Characterization of a trimeric MPER containing HIV-1 gp41 antigen

Virology

Volumn 390, Issue 2, 2009, Pages 221-227

  Hinz, Andreas ^a   Schoehn, Guy ^a,b   Quendler, Heribert ^c   Hulsik, David Lutje ^a   Stiegler, Gabi ^c   Katinger, Hermann ^c   Seaman, Michael S ^e   Montefiori, David ^d   Weissenhorn, Winfried ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c UNIVERSITY OF AGRICULTURAL SCIENCES   (Austria)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

gp41; HIV 1; mAb 2F5; mAb 4E10; Membrane fusion

Indexed keywords

GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; MONOCLONAL ANTIBODY Z13; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNIZATION; MALE; MEMBRANE FUSION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; RABBIT; STAINING; VIRUS ENVELOPE; VIRUS ISOLATION; VIRUS NEUTRALIZATION;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, VIRAL; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV-1; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RABBITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

HUMAN IMMUNODEFICIENCY VIRUS 1; ORYCTOLAGUS CUNICULUS;

EID: 67649850373     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.05.015     Document Type: Article

References (68)

1. Alam S.M., McAdams M., Boren D., Rak M., Scearce R.M., Gao F., Camacho Z.T., Gewirth D., Kelsoe G., Chen P., and Haynes B.F. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 178 7 (2007) 4424-4435
2. Alam S.M., Scearce R.M., Parks R.J., Plonk K., Plonk S.G., Sutherland L.L., Gorny M.K., Zolla-Pazner S., Vanleeuwen S., Moody M.A., Xia S.M., Montefiori D.C., Tomaras G.D., Weinhold K.J., Karim S.A., Hicks C.B., Liao H.X., Robinson J., Shaw G.M., and Haynes B.F. 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 1 (2008) 115-125
3. Barbato G., Bianchi E., Ingallinella P., Hurni W.H., Miller M.D., Ciliberto G., Cortese R., Bazzo R., Shiver J.W., and Pessi A. 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 5 (2003) 1101-1115
4. Binley J.M., Cayanan C.S., Wiley C., Schulke N., Olson W.C., and Burton D.R. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J. Virol. 77 10 (2003) 5678-5684
5. Binley J.M., Lybarger E.A., Crooks E.T., Seaman M.S., Gray E., Davis K.L., Decker J.M., Wycuff D., Harris L., Hawkins N., Wood B., Nathe C., Richman D., Tomaras G.D., Bibollet-Ruche F., Robinson J.E., Morris L., Shaw G.M., Montefiori D.C., and Mascola J.R. Profiling the specificity of neutralizing antibodies in a large panel of HIV-1 plasmas from subtype B and C chronic infections. J. Virol. 82 23 (2008) 11651-11668
6. Brown B.K., Karasavvas N., Beck Z., Matyas G.R., Birx D.L., Polonis V.R., and Alving C.R. Monoclonal antibodies to phosphatidylinositol phosphate neutralize human immunodeficiency virus type 1: role of phosphate-binding subsites. J. Virol. 81 4 (2007) 2087-2091
7. Brown B.K., Wieczorek L., Sanders-Buell E., Rosa Borges A., Robb M.L., Birx D.L., Michael N.L., McCutchan F.E., and Polonis V.R. Cross-clade neutralization patterns among HIV-1 strains from the six major clades of the pandemic evaluated and compared in two different models. Virology 375 2 (2008) 529-538
8. Brunel F.M., Zwick M.B., Cardoso R.M., Nelson J.D., Wilson I.A., Burton D.R., and Dawson P.E. Structure-function analysis of the epitope for 4E10, a broadly neutralizing human immunodeficiency virus type 1 antibody. J. Virol. 80 4 (2006) 1680-1687
