Extreme entropy-enthalpy compensation in a drug-resistant variant of HIV-1 protease

ACS Chemical Biology

Volumn 7, Issue 9, 2012, Pages 1536-1546

  King, Nancy M ^a   Prabu Jeyabalan, Moses ^a,c   Bandaranayake, Rajintha M ^a,d   Nalam, Madhavi N L ^a   Nalivaika, Ellen A ^a   Özen, Ayşegül ^a   Haliloǧlu, Türkan ^b   Yilmaz, Neşe Kurt ^a   Schiffer, Celia A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOGAZICI UNIVERSITY   (Turkey)

^c Janet Weis Children s Hospital   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPRENAVIR; ATAZANAVIR; DARUNAVIR; ENZYME VARIANT; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; INDINAVIR; NELFINAVIR; SAQUINAVIR;

ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; ENTHALPY; ENTROPY; ENZYME ACTIVE SITE; ENZYME BINDING; HYDROGEN BOND; MUTATION; NONHUMAN; PRIORITY JOURNAL; THERMODYNAMICS; WILD TYPE;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, VIRAL; ENTROPY; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; THERMODYNAMICS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84868151351     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300191k     Document Type: Article

References (53)

1. Chaires, J. B. (2008) Calorimetry and thermodynamics in drug design, Iin Annual Review of Biophysics, pp 135-151, Annual Reviews, Palo Alto.
2. Wlodawer, A., and Erickson, J. W. (1993) Structure-based inhibitors of HIV-1 protease. Annu. Rev. Biochem. 62, 543-585. (Pubitemid 23237881)
3. Todd, M. J., Luque, I., Velazquez-Campoy, A., and Freire, E. (2000) Thermodynamic basis of resistance to HIV-1 protease inhibition: calorimetric analysis of the V82F/I84V active site resistant mutant. Biochemistry 39, 11876-11883.
4. Valzaquez-Campoy, A., Luque, I., Todd, M. J., Milutinovich, M., Kiso, Y., and Freire, E. (2000) Thermodynamic dissection of the binding energetics of KNI-272, a potent HIV-1 protease inhibitor. Protein Sci. 9, 1801-1809.
5. Valzaquez-Campoy, A., Todd, M. J., and Freire, E. (2000) HIV-1 protease inhibitors: enthalpic versus entropic optimization of the binding affinity. Biochemistry 39, 2201-2207. (Pubitemid 30130068)
6. King, N. M., Prabu-Jeyabalan, M., Nalivaika, E. A., Wigerinck, P., de Bethune, M.-P., and Schiffer, C. A. (2004) Structural and thermodynamic basis for the binding of TMC114, a next-generation human immunodeficiency virus type-1 protease inhibitor. J. Virol. 78, 12012-12021. (Pubitemid 39390785)
7. Ohtaka, H., Velazquez-Campoy, A., Xie, D., and Freire, E. (2002) Overcoming drug resistance in HIV-1 chemotherapy: the binding thermodynamics of Amprenavir and TMC-126 to wild-type and drugresistant mutants of the HIV-1 protease. Protein Sci. 11, 1908-1916. (Pubitemid 34791410)
8. Surleraux, D. L., de Kock, H. A., Verschueren, W. G., Pille, G. M., Maes, L. J., Peeters, A., Vendeville, S., De Meyer, S., Azijn, H., Pauwels, R., de Bethune, M. P., King, N. M., Prabu-Jeyabalan, M., Schiffer, C. A., and Wigerinck, P. B. (2005) Design of HIV-1 protease inhibitors active on multidrug-resistant virus. J. Med. Chem. 48, 1965-1973. (Pubitemid 40403065)
9. Muzammil, S., Armstrong, A. A., Kang, L. W., Jakalian, A., Bonneau, P. R., Schmelmer, V., Amzel, L. M., and Freire, E. (2007) Unique thermodynamic response of tipranavir to human immunodeficiency virus type 1 protease drug resistance mutations. J. Virol. 81, 5144-5154. (Pubitemid 46744425)
10. Fernandez, A., Fraser, C., and Scott, L. R. (2012) Purposely engineered drug-target mismatches for entropy-based drug optimization. Trends Biotechnol. 30, 1-7.
11. Kuroki, R., Nitta, K., and Yutani, K. (1992) Thermodynamic changes in the binding of Ca2+ to a mutant human lysozyme (D86/92). Enthalpy-entropy compensation observed upon Ca2+ binding to proteins. J. Biol. Chem. 267, 24297-24301.
12. Blasie, C. A., and Berg, J. M. (2004) Entropy-enthalpy compensation in ionic interactions probed in a zinc finger peptide. Biochemistry 43, 10600-10604. (Pubitemid 39079330)
13. Krueger, S., Gregurick, S., Shi, Y., Wang, S., Wladkowski, B. D., and Schwarz, F. P. (2003) Entropic nature of the interaction between promoter bound CRP mutants and RNA polymerase. Biochemistry 42, 1958-1968. (Pubitemid 36258668)
