Suppression of HIV-1 Protease Inhibitor Resistance by Phosphonate-mediated Solvent Anchoring

Journal of Molecular Biology

Volumn 363, Issue 3, 2006, Pages 635-647

  Cihlar, Tomas ^a   He, Gong Xin ^a   Liu, Xiaohong ^a   Chen, James M ^a   Hatada, Marcos ^a   Swaminathan, Swami ^a   McDermott, Martin J ^a   Yang, Zheng Yu ^a   Mulato, Andrew S ^a   Chen, Xiaowu ^a   Leavitt, Stephanie A ^a   Stray, Kirsten M ^a   Lee, William A ^a  

^a GILEAD SCIENCES   (United States)

Author keywords

HIV 1; phosphonate mediated; protease inhibitors; solvent anchoring

Indexed keywords

AMPRENAVIR; ATAZANAVIR; GS 16571; GS 8373; GS 8374; INDINAVIR; LOPINAVIR; NELFINAVIR; PHOSPHONIC ACID DERIVATIVE; PROTEINASE INHIBITOR; RITONAVIR; SAQUINAVIR; SOLVENT; TMC 126; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; COVALENT BOND; CROSS RESISTANCE; CRYSTALLOGRAPHY; DRUG DESIGN; DRUG POTENCY; ENTROPY; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN INTERACTION; THERMODYNAMICS; VIRUS STRAIN;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33749240210     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.073     Document Type: Article

References (49)

