X-ray Crystallographic Study of an HIV-1 Fusion Inhibitor with the gp41 S138A Substitution

Journal of Molecular Biology

Volumn 392, Issue 3, 2009, Pages 657-665

  Watabe, Tsuyoshi ^a   Terakawa, Yukihiro ^a   Watanabe, Kentaro ^a   Ohno, Hiroaki ^a   Nakano, Hiroaki ^a   Nakatsu, Toru ^a   Kato, Hiroaki ^a   Izumi, Kazuki ^a   Kodama, Eiichi ^a   Matsuoka, Masao ^a   Kitaura, Kazuo ^a   Oishi, Shinya ^a   Fujii, Nobutaka ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

C HR derived peptide; desolvation energy; gp41 S138A substitution; HIV 1 fusion inhibitor; hydrophobicity

Indexed keywords

ALANINE; GLYCOPROTEIN GP 41; HYBRID PROTEIN; PEPTIDE DERIVATIVE; SERINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; SOLVATION; X RAY CRYSTALLOGRAPHY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, VIRAL; HIV ENVELOPE PROTEIN GP41; HIV FUSION INHIBITORS; HIV-1; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 69349103719     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.027     Document Type: Article

References (35)

1. Lu M., Blacklow S.C., and Kim P.S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2 (1995) 1075-1082
2. Chan D.C., Fass D., Berger J.M., and Kim P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89 (1997) 263-273
3. Weissenhorn W., Dessen A., Harrison S.C., Skehel J.J., and Wiley D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387 (1997) 426-430
4. Melikyan G.B., Markosyan R.M., Hemmati H., Delmedico M.K., Lambert D.M., and Cohen F.S. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol. 151 (2000) 413-423
5. Wild C., Oas T., McDanal C., Bolognesi D., and Matthews T. A synthetic peptide inhibitor of human immunodeficiency virus replication: correlation between solution structure and viral inhibition. Proc. Natl Acad. Sci. USA 89 (1992) 10537-10541
6. Wild C.T., Shugars D.C., Greenwell T.K., McDanal C.B., and Matthews T.J. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl Acad. Sci. USA 91 (1994) 9770-9774
7. Chen C.H., Matthews T.J., McDanal C.B., Bolognesi D.P., and Greenberg M.L. A molecular clasp in the human immunodeficiency virus (HIV) type 1 TM protein determines the anti-HIV activity of gp41 derivatives: implication of viral fusion. J. Virol. 69 (1995) 3771-3777
8. Kilby J.M., Hopkins S., Venetta T.M., DiMassimo B., Cloud G.A., Lee J.Y., et al. Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat. Med. 4 (1998) 1302-1307
9. Matthews T., Salgo M., Greenberg M., Chung J., DeMasi R., and Bolognesi D. Enfuvirtide: the first therapy to inhibit the entry of HIV-1 into host CD4 lymphocytes. Nat. Rev., Drug Discov. 3 (2004) 215-225
10. Wei X., Decker J.M., Liu H., Zhang Z., Arani R.B., Kilby J.M., et al. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46 (2002) 1896-1905
11. Marcelin A.G., Reynes J., Yerly S., Ktorza N., Segondy M., Piot J.C., et al. Characterization of genotypic determinants in HR-1 and HR-2 gp41 domains in individual with persistent HIV viraemia under T-20. AIDS 18 (2004) 1340-1342
12. Xu L., Pozniak A., Wildfire A., Stanfield-Oakley S.A., Mosier S.M., Ratcliffe D., et al. Emergence and evolution of enfuvirtide resistance following long-term therapy involves heptad repeat 2 mutations within gp41. Antimicrob. Agents Chemother. 49 (2005) 1113-1119
13. Otaka A., Nakamura M., Nameki D., Kodama E., Uchiyama S., Nakamura S., et al. Remodeling gp41-C34 peptide leads to high effective inhibitors of the fusion of HIV-1 with target cells. Angew. Chem., Int. Ed. 41 (2002) 2937-2940