14. Davidson, J. P., Lubman, O., Rose, T., Waksman, G., and Martin, S. F. (2002) Calorimetric and structural studies of 1,2,3- trisubstituted cyclopropanes as conformationally constrained peptide inhibitors of Src SH2 domain binding. J. Am. Chem. Soc. 124, 205-215. (Pubitemid 34062753)
15. Houk, K. N., Leach, A. G., Kim, S. P, and Zhang, X. (2003) Binding affinities of host-guest, protein-ligand, and protein-transitionstate complexes. Angew. Chem., Int. Ed. 42, 4872-4897. (Pubitemid 37345385)
16. Rekharsky, M. V., and Inoue, Y. (1998) Complexation thermodynamics of cyclodextrins. Chem. Rev. 98, 1875-1918.
17. Sharp, K. (2001) Entropy-enthalpy compensation: Fact or artifact? Protein Sci. 10, 661-667. (Pubitemid 32221155)
18. Olsen, D. B., Stahlhut, M. W., Rutkowski, C. A., Schock, H. B., vanOlden, A. L., and Kuo, L. C. (1999) Non-active site changes elicit broad-based cross-resistance of the HIV-1 protease to inhibitors. J. Biol. Chem. 274, 23699-23701.
19. Ohtaka, H., Schon, A., and Freire, E. (2003) Multidrug resistance to HIV-1 protease inhibition requires cooperative coupling between distal mutations. Biochemistry 42, 13659-13666. (Pubitemid 37444916)
20. King, N. M., Melnick, L., Prabu-Jeyabalan, M., Nalivaika, E. A., Yang, S.-S., Gao, Y., Nie, X., Zepp, C., Heefner, D. L., and Schiffer, C. A. (2002) Lack of synergy for inhibitors targeting a multi-drugresistant HIV-1 protease. Protein Sci. 11, 418-429. (Pubitemid 34075805)
21. King, N. M., Prabu-Jeyabalan, M., Nalivaika, E., and Schiffer, C. A. (2004) Combating susceptibility to drug resistance: Lessons from HIV-1 protease. Chem. Biol. 11, 1333-1338. (Pubitemid 39351371)
22. Lafont, V., Armstrong, A. A., Ohtaka, H., Kiso, Y., Mario Amzel, L., and Freire, E. (2007) Compensating enthalpic and entropic changes hinder binding affinity optimization. Chem. Biol. Drug Des. 69, 413-422. (Pubitemid 46955533)
23. Ohtaka, H., Muzammil, S., Schön, A., Velazquez-Campoy, A., Vega, S., and Freire, E. (2004) Thermodynamic rules for the design of high affinity HIV-1 protease inhibitors with adaptability to mutations and high selectivity towards unwanted targets. Int. J. Biochem. Cell Biol. 36, 1787-1799. (Pubitemid 38748533)
24. Steuber, H., Heine, A., and Klebe, G. (2007) Structural and thermodynamic study on aldose reductase: nitro-substituted inhibitors with strong enthalpic binding contribution. J. Mol. Biol. 368, 618-638. (Pubitemid 46527606)
25. Bottcher, J., Blum, A., Heine, A., Diederich, W. E., and Klebe, G. (2008) Structural and kinetic analysis of pyrrolidine-based inhibitors of the drug-resistant Ile84Val mutant of HIV-1 protease. J. Mol. Biol. 383, 347-357.
26. Shafer, R. W., Stevenson, D., and Chan, B. (1999) Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res. 27, 348-352. (Pubitemid 29209482)
27. King, N. M., Prabu-Jeyabalan, M., Nalivaika, E. A., Wigerinck, P., de Bethune, M. P., and Schiffer, C. A. (2004) Structural and thermodynamic basis for the binding of TMC114, a next-generation human immunodeficiency virus type 1 protease inhibitor. J. Virol. 78, 12012-12021. (Pubitemid 39390785)
28. Eftink, M. R., Anusiem, A. C., and Biltonen, R. L. (1983) Enthalpy-entropy compensation and heat capacity changes for proteinligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry 22, 3884-3896.
29. Guan, R., Ho, M. C., Brenowitz, M., Tyler, P. C., Evans, G. B., Almo, S. C., and Schramm, V. L. (2011) Entropy-driven binding of picomolar transition state analogue inhibitors to human 5'- methylthioadenosine phosphorylase. Biochemistry 50, 10408-10417.
30. Prabu-Jeyabalan, M., King, N. M., Nalivaika, E., Heilek-Snyder, G., Cammack, N., and Schiffer, C. A. (2006) Substrate envelope and drug resistance: Crystal structure of RO1 in complex with wild-type human immunodeficiency virus type 1 protease. Antimicrob. Agents Chemother. 50, 1518-1521.
31. Williams, T., and Kelley, C. (1998) GNUPLOT.
32. Freedberg, D. I., Wang, Y. X., Stahl, S. S., Kaufman, J. D., Wingfield, P. T., Kiso, Y., and Torchia, D. A. (1998) Flexibility and function in HIV protease: Dynamics of the HIV-1 protease bound to the asymmetric inhibitor kynostatin 272. J. Am. Chem. Soc. 120, 7916-7923. (Pubitemid 28392075)
