specific binding of aminoglycosides to the A site of 16 S rRNA: elucidation of the number of drug amino groups involved and their identities. J. Mol. Biol. 326 (2003) 1373-1387
15. Özen C., and Serpersu E.H. Thermodynamics of aminoglycoside binding to aminoglycoside-3′-phosphotransferase IIIa studied by isothermal titration calorimetry. Biochemistry 43 (2004) 14667-14675
16. Doyle M.L., Louie G., Dal Monte P.R., and Sokoloski T.D. Tight binding affinities determined from thermodynamic linkage to protons by titration calorimetry. Methods Enzymol. 259 (1995) 183-194
17. Pilch D.S., Kaul M., and Barbieri C.M. Ribosomal RNA recognition by aminoglycoside antibiotics. Top. Curr. Chem. 253 (2005) 179-204
18. 15N NMR study. Biophys. J. 90 (2006) 1338-1349
19. Böhm G., Muhr R., and Jaenicke R. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. Des. Selec. 5 (1992) 191-195
20. Trieu-Cuot P., and Courvalin P. Nucleotide sequence of the Streptococcus faecalis plasmid gene encoding the 3′5″-aminoglycoside phosphotransferase type III. Gene 23 (1983) 331-341
21. Botto R.E., and Coxon B. Nitrogen-15 nuclear magnetic resonance spectroscopy of neomycin B and related aminoglycosides. J. Am. Chem. Soc. 105 (1983) 1021-1028
22. 15N nuclear magnetic resonance spectroscopy. The nebramycin aminoglycosides. J. Am. Chem. Soc. 98 (1976) 6885-6888
23. Koch K.F., Merkel K.E., O'Connor S.C., Occolowitz J.L., Paschal J.W., and Dorman D.E. Structures of some of the minor aminoglycoside factors of the nebramycin fermentation. J. Org. Chem. 43 (1978) 1430-1434
24. Case D.A., Darden T.A., Cheatham III T.E., Simmerling C.L., Wang J., Duke R.E., et al. AMBER 8.0 (2004), University of California, San Francisco, CA
25. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz Jr. K.M., Ferguson D.M., et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
26. Wang J., Cieplak P., and Kollman P.A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules?. J. Comput. Chem. 21 (2000) 1049-1074
27. Goldman P.R., and Northrop D.B. Purification and spectrophotometric assay of neomycin phosphotransferase II1. Biochem. Biophys. Res. Commun. 69 (1976) 230-236