1. Palella Jr. F.J., Delaney K.M., Moorman A.C., Loveless M.O., Fuhrer J., Satten G.A., et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. New Engl. J. Med. 338 (1998) 853-860
2. Detels R., Munoz A., McFarlane G., Kingsley L.A., Margolick J.B., Giorgi J., et al. Effectiveness of potent antiretroviral therapy on time to AIDS and death in men with known HIV infection duration. Multicenter AIDS Cohort Study Investigators. JAMA 280 (1998) 1497-1503
3. Richman D.D., Morton S.C., Wrin T., Hellmann N., Berry S., Shapiro M.F., and Bozzette S.A. The prevalence of antiretroviral drug resistance in the United States. AIDS 18 (2004) 1393-1401
4. Tamalet C., Fantini J., Tourres C., and Yahi N. Resistance of HIV-1 to multiple antiretroviral drugs in France: a 6-year survey (1997-2002) based on an analysis of over 7000 genotypes. AIDS 17 (2003) 2383-2388
5. Wensing A.M., and Boucher C.A. Worldwide transmission of drug-resistant HIV. AIDS Rev. 5 (2003) 140-155
6. Navia M.A., Fitzgerald P.M., McKeever B.M., Leu C.T., Heimbach J.C., Herber W.K., et al. Three-dimensional structure of aspartyl protease from human immunodeficiency virus HIV-1. Nature 337 (1989) 615-620
7. Wu T.D., Schiffer C.A., Gonzales M.J., Taylor J., Kantor R., Chou S., et al. Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J. Virol. 77 (2003) 4836-4847
8. Mendoza C., and Soriano V. Resistance to HIV protease inhibitors: mechanisms and clinical consequences. Curr. Drug Metab. 5 (2004) 321-328
9. Yusa K., and Harada S. Acquisition of multi-PI (protease inhibitor) resistance in HIV-1 in vivo and in vitro. Curr. Pharm. Des. 10 (2004) 4055-4064
10. Moyle G.J., and Back D. Principles and practice of HIV-protease inhibitor pharmacoenhancement. HIV Med. 2 (2001) 105-113
11. Zeldin R.K., and Petruschke R.A. Pharmacological and therapeutic properties of ritonavir-boosted protease inhibitor therapy in HIV-infected patients. J. Antimicrob. Chemother. 53 (2004) 4-9
12. Carr. Toxicity of antiretroviral therapy and implications for drug development. Nature Rev. Drug Discov. 2 (2003) 624-634
13. Nolan D. Metabolic complications associated with HIV protease inhibitor therapy. Drugs 63 (2003) 2555-2574
14. Ghosh A.K., Pretzer E., Cho H., Hussain K.A., and Duzgunes N. Antiviral activity of UIC-PI, a novel inhibitor of the human immunodeficiency virus type 1 protease. Antiviral Res. 54 (2002) 29-36
15. Yoshimura K., Kato R., Kavlick M.F., Nguyen A., Maroun V., Maeda K., et al. A potent human immunodeficiency virus type 1 protease inhibitor, UIC-94003 (TMC-126), and selection of a novel (A28S) mutation in the protease active site. J. Virol. 76 (2002) 1349-1358
16. Kim E.E., Baker C.T., Dwyer M.D., Murcko M.A., Tung R.D., and Navia M.A. Crystal structure of HIV-1 protease in complex with VX-478, a potent and orally bioavailable inhibitor of the enzyme. J. Am. Chem. Soc. 117 (1995) 1181-1182
17. Lee W.A., He G.X., Eisenberg E., Cihlar T., Swaminathan S., Mulato A., and Cundy K.C. Selective intracellular activation of a novel prodrug of the human immunodeficiency virus reverse transcriptase inhibitor tenofovir leads to preferential distribution and accumulation in lymphatic tissue. Antimicrob. Agents Chemother. 49 (2005) 1898-1906
18. Eisenberg E.J., He G.X., and Lee W.A. Metabolism of GS-7340, a novel phenyl monophosphoramidate intracellular prodrug of PMPA, in blood. Nucleosides Nucleotides Nucl. Acids 20 (2001) 1091-1098
19. Maguire M., Shortino D., Klein A., Harris W., Manohitharajah V., and Tisdale M. Emergence of resistance to protease inhibitor amprenavir in human immunodeficiency virus type 1-infected patients: selection of four alternative viral protease genotypes and influence of viral susceptibility to coadministered reverse transcriptase nucleoside inhibitors. Antimicrob. Agents Chemother. 46 (2002) 731-738
20. Ait-Khaled M., Rakik A., Griffin P., Stone C., Richards N., Thomas D., et al., CNA2007 International Study Team. HIV-1 reverse transcriptase and protease resistance mutations selected during 16-72 weeks of therapy in isolates from antiretroviral therapy-experienced patients receiving abacavir/efavirenz/amprenavir in the CNA2007 study. Antivir. Ther. 8 (2003) 111-120
21. Carrillo A., Stewart K.D., Sham H.L., Norbeck D.W., Kohlbrenner W.E., Leonard J.M., et al. In vitro selection and characterization of human immunodeficiency virus type 1 variants with increased resistance to ABT-378, a novel protease inhibitor. J. Virol. 72 (1998) 7532-7541
22. Kempf D.J., Isaacson J.D., King M.S., Brun S.C., Xu Y., Real K., et al. Identification of genotypic changes in human immunodeficiency virus protease that correlate with reduced susceptibility to the protease inhibitor lopinavir among viral isolates from protease inhibitor-experienced patients. J. Virol. 75 (2001) 7462-7469