33. Jhoti, H., Singh, O. M., Weir, M. P., Cooke, R., Murray-Rust, P., and Wonacott, A. (1994) X-ray crystallographic studies of a series of penicillin-derived asymmetric inhibitors of HIV-1 protease. Biochemistry 33, 8417-8427. (Pubitemid 24242678)
34. Prabu-Jeyabalan, M., Nalivaika, E., and Schiffer, C. A. (2000) How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J. Mol. Biol. 301, 1207-1220.
35. Ohtaka, H., and Freire, E. (2005) Adaptive inhibitors of the HIV-1 protease. Prog. Biophys. Mol. Biol. 88, 193-208. (Pubitemid 39568611)
36. Muzammil, S., Ross, P., and Freire, E. (2003) A major role for a set of non-active site mutations in the development of HIV-1 protease drug resistance. Biochemistry 42, 631-638. (Pubitemid 36133287)
37. Stoica, I., Sadiq, S. K., and Coveney, P. V. (2008) Rapid and accurate prediction of binding free energies for saquinavir-bound HIV- 1 proteases. J. Am. Chem. Soc. 130, 2639-2648. (Pubitemid 351304779)
38. Freedberg, D. I., Ishima, R., Jacob, J., Wang, Y. X., Kustanovich, I., Louis, J. M., and Torchia, D. A. (2002) Rapid structural fluctuations of the free HIV protease flaps in solution: relationship to crystal structures and comparison with predictions of dynamics calculations. Protein Sci. 11, 221-232. (Pubitemid 34075785)
39. Ishima, R., Freedberg, D. I., Wang, Y. X., Louis, J. M., and Torchia, D. A. (1999) Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function. Structure 7, 1047-1055. (Pubitemid 29436502)
40. Scott, W. R. P., and Schiffer, C. A. (2000) Curling of flap tips in HIV-1 protease as a mechanism for substrate entry and tolerance of drug resistance. Structure 8, 1259-1265. (Pubitemid 32149752)
41. Ladbury, J. E., and Chowdhry, B. Z., Eds. (1998) Biocalorimetry. Applications of Calorimetry in the Biological Sciences, John Wiley & Sons Ltd., Chichester.
42. Dunitz, J. D. (1995) Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 2, 709-712.
43. Diehl, C., Engstrom, O., Delaine, T., Hakansson, M., Genheden, S., Modig, K., Leffler, H., Ryde, U., Nilsson, U. J., and Akke, M. (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J. Am. Chem. Soc. 132, 14577-14589.
44. Hamelberg, D., and McCammon, J. A. (2005) Fast peptidyl cistrans isomerization within the flexible Gly-rich flaps of HIV-1 protease. J. Am. Chem. Soc. 127, 13778-13779. (Pubitemid 41437013)
45. Cai, Y., Kurt Yilmaz, N., Myint, W., Ishima, R., and Schiffer, C. (2012) Differential flap dynamics in wild-type and a drug resistant variant of HIV-1 protease revealed by molecular dynamics and NMR relaxation. J. Chem. Theory Comput., DOI: 10.1021/ct300076y.
46. Rose, J. R., Salto, R., and Craik, C. S. (1993) Regulation of autoproteolysis of the HIV-1 and HIV-2 proteases with engineered amino acid substitutions. J. Biol. Chem. 268, 11939-11945. (Pubitemid 23168153)
47. Hui, J. O., A.G., T., Reardon, I. M., Lull, J. M., Brunner, D. P., Tomich, C. C., and Heinrikson, R. L. (1993) Large scale purification and refolding of HIV-1 protease from Escherichia coli inclusion bodies. J. Prot. Chem. 12, 323-327. (Pubitemid 23213752)
48. Prabu-Jeyabalan, M., Nalivaika, E. A., King, N. M., and Schiffer, C. A. (2004) Structural basis for coevolution of a human immunodeficiency virus type 1 nucleocapsid-p1 cleavage site with a V82A drug-resistant mutation in viral protease. J. Virol. 78, 12446-12454. (Pubitemid 39458763)
49. Sigurskjold, B. (2000) Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 277, 260-266. (Pubitemid 30055877)
50. Krohn, A., Redshaw, S., Ritchie, J. C., Graves, B. J., and Hatada, M. H. (1991) Novel binding mode of highly potent HIV-proteinase inhibitors incorporating the (R)-hydroxyethylamine isostere. J. Med. Chem. 34, 3340-3342.
51. Otwinowski, Z. (1993) Oscillation data reduction program, In CCP4 Study Weekend: Data Collection and Processing, 29-30 Jan 1993 (Sawyer, L., Isaacs, N., and Bailey, S., Eds.), pp 56-62, SERC Daresbury Laboratory, England.
52. Minor, W. (1993) XDISPLAYF program, Purdue University, West Lafayette, IN.
53. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure refinement, Acta Crystallogr. Sect. A 47, 392-400.