Efavirenz binding site in HIV-1 reverse transcriptase monomers

Biochemistry

Volumn 49, Issue 49, 2010, Pages 10565-10573

  Braz, Valerie A ^a   Barkley, Mary D ^a,b   Jockusch, Rebecca A ^c   Wintrode, Patrick L ^b  

^a Department of Chemistry ^*  (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MECHANISMS; BINDING POCKETS; EFAVIRENZ; ELECTROSPRAYS; FOURIER TRANSFORM ION CYCLOTRON RESONANCE MASS SPECTROMETRY; FT-ICR MS; HETERODIMERS; HIV-1 REVERSE TRANSCRIPTASE; HYDROGEN-DEUTERIUM EXCHANGE; HYDROPHOBIC POCKETS; MASS SPECTRA; MONOMERIC FORMS; NANOELECTROSPRAY IONIZATION; NON-NUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITORS; REFOLDING; REVERSE TRANSCRIPTASES; SOLUTION CONFORMATIONS;

BINDING SITES; CRYSTAL STRUCTURE; DEUTERIUM; ENZYME INHIBITION; FOURIER TRANSFORMS; ION EXCHANGE; MASS SPECTROMETERS; MASS SPECTROMETRY; MONOMERS; PEPTIDES;

CONFORMATIONS;

EFAVIRENZ; PROTEIN P51; PROTEIN P66; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DRUG BINDING SITE; HUMAN IMMUNODEFICIENCY VIRUS 1; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; BENZOXAZINES; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HIV REVERSE TRANSCRIPTASE; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE INHIBITORS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78650160167     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101480z     Document Type: Article

References (51)

