Enhanced stability of monomer fold correlates with extreme drug resistance of hiv-1 protease

Biochemistry

Volumn 52, Issue 43, 2013, Pages 7678-7688

  Louis, John M ^a   Tözsér, József ^b   Roche, Julien ^a   Matúz, Krisztina ^b   Aniana, Annie ^a   Sayer, Jane M ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; CONFORMATIONAL STABILITIES; DRUG RESISTANCE; ENHANCED STABILITY; HIV-1 PROTEASE; MONOMER UNITS; PROTEASE INHIBITOR; VIRAL MATURATION;

BINDING ENERGY; DIMERS; DISEASES; MONOMERS; VIRUSES;

STABILIZATION;

DARUNAVIR; GAG PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ARTICLE; BINDING AFFINITY; COVALENT BOND; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME SUBSTRATE; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VIVO STUDY; KINETICS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SEQUENCE ANALYSIS; THERMOSTABILITY; VIRUS MUTATION;

AMINO ACID SUBSTITUTION; DIMERIZATION; DRUG RESISTANCE, VIRAL; ENZYME PRECURSORS; FUSION PROTEINS, GAG-POL; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; KINETICS; MODELS, BIOLOGICAL; MUTANT PROTEINS; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; SULFONAMIDES; TRANSITION TEMPERATURE;

EID: 84887053357     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400962r     Document Type: Article

References (42)

