Allosteric suppression of HIV-1 reverse transcriptase structural dynamics upon inhibitor binding

Biophysical Journal

Volumn 100, Issue 1, 2011, Pages 144-153

  Seckler, James M ^a   Barkley, Mary D ^a,b   Wintrode, Patrick L ^a  

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

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78651233149     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.11.004     Document Type: Article

References (52)

1. Jacobo-Molina, A., J. Ding, ., E. Arnold. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A° resolution shows bent DNA. Proc. Natl. Acad. Sci. USA. 90:6320-6324.
2. Sarafianos, S. G., B. Marchand, ., E. Arnold. 2009. Structure and function of HIV-1 reverse transcriptase: Molecular mechanisms of polymerization and inhibition. J. Mol. Biol. 385:693-713.
3. Sarafianos, S. G., K. Das,., E. Arnold. 2001. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20:1449-1461.
4. Shen, L., S. Peterson, ., R. F. Siliciano. 2008. Dose-response curve slope sets class-specific limits on inhibitory potential of anti-HIV drugs. Nat. Med. 14:762-766.
5. Abbondanzieri, E. A., G. Bokinsky, ., X. Zhuang. 2008. Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature. 453:184-189.
6. Liu, S., E. A. Abbondanzieri, ., X. Zhuang. 2008. Slide into action: Dynamic shuttling of HIV reverse transcriptase on nucleic acid substrates. Science. 322:1092-1097.
7. Figueiredo, A., K. L. Moore, ., G. Tachedjian. 2006. Potent nonnucleoside reverse transcriptase inhibitors target HIV-1 Gag-Pol. PLoS Pathog. 2:e119.
8. Kohlstaedt, L. A., J. Wang, ., T. A. Steitz. 1992. Crystal structure at 3.5 A° resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science. 256:1783-1790.
9. Hsiou, Y., J. Ding,., E. Arnold. 1996. Structure of unliganded HIV-1 reverse transcriptase at 2.7 A° resolution: Implications of conformational changes for polymerization and inhibition mechanisms. Structure. 4:853-860.
10. Rodgers, D. W., S. J. Gamblin, ., S. C. Harrison. 1995. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA. 92:1222-1226.
11. Ren, J., and D. K. Stammers. 2008. Structural basis for drug resistance mechanisms for non-nucleoside inhibitors of HIV reverse transcriptase. Virus Res. 134:157-170.
12. Ivetac, A., and J. A. McCammon. 2009. Elucidating the inhibition mechanism of HIV-1 non-nucleoside reverse transcriptase inhibitors through multicopy molecular dynamics simulations. J. Mol. Biol. 388:644-658.
13. Shen, L., J. Shen, ., H. Jiang. 2003. Steered molecular dynamics simulation on the binding of NNRTI to HIV-1 RT. Biophys. J. 84:3547-3563.
14. Temiz, N. A., and I. Bahar. 2002. Inhibitor binding alters the directions of domain motions in HIV-1 reverse transcriptase. Proteins Struct. Funct. Bioinf. 49:61-70.
15. Zhou, Z., M. Madrid, ., J. D. Madura. 2005. Effect of a bound nonnucleoside RT inhibitor on the dynamics of wild-type and mutant HIV-1 reverse transcriptase. J. Am. Chem. Soc. 127:17253-17260.
16. Braz, V. A., L. A. Holladay, and M. D. Barkley. 2010. Efavirenz binding to HIV-1 reverse transcriptase monomers and dimers. Biochemistry. 49:601-610.
17. Geitmann, M., T. Unge, and U. H. Danielson. 2006. Biosensor-based kinetic characterization of the interaction between HIV-1 reverse transcriptase and non-nucleoside inhibitors. J. Med. Chem. 49:2367-2374.
18. Weikl, T. R., and C. von Deuster. 2009. Selected-fit versus induced-fit protein binding: Kinetic differences and mutational analysis. Proteins Struct. Funct. Bioinf. 75:104-110.
19. Tsai, C.-J., A. del Sol, and R. Nussinov. 2008. Allostery: Absence of a change in shape does not imply that allostery is not at play. J. Mol. Biol. 378:1-11.
20. del Sol, A., C.-J. Tsai, ., R. Nussinov. 2009. The origin of allosteric functional modulation: Multiple pre-existing pathways. Structure. 17:1042-1050.
21. Liu, T., S. T. Whitten, and V. J. Hilser. 2006. Ensemble-based signatures of energy propagation in proteins: A new view of an old phenomenon. Proteins Struct. Funct. Bioinf. 62:728-738.
22. Brier, S., and J. R. Engen. 2008. Hydrogen exchange mass spectrometry: Principles and capabilities. In Mass Spectrometry Analysis for Protein-Protein Interactions and Dynamics. M. Chance, editor. Wiley, Hoboken, NJ. 11-43.
23. Engen, J. R., T. E. Smithgall, ., D. L. Smith. 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.
24. Seckler, J. M., K. J. Howard, ., P. L. Wintrode. 2009. Solution structural dynamics of HIV-1 reverse transcriptase heterodimer. Biochemistry. 48:7646-7655.
