Detection of specific solvent rearrangement regions of an enzyme: NMR and ITC studies with aminoglycoside phosphotransferase(3′)-IIIa

Biochemistry

Volumn 47, Issue 1, 2008, Pages 40-49

  Özen, Can ^a   Norris, Adrianne L ^a   Land, Miriam L ^a,b   Tjioe, Elina ^a   Serpersu, Engin H ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE PHOSPHOTRANSFERASE; HYDROPHOBIC PATCHES; NEOMYCINS;

AMIDES; BINDING SITES; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE; PROTONS; SOLVENTS;

ENZYMES;

AMINOGLYCOSIDE DERIVATIVE; AMINOGLYCOSIDE PHOSPHOTRANSFERASAE; KANAMYCIN; KANAMYCIN A; KANAMYCIN B; NEOMYCIN; PAROMOMYCIN; PHOSPHOTRANSFERASE; RIBOSTAMYCIN; SOLVENT; TOBRAMYCIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL ANALYSIS; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

AMINOGLYCOSIDES; CALORIMETRY; DEUTERIUM OXIDE; KANAMYCIN; KANAMYCIN KINASE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR STRUCTURE; NEOMYCIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SOLVENTS; SUBSTRATE SPECIFICITY; THERMODYNAMICS; WATER;

EID: 37849019274     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701711j     Document Type: Article

References (52)