9. Bures R., Gaitan A., Zhu T., Graziosi C., McGrath K.M., Tartaglia J., Caudrelier P., El Habib R., Klein M., Lazzarin A., Stablein D.M., Deers M., Corey L., Greenberg M.L., Schwartz D.H., and Montefiori D.C. Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 16 18 (2000) 2019-2035
10. Burton D.R., Pyati J., Koduri R., Sharp S.J., Thornton G.B., Parren P.W., Sawyer L.S., Hendry R.M., Dunlop N., Nara P.L., et al. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266 5187 (1994) 1024-1027
11. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., and Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5 3 (2004) 233-236
12. Cardoso R.M., Zwick M.B., Stanfield R.L., Kunert R., Binley J.M., Katinger H., Burton D.R., and Wilson I.A. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 22 2 (2005) 163-173
13. Cardoso R.M., Brunel F.M., Ferguson S., Zwick M., Burton D.R., Dawson P.E., and Wilson I.A. Structural basis of enhanced binding of extended and helically constrained peptide epitopes of the broadly neutralizing HIV-1 antibody 4E10. J. Mol. Biol. 365 5 (2007) 1533-1544
14. Cavacini L.A., Duval M., Robinson J., and Posner M.R. Interactions of human antibodies, epitope exposure, antibody binding and neutralization of primary isolate HIV-1 virions. Aids 16 18 (2002) 2409-2417
15. Choudhry V., Zhang M.Y., Harris I., Sidorov I.A., Vu B., Dimitrov A.S., Fouts T., and Dimitrov D.S. Increased efficacy of HIV-1 neutralization by antibodies at low CCR5 surface concentration. Biochem. Biophys. Res. Commun. 348 3 (2006) 1107-1115
16. Conway J.F., and Steven A.C. Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128 1 (1999) 106-118
17. de Rosny E., Vassell R., Jiang S., Kunert R., and Weiss C.D. Binding of the 2F5 monoclonal antibody to native and fusion-intermediate forms of human immunodeficiency virus type 1 gp41: implications for fusion-inducing conformational changes. J. Virol. 78 5 (2004) 2627-2631
18. Dimitrov A.S., Jacobs A., Finnegan C.M., Stiegler G., Katinger H., and Blumenthal R. Exposure of the membrane-proximal external region of HIV-1 gp41 in the course of HIV-1 envelope glycoprotein-mediated fusion. Biochemistry 46 5 (2007) 1398-1401
19. Finnegan C.M., Berg W., Lewis G.K., and DeVico A.L. Antigenic properties of the human immunodeficiency virus transmembrane glycoprotein during cell-cell fusion. J. Virol. 76 23 (2002) 12123-12134
20. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 1 (1996) 190-199
21. Frey G., Peng H., Rits-Volloch S., Morelli M., Cheng Y., and Chen B. A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 105 10 (2008) 3739-3744
22. Gnann J.W.J., Nelson J.A., and Oldstone M.B. Fine mapping of an immunodominant domain in the transmembrane glycoprotein of human immunodeficiency virus. J. Virol. 61 8 (1987) 2639-2641
23. Grundner C., Mirzabekov T., Sodroski J., and Wyatt R. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glycoproteins. J. Virol. 76 7 (2002) 3511-3521
24. Gustchina E., Louis J.M., Lam S.N., Bewley C.A., and Clore G.M. A monoclonal Fab derived from a human nonimmune phage library reveals a new epitope on gp41 and neutralizes diverse human immunodeficiency virus type 1 strains. J. Virol. 81 23 (2007) 12946-12953
25. Harbury P.B., Zhang T., Kim P.S., and Alber T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262 5138 (1993) 1401-1407
26. Harrison S.C. Mechanism of membrane fusion by viral envelope proteins. Adv. Virus. Res. 64 (2005) 231-259
27. Haynes B.F., Fleming J., St Clair E.W., Katinger H., Stiegler G., Kunert R., Robinson J., Scearce R.M., Plonk K., Staats H.F., Ortel T.L., Liao H.X., and Alam S.M. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308 5730 (2005) 1906-1908