1. Wang, J., Smerdon, S. J., Jäger, J., Kohlstaedt, L. A., Rice, P. A., Friedman, J. M., and Steitz, T. A. (1994) Structural basis of asymmetry in the human immunodeficiency virus type 1 reverse transcriptase heterodimer Proc. Natl. Acad. Sci. U.S.A. 91, 7242-7246 (Pubitemid 24226839)
2. Kohlstaedt, L. A., Wang, J., Friedman, J. M., Rice, P. A., and Steitz, T. A. (1992) Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor Science 256, 1783-1790
3. Le Grice, S. F. J., Naas, T., Wohlgensinger, B., and Schatz, O. (1991) Subunit-selective mutagenesis indicates minimal polymerase activity in heterodimer-associated p51 HIV-1 reverse transcriptase EMBO J. 10, 3905-3911
4. Coffin, J. M., Hughes, S. H., and Varmus, H. E. (1997) Retroviruses, Cold Spring Harbor Laboratory Press, Woodbury, NY.
5. Sluis-Cremer, N., Arion, D., Abram, M. E., and Parniak, M. A. (2004) Proteolytic processing of an HIV-1 pol polyprotein precursor: Insights into the mechanism of reverse transcriptase p66/p51 heterodimer formation Int. J. Biochem. Cell Biol. 36, 1836-1847
6. di Marzo Veronese, F., Copeland, T. L., DeVico, A. L., Rahman, R., Oroslan, S., Gallo, R. C., and Sarngadharan, M. G. (1986) Characterization of highly immunogenic p66/p51 as reverse transcriptase of HTLV-III/LAV Science 231, 1289-1291
7. Restle, T., Müller, B., and Goody, R. S. (1990) Dimerization of human immunodeficiency virus type 1 reverse transcriptase J. Biol. Chem. 265, 8986-8988
8. Venezia, C. F., Meany, B. J., Braz, V. A., and Barkley, M. D. (2009) Kinetics of association and dissociation of HIV-1 reverse transcriptase subunits Biochemistry 48, 9084-9093
9. Venezia, C. F., Howard, K. J., Ignatov, M. E., Holladay, L. A., and Barkley, M. D. (2006) Effects of efavirenz binding on the subunit equilibria of HIV-1 reverse transcriptase Biochemistry 45, 2779-2789
10. Tachedjian, G., Moore, K. L., Goff, S. P., and Sluis-Cremer, N. (2005) Efavirenz enhances the proteolytic processing of an HIV-1 pol polyprotein precursor and reverse transcriptase homodimer formation FEBS Lett. 579, 379-384
11. Tachedjian, G., Orlova, M., Sarafianos, S. G., Arnold, E., and Goff, S. P. (2001) Nonnucleoside reverse transcriptase inhibitors are chemical enhancers of dimerization of the HIV type 1 reverse transcriptase Proc. Natl. Acad. Sci. U.S.A. 98, 7188-7193
12. Figueiredo, A., Moore, K. L., Mak, J., Sluis-Cremer, N., de Bethune, M.-P., and Tachedjian, G. (2006) Potent nonnucleoside reverse transcriptase inhibitors target HIV-1 Gag-Pol PLoS Pathog. 2, 1051-1059
13. Ignatov, M. E., Berdis, A. J., Le Grice, S. F. J., and Barkley, M. D. (2005) Attenuation of DNA replication by HIV-1 reverse transcriptase near the central termination sequence Biochemistry 44, 5346-5356
14. Braz, V. A., Holladay, L. A., and Barkley, M. D. (2010) Efavirenz binding to HIV-1 reverse transcriptase monomers and dimers Biochemistry 49, 601-610
15. Weikl, T. R. and von Deuster, C. (2009) Selected-fit versus induced-fit protein binding: Kinetic differences and mutational analysis Proteins: Struct., Funct., Bioinf. 75, 104-110
16. Geitmann, M., Unge, T., and Danielson, U. H. (2006) Biosensor-based kinetic characterization of the interaction between HIV-1 reverse transcriptase and non-nucleoside inhibitors J. Med. Chem. 49, 2367-2374
17. Das, K., Lewi, P. J., Hughes, S. H., and Arnold, E. (2005) Crystallography and the design of anti-AIDS drugs: Conformational flexibility and positional adaptability are important in the design of non-nucleoside HIV-1 reverse transcriptase inhibitors Prog. Biophys. Mol. Biol. 88, 209-231
18. Sluis-Cremer, N., Dmitrienko, G. I., Balzarini, J., Camarasa, M.-J., and Parniak, M. A. (2000) Human immunodeficiency virus type I reverse transcriptase dimer destablilization by 1-{spiro[4″-amino-2″,2″-dioxo- 1″,2″-oxathiole-5″,3′-[2′,5′-bis- O -(tert -butyldimethylsilyl)- b- d -ribofuranosyl]]}-3-ethylthymine Biochemistry 39, 1427-1433
19. Sluis-Cremer, N. and Tachedjian, G. (2008) Mechanisms of inhibition of HIV replication by non-nucleoside reverse transcriptase inhibitors Virus Res. 134, 147-156
20. Spence, R. A., Kati, W. M., Anderson, K. S., and Johnson, K. A. (1995) Mechanism of inhibition of HIV-1 reverse transcriptase by nonnucleoside inhibitors Science 267, 988-993
21. Lindberg, J., Sigurdsson, S., Löwgren, S., Andersson, H. O., Sahlberg, C., Noréen, R., Fridborg, K., Zhang, H., and Unge, T. (2002) Structural basis for the inhibitory efficacy of efavirenz (DMP-266), MSC194 and PNU142721 towards the HIV-1 RT K103N mutant Eur. J. Biochem. 269, 1670-1677
22. Ren, J., Milton, J., Weaver, K. L., Short, S. A., Stuart, D. I., and Stammers, D. K. (2000) Structural basis for the resilience of efavirenz (DMP-266) to drug resistance mutations in HIV-1 reverse transcriptase Structure 8, 1089-1094
23. Sobolev, V., Sorokine, A., Prilusky, J., Abola, E. E., and Edelman, M. (1999) Automated analysis of interatomic contacts in proteins Bioinformatics 15, 327-332
24. Wales, T. E. and Engen, J. R. (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics Mass Spectrom. Rev. 25, 158-170