1. Moazed, D., and Noller, H. F. (1987) Interaction of antibiotics with functional sites in 16 S ribosomal RNA, Nature 327, 389-394.
2. Umezawa, H. (1974) Biochemical mechanism of resistance to aminoglycosidic antibiotics, Adv. Carbohydr. Chem. Biochem. 30, 183-225.
3. Benveniste, R., and Davies, J. (1973) Aminoglycoside Antibiotic- Inactivating Enzymes in Actinomycetes Similar to Those Present in Clinical Isolates of Antibiotic-Resistant Bacteria, Proc. Natl. Acad. Sci. U.S.A. 70, 2276-2280.
4. Davies, J. E. (1994) Inactivation of antibiotics and the dissemination of resistance genes, Science 264, 375-382.
5. Magnet, S., and Blanchard, J. S. (2005) Molecular insights into aminoglycoside action and resistance, Chem. Rev. 105, 477-497.
6. 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.
7. 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.
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. Fong, D. H., and Berghuis, A. M. (2002) Substrate promiscuity of an aminoglycoside antibiotic resistance enzyme via target mimicry, EMBO J. 21, 2323-2331.
11. Liu, M., Haddad, J., Azucena, E., Kotra, L. P., Kirzhner, M., and Mobashery, S. (2000) Tethered bisubstrate derivatives as probes for mechanism and as inhibitors of aminoglycoside 3′-phosphotransferases, J. Org. Chem. 65, 7422-31.
12. Ozen, C., Malek, J. M., and Serpersu, E. H. (2006) Dissection of aminoglycoside-enzyme interactions: A calorimetric and NMR study of neomycin B binding to the aminoglycoside phosphotransferase(3′)-IIIa, J. Am. Chem. Soc. 128, 15248-15254.
13. Ozen, C., and Serpersu, E. H. (2004) Thermodynamics of aminoglycoside binding to aminoglycoside-3′-phosphotransferase IIIa studied by isothermal titration calorimetry, Biochemistry 43, 14667-14675.
14. Burkhalter, N. F., Dimick, S. M., and Toone, E. J. (2000) Protein-Carbohydrate interaction: Fundamental considerations, in Carbohydrates in Chemistry and Biology (B. Ernst, G. W. H., and P. Sinay, Ed.) pp 863-914, Wiley-VCH, New York.
15. Dam, T. K., and Brewer, F. C. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry, Chem. Rev. 102, 387-429.
16. Wright, E., and Serpersu, E. H. (2006) Molecular Determinants of Affinity for Aminoglycoside Binding to the Aminoglycoside Nucleotidyltransferase(2″)-Ia, Biochemistry 45, 10243-10250.
17. Wright, E., and Serpersu, E. H. (2005) Enzyme-Substrate Interactions with an Antibiotic Resistance Enzyme: Aminoglycoside Nucleotidyltransferase(2″ )-Ia Characterized by Kinetic and Thermodynamic Methods, Biochemistry 44, 11581-11591.
18. 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.
19. Kaul, M., Barbieri, C. M., Srinivasan, A. R., and Pilch, D. S. (2007) Molecular Determinants of Antibiotic Recognition and Resistance by Aminoglycoside Phosphotransferase (3′)-IIIa: A Calorimetric and Mutational Analysis, J. Mol. Biol. 369, 142-156.
20. Burk, D. L., Hon, W. C., Leung, A. K. -W., and Berghuis, A. M. (2001) Structural analyses of nucleotide binding to an aminoglycoside phosphotransferase, Biochemistry 40, 8756-8764.
21. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure Absorption Gradient Enhanced Heteronuclear Single Quantum Correlation Spectroscopy with Improved Sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
22. Pervushin, K., Riek, R., Wider, G., and Wuthrich, K. (1997) Attenuated T-2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution, Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371.
23. States, D. J., Haberkorn, R. A., and Ruben, D. J. (1982) A Two-Dimensional Nuclear Overhauser Experiment with Pure Absorption Phase in 4 Quadrants, J. Magn. Reson. 48, 286-292.
24. Johnson, B. A., and Blevins, R. A. (1994) Nmr View - a Computer-Program for the Visualization and Analysis of Nmr Data, J. Biomol. NMR 4, 603-614.
25. Chervenak, M. C., and Toone, E. J. (1995) Calorimetric Analysis of the Binding of Lectins with Overlapping Carbohydrate-Binding Ligand Specificities, Biochemistry 34, 7966-7966.
26. Bundi, A., and Wuthrich, K. (1979) Use of Amide H-1-Nmr Titration Shifts for Studies of Polypeptide Conformation, Biopolymers 18, 299-311.
27. Welch, K. T., Virga, K. G., Whittemore, N. A., Ozen, C., Wright, E., Brown, C. L., Lee, R. E., and Serpersu, E. H. (2005) Discovery of non-carbohydrate inhibitors of aminoglycoside-modifying enzymes, Bioorg. Med. Chem. 13, 6252-6263.
28. Dam, T. K., Oscarson, S., Sacchettini, J. C., and Brewer, C. F. (1998) Differential solvation of "core" trimannoside complexes of the Dioclea grandiflora lectin and concanavalin A detected by primary solvent isotope effects in isothermal titration microcalorimetry, J. Biol. Chem. 273, 32826-32832.