25. Venezia, C. F., K. J. Howard, ., M. D. Barkley. 2006. Effects of efavirenz binding on the subunit equilibria of HIV-1 reverse transcriptase. Biochemistry. 45:2779-2789.
26. Tsutsui, Y., L. Liu, ., P. L. Wintrode. 2006. The conformational dynamics of a metastable serpin studied by hydrogen exchange and mass spectrometry. Biochemistry. 45:6561-6569.
27. Zhang, Z., and D. L. Smith. 1993. Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci. 2:522-531.
28. Weis, D. D., J. R. Engen, and I. J. Kass. 2006. Semi-automated data processing of hydrogen exchange mass spectra using HX-Express. J. Am. Soc. Mass Spectrom. 17:1700-1703.
29. Lindberg, J., S. Sigurdsson, ., T. Unge. 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.
30. Ren, J., J. Milton, ., D. K. Stammers. 2000. Structural basis for the resilience of efavirenz (DMP-266) to drug resistance mutations in HIV-1 reverse transcriptase. Structure. 8:1089-1094.
31. Tsutsui, Y., and P. L. Wintrode. 2007. Hydrogen/deuterium exchangemass spectrometry: A powerful tool for probing protein structure, dynamics and interactions. Curr. Med. Chem. 14:2344-2358.
32. Das, K., P. J. Lewi,., E. Arnold. 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.
33. Sobolev, V., A. Sorokine, ., M. Edelman. 1999. Automated analysis of interatomic contacts in proteins. Bioinformatics. 15:327-332.
34. Deng, Y., and D. L. Smith. 1998. Identification of unfolding domains in large proteins by their unfolding rates. Biochemistry. 37:6256-6262.
35. Sluis-Cremer, N., and G. Tachedjian. 2008. Mechanisms of inhibition of HIV replication by non-nucleoside reverse transcriptase inhibitors. Virus Res. 134:147-156.
36. Tachedjian, G., M. Orlova,., S. P. Goff. 2001. Nonnucleoside reverse transcriptase inhibitors are chemical enhancers of dimerization of the HIV type 1 reverse transcriptase. Proc. Natl. Acad. Sci. USA. 98:7188-7193.
37. Steitz, T. A. 2006. Visualizing polynucleotide polymerase machines at work. EMBO J. 25:3458-3468.
38. Svetlov, V., and E. Nudler. 2009. Macromolecular micromovements: how RNA polymerase translocates. Curr. Opin. Struct. Biol. 19: 701-707.
39. Hang, J. Q., Y. Li, ., K. Klumpp. 2007. Substrate-dependent inhibition or stimulation of HIV RNase H activity by non-nucleoside reverse transcriptase inhibitors (NNRTIs). Biochem. Biophys. Res. Commun. 352:341-350.
40. Radzio, J., and N. Sluis-Cremer. 2008. Efavirenz accelerates HIV-1 reverse transcriptase ribonuclease H cleavage, leading to diminished zidovudine excision. Mol. Pharmacol. 73:601-606.
41. Himmel, D. M., S. G. Sarafianos, ., E. Arnold. 2006. HIV-1 reverse transcriptase structure with RNase H inhibitor dihydroxy benzoyl napthyl hydrazone bound at a novel site. ACS Chem. Biol. 1:702-712.
42. Braz, V. A., M. D. Barkley,., P. L.Wintrode. 2010. Efavirenz binding site in HIV-1 reverse transcriptase monomers. Biochemistry. 49:10565-10573.
43. Ehteshami, M., and M. Götte. 2008. Effects of mutations in the connection and RNase H domains of HIV-1 reverse transcriptase on drug susceptibility. AIDS Rev. 10:224-235.
44. Hynes, R. O. 2002. Integrins: Bidirectional, allosteric signaling machines. Cell. 110:673-687.
45. Tian,W.-N., D. D. Miller, and R. C. Deth. 2000. Bidirectional allosteric effects of agonists and GTP at a2A/D-adrenoceptors. J. Pharmacol. Exp. Ther. 292:664-671.
46. Pari, K., G. A. Mueller, ., R. E. London. 2003. Solution structure of the RNase H domain of the HIV-1 reverse transcriptase in the presence of magnesium. Biochemistry. 42:639-650.
47. Smith, J. S., and M. J. Roth. 1993. Purification and characterization of an active human immunodeficiency virus type 1 RNase H domain. J. Virol. 67:4037-4049.
48. Luque, I., S. A. Leavitt, and E. Freire. 2002. The linkage between protein folding and functional cooperativity: Two sides of the same coin? Annu. Rev. Biophys. Biomol. Struct. 31:235-256.
49. Pan, H., J. C. Lee, and V. J. Hilser. 2000. Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc. Natl. Acad. Sci. USA. 97:12020-12025.
50. Freire, E. 1999. The propagation of binding interactions to remote sites in proteins: Analysis of the binding of the monoclonal antibody D1.3 to lysozyme. Proc. Natl. Acad. Sci. USA. 96:10118-10122.
51. Goodey, N. M., and S. J. Benkovic. 2008. Allosteric regulation and catalysis emerge via a common route. Nat. Chem. Biol. 4:474-482.
52. DeLano,W. L. 2002. The PyMOL Molecular Graphic System. DeLano Scientific, San Carlos, CA. http://www.pymol.org.