Importance of the membrane-perturbing properties of the membrane-proximal external region of human immunodeficiency virus type 1 gp41 to viral fusion

Journal of Virology

Volumn 82, Issue 11, 2008, Pages 5118-5126

  Vishwanathan, Sundaram A ^a   Hunter, Eric ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCOPROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROLINE; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL SURFACE; CELL TRANSPORT; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE; MEMBRANE DAMAGE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN TRANSPORT; VIRION; VIRUS ENTRY; VIRUS MORPHOLOGY; WILD TYPE;

AMINO ACID SEQUENCE; CELL LINE; GENE EXPRESSION REGULATION; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 43949135190     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00305-08     Document Type: Article

References (46)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Alam, S. M., R. M. Scearce, R. J. Parks, K. Plonk, S. G. Plonk, L. L. Sutherland, M. K. Gorny, S. Zolla-Pazner, S. Vanleeuwen, M. A. Moody, S. M. Xia, D. C. Montefiori, G. D. Tomaras, K. J. Weinhold, S. A. Karim, C. B. Hicks, H. X. Liao, J. Robinson, G. M. Shaw, and B. F. Haynes. 2008. Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J. Virol. 82:115-125.
3. Barbate, G., E. Bianchi, P. Ingallinella, W. H. Hurni, M. D. Miller, G. Ciliberto, R. Cortese, R. Bazzo, J. W. Shiver, and A. Pessi. 2003. Structural analysis of the epitope of the anti-HIV antibody 2F5 sheds light into its mechanism of neutralization and HIV fusion. J. Mol. Biol. 330:1101-1115.
4. Bennett, A., J. Liu, D. Van Ryk, D. Bliss, J. Arthos, R. M. Henderson, and S. Subramaniam. 2007. Cryoelectron tomographic analysis of an HIV-neutralizing protein and its complex with native viral gp120. J. Biol. Chem. 282: 27754-27759.
5. Biron, Z., S. Khare, A. O. Samson, Y. Hayek, F. Naider, and J. Anglister. 2002. A monomeric 3(10)-helix is formed in water by a 13-residue peptide representing the neutralizing determinant of HIV-1 on gp41. Biochemistry 41:12687-12696.
6. Chakrabartty, A., T. Kortemme, and R. L. Baldwin. 1994. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci. 3:843-852.
7. Chiu, J., P. E. March, R. Lee, and D. Tillett. 2004. Site-directed, ligase-independent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res. 32:e174.
8. Davis, M. R., J. Jiang, J. Zhou, E. O. Freed, and C. Aiken. 2006. A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J. Virol. 80: 2405-2417.
9. Decroly, E., M. Vandenbranden, J. M. Ruysschaert, J. Cogniaux, G. S. Jacob, S. C. Howard, G. Marshall, A. Kompelli, A. Basak, F. Jean, and et al. 1994. The convertases furin and PC1 can both cleave the human immunodeficiency virus (HIV)-1 envelope glycoprotein gp160 into gp120 (HIV-1 SU) and gp41 (HIV-I TM). J. Biol. Chem. 269:12240-12247.
10. Dorfman, T., F. Mammano, W. A. Haseltine, and H. G. Gottlinger. 1994. Role of the matrix protein in the virion association of the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 68:1689-1696.
11. Dubay, J. W., S. J. Roberts, B. H. Hahn, and E. Hunter. 1992. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J. Virol. 66:6616-6625.
12. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
13. Edwards, T. G., S. Wyss, J. D. Reeves, S. Zolla-Pazner, J. A. Hoxie, R. W. Doms, and F. Baribaud. 2002. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J. Virol. 76:2683-2691.
14. Falla, T. J., D. N. Karunaratne, and R. E. Hancock. 1996. Mode of action of the antimicrobial peptide indolicidin. 1. Biol. Chem. 271:19298-19303.
15. Forster, F., O. Medalia, N. Zauberman, W. Baumeister, and D. Fass. 2005. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102:4729-4734.
16. Freed, E. O., and M. A. Martin. 1996. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70:341-351.
17. Friedrich, C. L., A. Rozek, A. Patrzykat, and R. E. Hancock. 2001. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria. J. Biol. Chem. 276:24015-24022.
18. Gray, E. S., P. L. Moore, F. Bibollet-Ruche, H. Li, J. M. Decker, T. Meyers, G. M. Shaw, and L. Morris. 2008. 4E10-resistant variants in a human immunodeficiency virus type 1 subtype C-infected individual with an anti-membrane proximal external region-neutralizing antibody response. J. Virol. 82:2367-2375.