1. Oroszlan, S. and Luftig, R. B. (1990) Retroviral proteinases Curr. Top. Microbiol. Immunol. 157, 153-185
2. Lee, S. K., Potempa, M., and Swanstrom, R. (2012) The choreography of HIV-1 proteolytic processing and virion assembly J. Biol. Chem. 287, 40867-40874
3. Louis, J. M., Weber, I. T., Tozser, J., Clore, G. M., and Gronenborn, A. M. (2000) HIV-1 protease: maturation, enzyme specificity, and drug resistance Adv. Pharmacol. (San Diego, CA, U. S.) 49, 111-146
4. Louis, J. M., Ishima, R., Torchia, D. A., and Weber, I. T. (2007) HIV-1 Protease: Structure, Dynamics, and Inhibition Adv. Pharmacol. (San Diego, CA, U. S.) 55, 261-298
5. Pearl, L. H. and Taylor, W. R. (1987) A structural model for the retroviral proteases Nature 329, 351-354
6. Wlodawer, A. and Erickson, J. (1993) Structure-based inhibitors of HIV-1 protease Annu. Rev. Biochem. 62, 543-585
7. Johnson, V. A., Calvez, V., Gunthard, H. F., Paredes, R., Pillay, D., Shafer, R. W., Wensing, A. M., and Richman, D. D. (2013) Update of the drug resistance mutations in HIV-1: March 2013 Top. Antivir. Med. 21, 6-14
8. Agniswamy, J. and Weber, I. T. (2009) HIV-1 Protease: Structural perspectives on drug resistance Viruses 1, 1110-1136
9. Louis, J. M., Aniana, A., Weber, I. T., and Sayer, J. M. (2011) Inhibition of autoprocessing of natural variants and multidrug resistant mutant precursors of HIV-1 protease by clinical inhibitors Proc. Natl. Acad. Sci. U. S. A. 108, 9072-9077
10. Pieniazek, D., Rayfield, M., Hu, D. J., Nkengasong, J., Wiktor, S. Z., Downing, R., Biryahwaho, B., Mastro, T., Tanuri, A., Soriano, V., Lal, R., and Dondero, T. (2000) Protease sequences from HIV-1 group M subtypes A-H reveal distinct amino acid mutation patterns associated with protease resistance in protease inhibitor-naive individuals worldwide. HIV Variant Working Group AIDS 14, 1489-1495
11. 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
12. Martin, P., Vickrey, J. F., Proteasa, G., Jimenez, Y. L., Wawrzak, Z., Winters, M. A., Merigan, T. C., and Kovari, L. C. (2005) ″Wide-open″ 1.3 A structure of a multidrug-resistant HIV-1 protease as a drug target Structure 13, 1887-1895
13. Agniswamy, J., Shen, C. H., Aniana, A., Louis, J. M., Sayer, J. M., and Weber, I. T. (2012) HIV-1 protease with 20 mutations exhibits extreme resistance to clinical inhibitors through coordinated structural rearrangements Biochemistry. 51, 2819-2828
14. Nijhuis, M., Schuurman, R., de Jong, J. D., Erickson, J., Gustchina, E., Albert, J., Schipper, P., Gulnik, S., and Boucher, C. A. (1999) Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy AIDS 13, 2349-2359
15. Quiñones-Mateu, M. E., Weber, J., Rangel, H. R., and Chakraborty, B. (2001) HIV-1 Fitness and Antiviral Drug Resistance AIDS Rev 3, 223-234
16. van Maarseveen, N. M., de Jong, J. D., Boucher, C. A., and Nijhuis, M. (2006) An increase in viral replicative capacity drives the evolution of protease inhibitor-resistant human immunodeficiency virus type 1 in the absence of drugs J. Acquired Immune Defic. Syndr. 42, 162-168
17. Chang, M. W. and Torbett, B. E. (2011) Accessory mutations maintain stability in drug-resistant HIV-1 protease J. Mol. Biol. 410, 756-760
18. Yanchunas, J., Jr., Langley, D. R., Tao, L., Rose, R. E., Friborg, J., Colonno, R. J., and Doyle, M. L. (2005) Molecular basis for increased susceptibility of isolates with atazanavir resistance-conferring substitution I50L to other protease inhibitors Antimicrob. Agents Chemother. 49, 3825-3832
19. Dierynck, I., De Wit, M., Gustin, E., Keuleers, I., Vandersmissen, J., Hallenberger, S., and Hertogs, K. (2007) Binding kinetics of darunavir to human immunodeficiency virus type 1 protease explain the potent antiviral activity and high genetic barrier J. Virol. 81, 13845-13851
20. Louis, J. M., Clore, G. M., and Gronenborn, A. M. (1999) Autoprocessing of HIV-1 protease is tightly coupled to protein folding Nat. Struct. Biol. 6, 868-875
21. Sayer, J. M., Liu, F., Ishima, R., Weber, I. T., and Louis, J. M. (2008) Effect of the active-site D25N mutation on the structure, stability and ligand binding of the mature HIV-1 protease J. Biol. Chem. 283, 13459-13470
22. Louis, J. M., Ishima, R., Nesheiwat, I., Pannell, L. K., Lynch, S. M., Torchia, D. A., and Gronenborn, A. M. (2003) Revisiting monomeric HIV-1 protease. Characterization and redesign for improved properties J. Biol. Chem. 278, 6085-6092