14. Oishi S., Ito S., Nishikawa H., Watanabe K., Tanaka M., Ohno H., et al. Design of a novel HIV-1 fusion inhibitor that displays a minimal interface for binding affinity. J. Med. Chem. 51 (2008) 388-391
15. Joyce J.G., Hunri W.M., Bogusky M.J., Garsky V.M., Liang X., Citron M.P., et al. Enhancement of α-helicity in the HIV-1 inhibitory peptide DP178 leads to an increased affinity for human monoclonal antibody 2F5 but does not elicit neutralizing responses in vitro. J. Biol. Chem. 277 (2002) 45811-45820
16. Dweyr J.J., Wilson K.L., Davison D.K., Freel S.A., Seedolff J.E., Wring S.A., et al. Design of helical, oligomeric HIV-1 fusion inhibitor peptides with potent activity against enfuvirtide-resistant virus. Proc. Natl Acad. Sci. USA 104 (2007) 12772-12777
17. Chan D.C., Chutkowski C.T., and Kim P.S. Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target. Proc. Natl Acad. Sci. USA 95 (1998) 15613-15617
18. Strockbine B., and Rizzo R.C. Binding of antifusion peptides with HIVgp41 from molecular dynamics simulations: quantitative correlation with experiment. Proteins: Struct. Funct. Bioinform. 67 (2007) 630-642
19. Izumi K., Kodama E., Shimura K., Sakagami Y., Watanabe K., Ito S., et al. Design of peptide-based inhibitors for human immunodeficiency virus type 1 strains resistant to T-20. J. Biol. Chem. 284 (2009) 4914-4920
20. Sitkoff D., Sharp K.A., and Honig B. Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98 (1994) 1978-1988
21. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59 (1986) 284-291
22. Judice J.K., Tom J.Y., Huang W., Wrin T., Vennari J., Petropoulos C.J., and McDowell R.S. Inhibition of HIV type 1 infectivity by constrained α-helical peptides: implications for the viral fusion mechanism. Proc. Natl Acad. Sci. USA 94 (1997) 13426-13430
23. Shu W., Liu J., Ji H., Radigen L., Jiang S., and Lu M. Helical interactions in the HIV-1 gp41 core reveal structural basis for the inhibitory activity of gp41 peptides. Biochemistry 39 (2000) 1634-1642
24. Ueno M., Kodama E., Shimura K., Sakurai Y., Kajiwara K., Sakagami Y., et al. Synonymous mutations in stem-loop III of Rev responsive elements enhance HIV-1 replication impaired by primary mutations for resistance to enfuvirtide. Antiviral Res. 82 (2009) 67-72
25. Bai X., Wilson K.L., Seedorff J.E., Ahrens D., Green J., Davison D.K., et al. Impact of the enfuvirtide resistance mutation N43D and the associated baseline polymorphism E137K on peptide sensitivity and six-helix bundle structure. Biochemistry 47 (2008) 6662-6670
26. Pflugrath J.W. The finer things in X-ray diffraction data collection. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 1718-1725
27. Vagin A., and Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr., Sect. D: Biol. Crystallogr. 56 (2000) 1622-1624
28. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
29. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
30. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
31. MOE software package from Chemical Computing Group Inc., http://www.chemcomp.com.
32. Wang J.M., Cieplak P., and Kollman P.A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules. J. Comput. Chem. 21 (2000) 1049-1074
33. Pearlman D.A., Case D.A., Caldwell J.W., Ross W.R., Cheatham T.E., DeBolt S., et al. AMBER, a computer program for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to elucidate the structures and energies of molecules. Comp. Phys. Commun. 91 (1995) 1-41
34. Honig B., and Nicholls A. Classical electrostatics in biology and chemistry. Science 268 (1995) 1144-1149
35. Sanner M.F., Olson A.J., and Spehner J. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38 (1996) 305-320