Thermodynamics of aminoglycoside binding to aminoglycoside-3′- phosphotransferase IIIa studied by isothermal titration calorimetry

Biochemistry

Volumn 43, Issue 46, 2004, Pages 14667-14675

  Özen, Can ^a   Serpersu, Engin H ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; BINDING ENERGY; PARAMETER ESTIMATION; SUBSTRATES;

AMINOGLYCOSIDE; PHOSPHOTRANSFERASE; THERMODYNAMIC PARAMETERS;

THERMODYNAMICS;

AMIKACIN; AMINOGLYCOSIDE 3' PHOSPHOTRANSFERASE IIIA; AMINOGLYCOSIDE ANTIBIOTIC AGENT; FRAMYCETIN; KANAMYCIN A; KANAMYCIN B; LIVIDOMYCIN; PAROMOMYCIN; PHOSPHOTRANSFERASE; RIBOSTAMYCIN; TOBRAMYCIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CALORIMETRY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENTHALPY; ENTROPY; ENZYME KINETICS; MOLECULAR SIZE; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; TITRIMETRY;

ADENOSINE TRIPHOSPHATE; AMINES; AMINOGLYCOSIDES; BINDING SITES; CALCIUM; CALORIMETRY; ENTROPY; HEXOSAMINES; HYDROXIDES; KANAMYCIN; KANAMYCIN KINASE; MACROMOLECULAR SUBSTANCES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 8744252619     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0487286     Document Type: Article

References (36)

