Collective motions in HIV-1 reverse transcriptase: Examination of flexibility and enzyme function

Journal of Molecular Biology

Volumn 285, Issue 3, 1999, Pages 1023-1037

  Bahar, Ivet ^a,b   Erman, Burak ^d   Jernigan, Robert L ^a   Atilgan, Ali Rana ^b   Covell, David G ^c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b BOGAZICI UNIVERSITY   (Turkey)

^c SAIC FREDERICK INC   (United States)

^d SABANCI UNIVERSITY   (Turkey)

Author keywords

Enzyme function; Flexibility; Mutations; Reverse transcriptase

Indexed keywords

AMINO ACID; DNA BINDING PROTEIN; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; MODEL; NONHUMAN; PRIORITY JOURNAL;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 3342877839     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2371     Document Type: Article

References (41)

1. Bahar I., Jernigan R. L. Inter-residue potentials in globular proteins and the dominance of highly specific hydrophilic interactions at close separation. J. Mol. Biol. 266:1997;195-214.
2. Bahar I., Jernigan R. L. Vibrational dynamics of transfer RNAs: comparison of the free and synthetase bound forms. J. Mol. Biol. 281:1998;871-884.
3. Bahar I., Atilgan A. R., Erman B. Direct evaluation of thermal fluctuations in proteins using a single parameter harmonic potential. Fold. Des. 2:1997;173-181.
4. Bahar I., Atilgan A. R., Demirel M. C., Erman B. Vibrational dynamics of folded proteins: significance of slow and fast modes in relation to function and stability. Phys. Rev. Letters. 80:1998a;2733-2736.
5. Bahar I., Wallqvist A., Covell D. G., Jernigan R. L. Correlation between native state hydrogen exchange and cooperative residue fluctuations from a simple model. Biochemistry. 37:1998b;1067-1075.
6. Boyer P. L., Ferris A. L., Hughes S. H. Cassette mutagenesis of the reverse transcriptase of the human immunodeficiency virus type 1. J. Virol. 66:1992;7533-7537.
7. Boyer P. L., Ferris A. L., Clark P., Whitmer J., Frank P., Tantillo C., Arnold E. A., Hughes S. H. Mutational analysis of the fingers and palm subdomains of human immunodeficiency virus type-1 (HIV-1) reverse transcriptase. J. Mol. Biol. 243:1994;472-483.
8. Cohen J. The daunting challenge of keeping HIV suppressed. Science. 277:1997;32-33.
9. Covell D. G., Smythers G. W., Gronenborn A. M., Clore A. M. Analysis of hydrophobicity in the alpha and beta chemokine families and its relevance to dimerization. Protein Sci. 3:1994;2064-2072.
10. Covell D. G., Jernigan R. L., Wallqvist A. Structural analysis of inhibitor binding to HIV-1 protease: Identification of a common binding motif. Theoret. Chem. 423:1998;93-100.
11. Das K., Ding J., Hsiou Y., Clark A. D. Jr., Moereels H., Koymans L., Andries K., Pauwels R., Janssen P. A. J., Boyer P. L., Clark P., Smith R. H. Jr, Smith M. B. K., Michejda C. J., Hughes S. H., Arnold E. Crystal structures of 8-CI and 9-CI TIBO complexed with wild type HIV-1 RT and 8-CI TIBO complexed with the Tyr181Cys HIV-1 RT drug-resistant mutant. J. Mol. Biol. 264:1996;1085-1100.
12. De Clercq E. HIV resistance to reverse transcriptase inhibitors. Biochem. Pharmacol. 47:1994;155-169.
13. De Clercq E. Antiviral therapy for human immunodeficiency virus infections. Clin. Microbiol. Rev. 8:1995a;200-239.
14. De Clercq E. Toward improved anti-HIV chemotherapy: therapeutic strategies for intervention with HIV-1 infections. J. Med. Chem. 38:1995b;2491-2517.
15. Demirel M. C., Atilgan A. R., Jernigan R. L., Erman B., Bahar I. Identification of kinetically hot residues in proteins. Protein Sci. 7:1998;2522-2532.
16. Ding J., Das K., Moereels H., Koymans L., Andries K., Janssen P. A. J., Hughes S. H., Arnold E. Structure of HIV-1 RT/TIBO R 86183 reveals similarity in the binding of diverse non-nucleoside inhibitors. Nature Struct. Biol. 2:1995a;407-415.
17. Ding J., Das K., Tantillo C., Zhang W., Clark A. D. Jr, Jessen S., Lu X., Hsiou Y., Jacobo-Molina A., Andries K., Pauwels R., Moereels H., Koymans L., Janssen P. A. J., Smith R. H. Jr et al. Structure of HIV-1 reverse transcriptase in a complex with the nonnucleoside inhibitor α-APA R 95845 at 2.8 Å resolution. Structure. 3:1995b;365-379.