25. Leavitt, S. and Freire, E. (2001) Direct measurement of protien binding energetics by isothermal titration calorimetry Curr. Opin. Struct. Biol. 11, 560-566
26. Tachedjian, G., Radzio, J., and Sluis-Cremer, N. (2005) Relationship between enzymatic activity and dimeric structure of recombinant HIV-1 reverse transcriptase Proteins: Struct., Funct., Bioinf. 60, 5-13
27. Tsutsui, Y., Liu, L., Gershenson, A., and Wintrode, P. L. (2006) The conformational dynamics of a metastable serpin studied by hydrogen exchange and mass spectrometry Biochemistry 45, 6561-6569
28. Zhang, Z. and Smith, D. L. (1993) Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation Protein Sci. 2, 779-791
29. Zhang, Z. MagTran (the magic transformer). http://www.reocities.com/ SiliconValley/hills/2679/magtran.html.
30. Sobott, F., Hernández, H., McCammon, M. G., Tito, M. A., and Robinson, C. V. (2002) A tandem mass spectrometer of improved transmission and analysis of large macromolecular assemblies Anal. Chem. 74, 1402-1407
31. Braz, V. A. and Howard, K. J. (2009) Separation of protein oligomers by blue native gel electrophoresis Anal. Biochem. 388, 170-172
32. Tachedjian, G., Aronson, H.-E. G., de los Santos, M., Seehra, J., McCoy, J. M., and Goff, S. P. (2003) Role of residues in the tryptophan repeat motif for HIV-1 reverse transcriptase dimerization J. Mol. Biol. 326, 381-396
33. Seckler, J. M., Howard, K. J., Barkley, M. D., and Wintrode, P. L. (2009) Solution structural dynamics of HIV-1 reverse transcriptase heterodimer Biochemistry 48, 7646-7655
34. Weis, D. D., Wales, T. E., Engen, J. R., Hotchko, M., and Ten Eyck, L. F. (2006) Identification and characterization of EX1 kinetics in H/D exchange mass spectrometry by peak width analysis J. Am. Soc. Mass Spectrom. 17, 1498-1509
35. Engen, J. R., Smithgall, T. E., Gmeiner, W. H., and Smith, D. L. (1997) Identification and localization of slow, natural, cooperative unfolding in the hematopoietic cell kinase SH3 domain by amide hydrogen exchange and mass spectrometry Biochemistry 36, 14384-14391
36. Hsiou, Y., Ding, J., Das, K., Clark, A. D., Jr., Hughes, S. H., and Arnold, E. (1996) Structure of unliganded HIV-1 reverse transcriptase at 2.7 Å resolution: Implications of conformational changes for polymerization and inhibition mechanisms Structure 4, 853-857
37. Benesch, J. L. P., Ruotolo, B. T., Simmons, D. A., and Robinson, C. V. (2007) Protein complexes in the gas phase: Technology for structural genomics and proteomics Chem. Rev. 107, 3544-3567
38. Fenn, J. B., Mann, M., Meng, C. K., Wong, S. F., and Whitehouse, C. M. (1989) Electrospray ionization for mass spectrometry of large biomolecules Science 246, 64-71
39. Chowdhury, S. K., Katta, V., and Chait, B. T. (1990) Probing conformational changes in proteins by mass spectrometry J. Am. Chem. Soc. 112, 9012-9013
40. Konermann, L. and Douglas, D. J. (1997) Acid-induced unfolding of cytochrome c at different methanol concentrations: Electrospray ionization mass spectrometry specifically monitors changes in tertiary structure Biochemistry 36, 12296-12302
41. Kaltashov, I. A. and Eyles, S. J. (2005) Mass Spectrometry in Biophysics, John Wiley & Sons, Hoboken, NJ.
42. Chen, M. L. and Cook, K. D. (2007) Oxidation artifacts in the electrospray mass spectrometry of Aβ peptide Anal. Chem. 79, 2031-2036
43. Van Berkel, G. L., Asano, K. G., and Schnier, P. D. (2001) Electrochemical processes in a wire-in-a-capillary bulk-loaded, nano-electrospray emitter J. Am. Soc. Mass Spectrom. 12, 853-862
44. Grobler, J. A., Dornadula, G., Rice, M. R., Simcoe, A. L., Hazuda, D. J., and Miller, M. D. (2007) HIV-1 reverse transcriptase plus-strand initiation exhibits preferential sensitivity to non-nucleoside reverse transcriptase inhibitors in vitro J. Biol. Chem. 282, 8005-8010
45. Shen, L., Peterson, S., Sedaghat, A. R., McMahon, M. A., Callender, M., Zhang, H., Zhou, Y., Pitt, E., Anderson, K. S., Acosta, E. P., and Siliciano, R. F. (2008) Dose-response curve slope sets class-specific limits on inhibitory potential of anti-HIV drugs Nat. Med. 14, 762-766
46. Jacobo-Molina, A., Ding, J., Nanni, R. G., Clark, A. D., Jr., Lu, X., Tantillo, C., Williams, R. L., Kamer, G., Ferris, A. L., Clark, P., Hizi, A., Hughes, S. H., and Arnold, E. (1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA Proc. Natl. Acad. Sci. U.S.A. 90, 6320-6324
47. Ren, J. and Stammers, D. K. (2008) Structural basis for drug resistance mechanisms for non-nucleoside inhibitors of HIV reverse transcriptase Virus Res. 134, 157-170
48. Seckler, J. M., Barkley, M. D., and Wintrode, P. L. (2010) Allosteric suppression of HIV-1 reverse transcriptase structural dynamics upon inhibitor binding Biophys. J. (in press)
49. Bavand, M. R., Wagner, R., and Richmond, T. J. (1993) HIV-1 reverse transcriptase: Polymerization properties of the p51 homodimer compared to the p66/p51 heterodimer Biochemistry 32, 10543-10552
50. Zheng, X., Mueller, G. A., Cuneo, M. J., DeRose, E. F., and London, R. E. (2010) Homodimerization of the p51 subunit of HIV-1 reverse transcriptase Biochemistry 49, 2821-2833
51. 13C]methionine HIV-1 reverse transcriptase by NMR spectroscopy Antiviral Res. 84, 205-214