28. Haynes B.F., Moody M.A., Verkoczy L., Kelsoe G., and Alam S.M. Antibody polyspecificity and neutralization of HIV-1: a hypothesis. Hum. Antibodies 4 3-4 (2005) 59-67
29. Karlsson Hedestam G.B., Fouchier R.A., Phogat S., Burton D.R., Sodroski J., and Wyatt R.T. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6 2 (2008) 143-155
30. Kim M., Qiao Z., Yu J., Montefiori D., and Reinherz E.L. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 25 27 (2007) 5102-5114
31. Lamb R.A., and Jardetzky T.S. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17 4 (2007) 427-436
32. Law M., Cardoso R.M., Wilson I.A., and Burton D.R. Antigenic and immunogenic study of membrane-proximal external region-grafted gp120 antigens by a DNA prime-protein boost immunization strategy. J. Virol. 81 8 (2007) 4272-4285
33. Lenz O., Dittmar M.T., Wagner A., Ferko B., Vorauer-Uhl K., Stiegler G., and Weissenhorn W. Trimeric membrane-anchored gp41 inhibits HIV membrane fusion. J. Biol. Chem. 280 6 (2005) 4095-4101
34. Louis J.M., Bewley C.A., Gustchina E., Aniana A., and Clore G.M. Characterization and HIV-1 fusion inhibitory properties of monoclonal Fabs obtained from a human non-immune phage library selected against diverse epitopes of the ectodomain of HIV-1 gp41. J. Mol. Biol. 353 5 (2005) 945-951
35. Luftig M.A., Mattu M., Di Giovine P., Geleziunas R., Hrin R., Barbato G., Bianchi E., Miller M.D., Pessi A., and Carfi A. Structural basis for HIV-1 neutralization by a gp41 fusion intermediate-directed antibody. Nat. Struct. Mol. Biol. 13 8 (2006) 740-747
36. Mantis N.J., Kozlowski P.A., Mielcarz D.W., Weissenhorn W., and Neutra M.R. Immunization of mice with recombinant gp41 in a systemic prime/mucosal boost protocol induces HIV-1-specific serum IgG and secretory IgA antibodies. Vaccine 19 28-29 (2001) 3990-4001
37. McGaughey G.B., Citron M., Danzeisen R.C., Freidinger R.M., Garsky V.M., Hurni W.M., Joyce J.G., Liang X., Miller M., Shiver J., and Bogusky M.J. HIV-1 vaccine development: constrained peptide immunogens show improved binding to the anti-HIV-1 gp41 MAb. Biochemistry 42 11 (2003) 3214-3223
38. Montefiori D.C. Evaluating neutralizing antibodies against HIV, SIV and SHIV in luciferase reporter gene assays. In: Coligan J.E., Kruisbeek A.M., Margulies D.H., Shevach E.M., Strober W., and Coico R. (Eds). Current Protocols in Immunology (2004), John Wiley and Sons 2.11.1-12.11.15
39. Montefiori D.C. Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol. Chapter 12 (2005) Unit 12.11
40. Montefiori D.C. Measuring HIV neutralization in a luciferase reporter gene assay. Methods. Mol. Biol. 485 (2009) 395-405
41. Montero M., van Houten N.E., Wang X.F., and Scott J.K. The membrane-proximal external region of the human immunodeficiency virus type I envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol. Mol. Biol. Rev. 72 (2008) 54-84
42. Muster T., Steindl F., Purtscher M., Trkola A., Klima A., Himmler G., Ruker F., and Katinger H. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67 11 (1993) 6642-6647
43. Nelson J.D., Brunel F.M., Jensen R., Crooks E.T., Cardoso R.M., Wang M., Hessell A., Wilson I.A., Binley J.M., Dawson P.E., Burton D.R., and Zwick M.B. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J. Virol. 81 8 (2007) 4033-4043
44. Ofek G., Tang M., Sambor A., Katinger H., Mascola J.R., Wyatt R., and Kwong P.D. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78 19 (2004) 10724-10737