29. 2O represents differential interactions with solute and solvent, J. Am. Chem. Soc. 116, 10533-10539.
30. Dashnau, J. L., Sharp, K. A., and Vanderkooi, J. M. (2005) Carbohydrate intramolecular hydrogen bonding cooperativity and its effect on water structure, J. Phys. Chem. B 109, 24152-24159.
31. Isbister, B. D., Phaedria, M. S. H., and Toone, E. J. (1995) Spatial organization versus total surface area as a predictor of protein hydrophobicity of the concanavalin A binding site, J. Am. Chem. Soc. 117, 12877-12878.
32. Freyer, M. W., Buscaglia, R., Hollingsworth, A., Ramos, J., Blynn, M., Pratt, R., Wilson, W. D., and Lewis, E. A. (2007) Break in the heat capacity change at 303 K for complex binding of netropsin to AATT containing hairpin DNA constructs, Biophys. J. 92, 2516-2522.
33. Dunitz, J. D. (1995) Win Some, Lose Some - Enthalpy-Entropy Compensation in Weak Intermolecular Interactions, Chem. Biol. 2, 709-712.
34. Cooper, A., Johnson, C. M., Lakey, J. H., and Nollmann, M. (2001) heat does not come in different colors: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and multiple causes of heat capacity effects in biomolecular interactions, Biophys. Chem. 93, 215-230.
35. Daranas, A. H., Shimizu, H., and Homans, S. W. (2004) Thermodynamics of binding of D-galactose and deoxy derivatives thereof to the L- arabinose-binding protein, J. Am Chem. Soc. 126, 11870-11876.
36. Guinto, E. R., and DiCera, E. (1996) Large heat capacity change in a protein-monovalent cation interaction, Biochemistry 35, 8800-8804.
37. 2O, Biochemistry 32, 5583-5590.
38. Petri, V., Hsieh, M., and Brenowitz, M. (1995) Thermodynamic and Kinetic Characterization of the Binding of the Tata-Binding Protein to the Adenovirus E4 Promoter, Biochemistry 34, 9977-9984.
39. Datta, K., Wowor, A. J., Richard, A. J., and LiCata, V. J. (2006) Temperature dependence and thermodynamics of Klenow polymerase binding to primed-template DNA, Biophys. J. 90, 1739-1751.
40. Izutani, Y., Kanaori, K., Imoto, T., and Oda, M. (2005) Interaction of gymnemic acid with cyclodextrins analyzed by isothermal titration calorimetry, NMR and dynamic light scattering, FEBS J. 272, 6154-6160.
41. Berger, C., Jelesarov, I., and Bosshard, H. R. (1996) Coupled folding and site-specific binding of the GCN4-bZIP transcription factor to the AP-1 and ATF/CREB DNA sites studied by microcalorimetry, Biochemistry 35, 14984-14991.
42. Ladbury, J. E., Wright, J. G., Sturtevant, J. M., and Sigler, P. B. (1994) A Thermodynamic Study of the Tip Repressor-Operator Interaction, J. Mol. Biol. 238, 669-681.
43. Sigurskjold, B. W., and Bundle, D. R. (1992) Thermodynamics of Oligosaccharide Binding to a Monoclonal-Antibody Specific for a Salmonella O-Antigen Point to Hydrophobic Interactions in the Binding-Site, J. Biol. Chem. 267, 8371-8376.
44. Kozlov, A. G., and Lohman, T. M. (2000) Large contributions of coupled protonation equilibria to the observed enthalpy and neat capacity changes for ssDNA binding to Escherichia coli SSB protein, Proteins, 8-22.
45. Eftink, M. R., Anusiem, A. C., and Biltonen, R. L. (1983) Enthalpy Entropy Compensation and Heat-Capacity Changes for Protein Ligand Interactions. General Thermodynamic Models and Data for the Binding of Nucleotides to Ribonuclease-A, Biochemistry 22, 3884-3896.
46. Hubbard, S. J., and Thornton, J. M. (1993) 'NACCESS' Computer Program, Department of Biochemistry and Molecular Biology, University College, London.
47. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant M-Values and Heat-Capacity Changes - Relation to Changes in Accessible Surface-Areas of Protein Unfolding, Protein Sci. 4, 2138-2148.
48. Spolar, R. S., Livingstone, J. R., and Record, M. T. (1992) Use of Liquid-Hydrocarbon and Amide Transfer Data to Estimate Contributions to Thermodynamic Functions of Protein Folding from the Removal of Nonpolar and Polar Surface from Water, Biochemistry 31, 3947-3955.
49. Murphy, K. P., Bhakuni, V., Xie, D., and Freire, E. (1992) Molecular-Basis of Cooperativity in Protein Folding. 3. Structural Identification of Cooperative Folding Units and Folding Intermediates, J. Mol. Biol. 227, 293-306.
50. Sturtevant, J. M. (1977) Heat-Capacity and Entropy Changes in Processes Involving Proteins, Proc. Natl. Acad. Sci. U.S.A. 74, 2236-2240.
51. 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, Carbohyd. Lett. 3, 17-24.
52. 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.