23. Shafer R.W. Genotypic testing for human immunodeficiency virus type 1 drug resistance. Clin. Microbiol. Rev. 15 (2002) 247-277
24. Ziermann R., Limoli K., Das K., Arnold E., Petropoulos C.J., and Parkin N.T. A mutation in human immunodeficiency virus type 1 protease, N88S, that causes in vitro hypersensitivity to amprenavir. J. Virol. 74 (2000) 4414-4419
25. Ohtaka H., Velazquez-Campoy A., Xie D., and Freire E. Overcoming drug resistance in HIV-1 chemotherapy: the binding thermodynamics of Amprenavir and TMC-126 to wild-type and drug-resistant mutants of the HIV-1 protease. Protein Sci. 11 (2002) 1908-1916
26. Baker B.M., and Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. J. Biophys. 71 (1996) 2049-2055
27. Eftink M.R., Anusiem A.C., and Biltonen R.L. 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 (1983) 3884-3896
28. Havlir D.V., and O'Marro S.D. Atazanavir: new option for treatment of HIV infection. Clin. Infect. Dis. 38 (2004) 1599-1604
29. Pazhanisamy S., Partaledis J.A., Rao B.G., and Livingston D.J. In vitro selection and characterization of VX-478 resistant HIV-1 variants. Advan. Exp. Med. Biol. 436 (1998) 75-83
30. Vega S., Kang L.W., Velazquez-Campoy A., Kiso Y., Amzel L.M., and Freire E.A. Structural and thermodynamic escape mechanism from a drug resistant mutation of the HIV-1 protease. Proteins: Struct. Funct. Genet. 55 (2004) 594-602
31. Yoshimura K., Kato R., Yusa K., Kavlick M.F., Maroun V., Nguyen A., et al. JE-2147: a dipeptide protease inhibitor (PI) that potently inhibits multi-PI-resistant HIV-1. Proc. Natl Acad. Sci. USA 96 (1999) 8675-8680
32. Reiling K.K., Endres N.F., Dauber D.S., Craik C.S., and Stroud R.M. Anisotropic dynamics of the JE-2147-HIV protease complex: drug resistance and thermodynamic binding mode examined in a 1.09 A structure. Biochemistry 41 (2002) 4582-4594
33. Wainberg M.A. HIV resistance to nevirapine and other non-nucleoside reverse transcriptase inhibitors. J. Acquir. Immune Defic. Syndr. 34 Suppl. 1 (2003) S2-S7
34. Charles C.H., Yelmene M., and Luo G.X. Recent advances in rhinovirus therapeutics. Curr. Drug Targets Infect. Disord. 4 (2004) 331-337
35. Pawlotsky J.M. Hepatitis C virus genetic variability: pathogenic and clinical implications. Clin. Liver Dis. 7 (2003) 45-66
36. Partaledis J.A., Yamaguchi K., Tisdale M., Blair E.E., Falcione C., Maschera B., et al. In vitro selection and characterization of human immunodeficiency virus type 1 (HIV-1) isolates with reduced sensitivity to hydroxyethylamino sulfonamide inhibitors of HIV-1 aspartyl protease. J. Virol. 69 (1995) 5228-5235
37. Weislow O.S., Kiser R., Fine D.L., Bader J., Shoemaker R.H., and Boyd M.R. New soluble-formazan assay for HIV-1 cytopathic effects: application to high-flux screening of synthetic and natural products for AIDS-antiviral activity. J. Natl Cancer Inst. 81 (1989) 77-86
38. Hostomsky Z., Appelt K., and Ogden R.C. High-level expression of self-processed HIV-1 protease in Escherichia coli using a synthetic gene. Biochem. Biophys. Res. Commun. 161 (1989) 1056-1063
39. Ido E., Han H.P., Kezdy F.J., and Tang J. Kinetic studies of human immunodeficiency virus type 1 protease and its active-site hydrogen bond mutant A28S. J. Biol. Chem. 266 (1991) 24359-24366
40. Hong L., Treharne A., Hartsuck J.A., Foundling S., and Tang J. Crystal structures of complexes of a peptidic inhibitor with wild-type and two mutant HIV-1 proteases. Biochemistry 35 (1996) 10627-10633
41. Toth M.V., and Marshall G.R. A simple, continuous fluorometric assay for HIV protease. Int. J. Pept. Protein Res. 36 (1990) 544-550
42. Knight C.G. Active-site titration of peptidases. Methods Enzymol. 248 (1995) 85-101
43. Bieth J.G. Theoretical and practical aspects of proteinase inhibition kinetics. Methods Enzymol. 248 (1995) 59-84
44. Sigurskjold B.W. Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 277 (2000) 260-266
45. Velazquez-Campoy A., Kiso Y., and Freire E. The binding energetics of first- and second-generation HIV-1 protease inhibitors: implications for drug design. Arch. Biochem. Biophys. 390 (2001) 169-175
46. Velazquez-Campoy A., Luque I., Todd M.J., Milutinovich M., Kiso Y., and Freire E. Thermodynamic dissection of the binding energetics of KNI-272, a potent HIV-1 protease inhibitor. Protein Sci. 9 (2000) 1801-1809
47. Todd M.J., Luque I., Velazquez-Campoy A., and Freire E. Thermodynamic basis of resistance to HIV-1 protease inhibition: calorimetric analysis of the V82F/I84V active site resistant mutant. Biochemistry 39 (2000) 11876-11883
48. Pflugrath J.W. The finer things in X-ray diffraction data collection. Acta Crystallog. sect. D 55 (1999) 1718-1725
49. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., and Jiang J.S. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921