23. Louis, J. M., Ishima, R., Aniana, A., and Sayer, J. M. (2009) Revealing the dimer dissociation and existence of a folded monomer of the mature HIV-2 protease Protein Sci. 18, 2442-2453
24. Sayer, J. M., Agniswamy, J., Weber, I. T., and Louis, J. M. (2010) Autocatalytic maturation, physical/chemical properties, and crystal structure of group N HIV-1 protease: relevance to drug resistance Protein Sci. 19, 2055-2072
25. Ishima, R., Torchia, D. A., and Louis, J. M. (2007) Mutational and structural studies aimed at characterizing the monomer of HIV-1 protease and its precursor J. Biol. Chem. 282, 17190-17199
26. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
27. Goddard, T. D. and Kneller, D. G. (2010) Sparky 3, University of California, San Francisco, San Francisco, CA.
28. Tozser, J., Blaha, I., Copeland, T. D., Wondrak, E. M., and Oroszlan, S. (1991) Comparison of the HIV-1 and HIV-2 proteinases using oligopeptide substrates representing cleavage sites in Gag and Gag-Pol polyproteins FEBS Lett. 281, 77-80
29. Mildner, A. M., Rothrock, D. J., Leone, J. W., Bannow, C. A., Lull, J. M., Reardon, I. M., Sarcich, J. L., Howe, W. J., Tomich, C. S., and Smith, C. W. (1994) The HIV-1 protease as enzyme and substrate: mutagenesis of autolysis sites and generation of a stable mutant with retained kinetic properties Biochemistry 33, 9405-9413
30. Tie, Y., Boross, P. I., Wang, Y. F., Gaddis, L., Hussain, A. K., Leshchenko, S., Ghosh, A. K., Louis, J. M., Harrison, R. W., and Weber, I. T. (2004) High resolution crystal structures of HIV-1 protease with a potent non-peptide inhibitor (UIC-94017) active against multi-drug-resistant clinical strains J. Mol. Biol. 338, 341-352
31. Ishima, R., Torchia, D. A., Lynch, S. M., Gronenborn, A. M., and Louis, J. M. (2003) Solution structure of the mature HIV-1 protease monomer: insight into the tertiary fold and stability of a precursor J. Biol. Chem. 278, 43311-43319
32. Szeltner, Z. and Polgar, L. (1996) Conformational stability and catalytic activity of HIV-1 protease are both enhanced at high salt concentration J. Biol. Chem. 271, 5458-5463
33. Chou, K. C., Tomasselli, A. G., Reardon, I. M., and Heinrikson, R. L. (1996) Predicting human immunodeficiency virus protease cleavage sites in proteins by a discriminant function method Proteins 24, 51-72
34. Agniswamy, J., Sayer, J. M., Weber, I. T., and Louis, J. M. (2012) Terminal Interface Conformations Modulate Dimer Stability Prior to Amino Terminal Autoprocessing of HIV-1 Protease Biochemistry 51, 1041-1050
35. Adamson, C. S. and Freed, E. O. (2007) Human immunodeficiency virus type 1 assembly, release, and maturation Adv. Pharmacol. 55, 347-387
36. Dam, E., Quercia, R., Glass, B., Descamps, D., Launay, O., Duval, X., Krausslich, H. G., Hance, A. J., and Clavel, F. (2009) Gag mutations strongly contribute to HIV-1 resistance to protease inhibitors in highly drug-experienced patients besides compensating for fitness loss PLoS. Pathog. 5, e1000345
37. Kozisek, M., Henke, S., Saskova, K. G., Jacobs, G. B., Schuch, A., Buchholz, B., Muller, V., Krausslich, H. G., Rezacova, P., Konvalinka, J., and Bodem, J. (2012) Mutations in HIV-1 gag and pol compensate for the loss of viral fitness caused by a highly mutated protease Antimicrob. Agents Chemother. 56, 4320-4330
38. 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
39. Feher, A., Weber, I. T., Bagossi, P., Boross, P., Mahalingam, B., Louis, J. M., Copeland, T. D., Torshin, I. Y., Harrison, R. W., and Tozser, J. (2002) Effect of sequence polymorphism and drug resistance on two HIV-1 Gag processing sites Eur. J. Biochem. 269, 4114-4120
40. Ishima, R., Ghirlando, R., Tozser, J., Gronenborn, A. M., Torchia, D. A., and Louis, J. M. (2001) Folded monomer of HIV-1 protease J. Biol. Chem. 276, 49110-49116
41. Ceccherini-Silberstein, F., Erba, F., Gago, F., Bertoli, A., Forbici, F., Bellocchi, M. C., Gori, C., D'Arrigo, R., Marcon, L., Balotta, C., Antinori, A., Monforte, A. D., and Perno, C. F. (2004) Identification of the minimal conserved structure of HIV-1 protease in the presence and absence of drug pressure AIDS 18, F11-F19
42. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612