18. Esnouf R., Ren J., Ross R., Jones Y., Stammers D., Stuart D. Mechanism of inhibition of HIV-1 reverse transcriptase by nonnucleoside inhibitors. Nature Struct. Biol. 2:1995;303-308.
19. Flory P. J. Statistical thermodynamics of random networks. Proc. Roy. Soc. ser. A. 351:1976;351-380.
20. Frauenfelder H., Petsko G. A., Tsernoglou D. Temperature-dependent X-Ray diffraction as a probe of protein structural dynamics. Nature. 280:1979;558-563.
21. Gao H., Boyer P. L., Arnold E., Hughes S. H. Effects of mutations in the polymerase domain on the polymerase, RNase H, and strand transfer activities of human immunodeficiency virus type 1 reverse transcriptase. J. Mol. Biol. 277:1998;559-572.
22. Garcia A. E., Krumhansl J. A., Frauenfelder H. Variations on a theme by Debye & Waller: from simple crystals to proteins. Proteins: Struct. Funct. Genet. 29:1997;153-160.
23. Haliloglu T., Bahar I., Erman B. Gaussian dynamics of folded proteins. Phys. Rev. Letters. 79:1997;3090-3093.
24. Hsiou Y., Ding J., Das K., Clark A. D. J., Hughes S. H., Arnold E. Structure of unliganded HIV-1 reverse transcriptase at 2.7 Å resolution: implications of conformational changes for polymerization and inhibition mechanisms. Structure. 4:1996;853-860.
25. Jacobo-Molina A., Ding J., Nanni R. G., Clark A. D. J., Lu X., Tantillo C., Williams R., Kamer G., Ferris A. L., Clark P., Hizi A., Hughes H. S., Arnold E. 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. USA. 90:1993;6320-6324.
26. Jäger J., Smerdon S. J., Wang J., Boisvert D. C., Steitz T. A. Comparison of three different crystal forms shows HIV-1 reverse transcriptase displays an internal swivel motion. Structure. 2:1994;869-876.
27. Jernigan R. L., Bahar I. Structure-derived potentials and protein simulations. Curr. Opin. Struct. Biol. 6:1996;195-209.
28. Kloczkowski A., Mark J. E., Erman B. Chain dimensions and fluctuations in random elastomeric networks. 1. Phantom Gaussian networks in the undeformed state. Macromolecules. 22:1989;1423-1432.
29. Kohlstaedt L. A., Wang J., Friedman J. M., Rice P. A., Steitz T. A. Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science. 256:1992;1783-1790.
30. Miyazawa S., Jernigan R. L. Estimation of effective interresidue contact energies from protein crystal structures: Quasi-chemical approximation. Macromolecules. 18:1985;534-552.
31. Miyazawa S., Jernigan R. L. Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J. Mol. Biol. 256:1996;623-644.
32. Nanni R. G., Ding J., Jacobo-Molina A., Arnold E., Hughes S. H. Review of HIV reverse transcriptase three-dimensional structure: implications for drug design. Pers. Drug Dis. Des. 1:1993;129-150.
33. Pearson D. S. Scattered intensity from a chain in a rubber network. Macromolecules. 10:1977;696-701.
34. Ren J., Esnouf R., Garman E., Somers D., Ross C., Kirby I., Keeling J., Darby G., Jones Y., Stuart D., Stammers D. High resolution structures of HIV-1 RT from four RT-inhibitor complexes. Nature Struct. Biol. 2:1995;293-308.
35. Rodgers D. W., Gamblin S. J., Harris B. A., Ray S., Culp J. S., Hellmig B., Woolf D. J., Debouck C., Harrison S. C. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA. 92:1995;1222-1226.
36. Skalka A. M., Goff S. P. Reverse Transcriptase. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
37. Tantillo C., Ding J., Jacobo-Molina A., Nanni R. G., Boyer P. L., Hughes S. H., Pauwels R., Andries K., Janssen P. A. J., Arnold E. Location of anti-AIDS drug binding sites and resistance mutations in the three-dimensional structure of HIV-1 reverse transcriptase: implications for mechanisms of drug inhibition and resistance. J. Mol. Biol. 243:1994;369-387.
38. Tirion M. M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Letters. 77:1996;1905-1908.
39. Varmus H. Retroviruses. Science. 240:1988;1427-1435.
40. Wallqvist A., Jernigan R. L., Covell D. G. A preference-based free energy parameterization of enzyme-inhibitor binding. Applications to HIV-1-protease inhibitor design. Protein Sci. 4:1995;1881-1903.
41. Weiss R., Teich N., Varmus H. E., Coffin J. RNA Tumor Viruses. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.