1. Davies, J. E. (1991) in Antibiotics in Laboratory Medicine (Lorian, V., Ed.) pp 691-713, Williams and Wilkins, Baltimore, MD.
2. Mingeot-Leclercq, M. P., Glupczynski, Y., and Tulkens, P. M. (1999) Aminoglycosides: activity and resistance, Antimicrob. Agents Chemother. 43, 727-737.
3. Umezawa, H. (1974) in Advances in Carbohydrate Chemistry and Biochemistry (Tipson, R. S., and Horton, D., Eds.) pp 183-225, Academic Press, New York, San Francisco, and London.
4. Moazed, D., and Noller, H. F. (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA, Nature 327, 389-394.
5. Davies, J. (1994) Inactivation of antibiotics and the dissemination of resistance genes, Science 264, 375-382.
6. 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.
7. Fong, D. H., and Berghuis, A. M. (2002) Substrate promiscuity of an aminoglycoside antibiotic resistance enzyme via target mimicry, EMBO J. 21, 2323-2331.
8. 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.
9. McKay, G. A., and Wright, G. D. (1995) Kinetic mechanism of aminoglycoside phosphotransferase type IIIa. Evidence for a Theorell-Chance mechanism, J. Biol. Chem. 270, 24686-24692.
10. McKay, G. A., and Wright, G. D. (1996) Catalytic mechanism of enterococcal kanamycin kinase (APH(3′)-IIIa): viscosity, thio, and solvent isotope effects support a Theorell-Chance mechanism, Biochemistry 35, 8680-8685.
11. Boehr, D. D., Thompson, P. R., and Wright, G. D. (2001) Molecular mechanism of aminoglycoside antibiotic kinase APH(3′)-IIIa: roles of conserved active site residues, J. Biol. Chem. 276, 23929-23936.
12. Burk, D. L., Hon, W. C., Leung, A. K., and Berghuis, A. M. (2001) Structural analyses of nucleotide binding to an aminoglycoside phosphotransferase, Biochemistry 40, 8756-8764.
13. Cox, J. R., McKay, G. A., Wright, G. D., and Serpersu, E. H. (1996) Arrangement of substrates at the active site of an aminoglycoside antibiotic 3′-phosphotransferase as determined by NMR, J. Am. Chem. Soc. 118, 1295-1301.
14. Cox, J. R., and Serpersu, E. H. (1997) Biologically important conformations of aminoglycoside antibiotics bound to an aminoglycoside 3′-phosphotransferase as determined by transferred nuclear Overhauser effect spectroscopy, Biochemistry 36, 2353-2359.
15. DiGiammarino, E. L., Draker, K. A., Wright, G. D., and Serpersu, E. H. (1998) Solution studies of isepamicin and conformational comparisons between isepamicin and butirosin A when bound to an aminoglycoside 6′-N- acetyltransferase determined by NMR spectroscopy, Biochemistry 37, 3638-3644.
16. Mohler, M. L., Cox, J. R., and Serpersu, E. H. (1998) Aminoglycoside phosphotransferase(3′)-IIIa (APH(3′)-IIIa)-bound conformation of the aminoglycoside lividomycin A characterized by NMR, Carbohydr. Lett. 3, 17-24.
17. Cox, J. R., Ekman, D. R., DiGiammarino, E. L., Akal-Strader, A., and Serpersu, E. H. (2000) Aminoglycoside antibiotics bound to aminoglycoside- detoxifying enzymes and RNA adopt similar conformations, Cell Biochem. Biophys. 33, 297-308.
18. Boehr, D. D., Farley, A. R., Wright, G. D., and Cox, J. R. (2002) Analysis of the pi-pi stacking interactions between the aminoglycoside antibiotic kinase APH(3′)-IIIa and its nucleotide ligands, Chem. Biol. 9, 1209-1217.
19. Ozen, C., and Serpersu, E. H. (2004) Annual Meeting Abstracts Issue, p 495-Pos, Biophysical Society, Bethesda, MD.
20. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
21. Ladbury, J. E., and Chowdhry, B. Z. (1996) Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions, Chem. Biol. 3, 791-801.
22. Jelesarov, I., and Bosshard, H. R. (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition, J. Mol. Recognit. 12, 3-18.
23. Leavitt, S., and Freire, E. (2001) Direct measurement of protein binding energetics by isothermal titration calorimetry, Curr. Opin. Struct. Biol. 11, 560-566.
24. Surolia, A., Sharon, N., and Schwarz, F. P. (1996) Thermodynamics of monosaccharide and disaccharide binding to Erythrina corallodendron lectin, J. Biol. Chem. 271, 17697-17703.
25. Dam, T. K., and Brewer, C. F. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry, Chem. Rev. 102, 387-429.
26. Chervenak, M. C., and Toone, E. J. (1995) Calorimetric analysis of the binding of lectins with overlapping carbohydrate-binding ligand specificities, Biochemistry 34, 5685-5695.
27. Xie, H., Bolam, D. N., Nagy, T., Szabo, L., Cooper, A., Simpson, P. J., Lakey, J. H., Williamson, M. P., and Gilbert, H. J. (2001) Role of hydrogen bonding in the interaction between a xylan binding module and xylan, Biochemistry 40, 5700-5707.
28. Kaul, M., Barbieri, C. M., Kerrigan, J. E., and Pilch, D. S. (2003) 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, 1373-1387.
29. Hegde, S. S., Dam, T. K., Brewer, C. F., and Blanchard, J. S. (2002) Thermodynamics of aminoglycoside and acyl-coenzyme A binding to the Salmonella enterica AAC(6′)-Iy aminoglycoside N-acetyltransferase, Biochemistry 41, 7519-7527.
30. Bernhard, S. A. (1956) Ionization constants and heats of tris-(hydroxymethyl)aminomethane and phosphate buffers, J. Biol. Chem. 218, 961-969.
31. Fukada, H., and Takahashi, K. (1998) Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride, Proteins 33, 159-166.
32. Doyle, M. L., Louie, G., Dal Monte, P. R., and Sokoloski, T. D. (1995) Tight binding affinities determined from thermodynamic linkage to protons by titration calorimetry, Methods Enzymol. 259, 183-194.
33. Walter, F., Vicens, Q., and Westhof, E. (1999) Aminoglycoside-RNA interactions, Curr. Opin. Chem. Biol. 3, 694-704.
34. McKay, G. A., Roestamadji, J., Mobashery, S., and Wright, G. D. (1996) Recognition of aminoglycoside antibiotics by enterococcal-staphylococcal aminoglycoside 3′-phosphotransferase type IIIa: role of substrate amino groups, Antimicrob. Agents Chemother. 40, 2648-2650.
35. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
36. Delano, W. L. (2002) The PyMol Molecular Graphics System, DeLano Scientific, San Carlos, CA.