19. Gray, E. S., P. L. Moore, I. A. Choge, J. M. Decker, F. Bibollet-Ruche, H. Li, N. Leseka, F. Treurnicht, K. Mlisana, G. M. Shaw, S. S. Karim, C. Williamson, and L. Morris. 2007. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. 81:6187-6196.
20. Hallenberger, S., V. Bosch, H. Angliker, E. Shaw, H. D. Klenk, and W. Garten. 1992. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360:358-361.
21. Hurley, J. H., D. A. Mason, and B. W. Matthews. 1992. Flexible-geometry conformational energy maps for the amino acid residue preceding a proline. Biopolymers 32:1443-1446.
22. Li, S. C., N. K. Goto, K. A. Williams, and C. M. Deber. 1996. Alpha-helical, but not beta-sheet, propensity of proline is determined by peptide environment. Proc. Natl. Acad. Sci. USA 93:6676-6681.
23. Lu, M., S. C. Blacklow, and P. S. Kim. 1995. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2:1075-1082.
24. Munoz-Barroso, I., K. Salzwedel, E. Hunter, and R. Blumenthal. 1999. Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J. Virol. 73:6089-6092.
25. Muster, T., F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Ruker, and H. Katinger. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:6642-6647.
26. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
27. Reithmeier, R. A. 1995. Characterization and modeling of membrane proteins using sequence analysis. Curr. Opin. Struct. Biol. 5:491-500.
28. Robison, C. S., and M. A. Whitt. 2000. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74:2239-2246.
29. Rozek, A., C. L. Friedrich, and R. E. Hancock. 2000. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 39:15765-15774.
30. Salzwedel, K., J. T. West, and E. Hunter. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
31. Schibli, D. J., R. C. Montelaro, and H. J. Vogel. 2001. The membrane-proximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well-defined helix in dodecylphosphocholine micelles. Biochemistry 40: 9570-9578.
32. Selsted, M. E., M. J. Novotny, W. L. Morris, Y. Q. Tang, W. Smith, and J. S. Cullor. 1992. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267:4292-4295.
33. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
34. Stiegler, G., R. Kunert, M. Purtscher, S. Wolbank, R. Voglauer, F. Steindl, and H. Katinger. 2001. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 17:1757-1765.
35. Suarez, T., W. R. Gallaher, A. Agirre, F. M. Goni, and J. L. Nieva. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047.
36. Subbalakshmi, C., V. Krishnakumari, R. Nagaraj, and N. Sitaram. 1996. Requirements for antibacterial and hemolytic activities in the bovine neutrophil derived 13-residue peptide indolicidin. FEBS Lett. 395:48-52.
37. Sun, Z. Y., K. J. Oh, M. Kim, J. Yu, V. Brusic, L. Song, Z. Qiao, J. H. Wang, G. Wagner, and E. L. Reinherz. 2008. HIV-1 Broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28:52-63.
38. Weissenhorn, W., L. J. Calder, S. A. Wharton, J. J. Skehel, and D. C. Wiley. 1998. The central structural feature of the membrane fusion protein subunit from the Ebola virus glycoprotein is a long triple-stranded coiled coil. Proc. Natl. Acad. Sci. USA 95:6032-6036.
39. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430.
40. Wild, C., T. Greenwell, and T. Matthews. 1993. A synthetic peptide from HIV-1 gp41 is a potent inhibitor of virus-mediated cell-cell fusion. AIDS Res. Hum. Retrovir. 9:1051-1053.
41. Williams, K. A., and C. M. Deber. 1991. Proline residues in transmembrane helices: structural or dynamic role? Biochemistry 30:8919-8923.
42. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
43. Zanetti, G., J. A. Briggs, K. Grunewald, Q. J. Sattentau, and S. D. Fuller. 2006. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog. 2:e83.
44. Zhu, P., J. Liu, J. Bess, Jr., E. Chertova, J. D. Lifson, H. Grise, G. A. Ofek, K. A. Taylor, and K. H. Roux. 2006. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852.
45. Zwick, M. B., R. Jensen, S. Church, M. Wang, G. Stiegler, R. Kunert, H. Katinger, and D. R. Burton. 2005. Anti-human immunodeficiency virus type 1 (HIV-1) antibodies 2F5 and 4E10 require surprisingly few crucial residues in the membrane-proximal external region of glycoprotein gp41 to neutralize HIV-1. J. Virol. 79:1252-1261.
46. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. Parren. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905.