45. Parker C.E., Deterding L.J., Hager-Braun C., Binley J.M., Schulke N., Katinger H., Moore J.P., and Tomer K.B. Fine definition of the epitope on the gp41 glycoprotein of human immunodeficiency virus type 1 for the neutralizing monoclonal antibody 2F5. J. Virol. 75 22 (2001) 10906-10911
46. Penn-Nicholson A., Han D.P., Kim S.J., Park H., Ansari R., Montefiori D.C., and Cho M.W. Assessment of antibody responses against gp41 in HIV-1-infected patients using soluble gp41 fusion proteins and peptides derived from M group consensus envelope. Virology 372 2 (2008) 442-456
47. Polonis V.R., Brown B.K., Rosa Borges A., Zolla-Pazner S., Dimitrov D.S., Zhang M.Y., Barnett S.W., Ruprecht R.M., Scarlatti G., Fenyo E.M., Montefiori D.C., McCutchan F.E., and Michael N.L. Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of the antibody response to infection and vaccination. Virology 375 2 (2008) 315-320
48. Qiao Z.S., Kim M., Reinhold B., Montefiori D., Wang J.H., and Reinherz E.L. Design, expression, and immunogenicity of a soluble HIV trimeric envelope fragment adopting a prefusion gp41 configuration. J. Biol. Chem. 280 24 (2005) 23138-23146
49. Sanchez-Martinez S., Lorizate M., Hermann K., Kunert R., Basanez G., and Nieva J.L. Specific phospholipid recognition by human immunodeficiency virus type-1 neutralizing anti-gp41 2F5 antibody. FEBS Lett. 580 9 (2006) 2395-2399
50. Sanchez-Martinez S., Lorizate M., Katinger H., Kunert R., and Nieva J.L. Membrane association and epitope recognition by HIV-1 neutralizing anti-gp41 2F5 and 4E10 antibodies. AIDS. Res. Hum. Retrovir. 22 10 (2006) 998-1006
51. Sather D.N., Armann J., Ching L.K., Mavrantoni A., Sellhorn G., Caldwell Z., Yu X., Wood B., Self S., Kalams S., and Stamatatos L. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83 2 (2009) 757-769
52. Scherer E.M., Zwick M.B., Teyton L., and Burton D.R. Difficulties in eliciting broadly neutralizing anti-HIV antibodies are not explained by cardiolipin autoreactivity. Aids 21 16 (2007) 2131-2139
53. Schibli D.J., Montelaro R.C., and Vogel H.J. The membrane-proximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well-defined helix in dodecylphosphocholine micelles. Biochemistry 40 32 (2001) 9570-9578
54. Shen X., Parks R.J., Montefiori D.C., Kirchherr J.L., Keele B.F., Decker J.M., Blattner W.A., Gao F., Weinhold K.J., Hicks C.B., Greenberg M.L., Hahn B.H., Shaw G.M., Haynes B.F., and Tomaras G.D. In vivo gp41 antibodies targeting the 2F5 monoclonal antibody epitope mediate human immunodeficiency virus Type 1 neutralization breadth. J. Virol. 83 8 (2009) 3617-3625
55. Stiegler G., Kunert R., Purtscher M., Wolbank S., Voglauer R., Steindl F., and Katinger H. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 17 18 (2001) 1757-1765
56. Sun Z.Y., Oh K.J., Kim M., Yu J., Brusic V., Song L., Qiao Z., Wang J.H., Wagner G., and Reinherz E.L. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28 1 (2008) 52-63
57. Trkola A., Purtscher M., Muster T., Ballaun C., Buchacher A., Sullivan N., Srinivasan K., Sodroski J., Moore J.P., and Katinger H. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70 2 (1996) 1100-1108
58. Verani A., Scarlatti G., Comar M., Tresoldi E., Polo S., Giacca M., Lusso P., Siccardi A.G., and Vercelli D. C-C chemokines released by lipopolysaccharide (LPS)-stimulated human macrophages suppress HIV-1 infection in both macrophages and T cells. J. Exp. Med. 185 5 (1997) 805-816
59. Wagner A., Stiegler G., Vorauer-Uhl K., Katinger H., Quendler H., Hinz A., and Weissenhorn W. One step membrane incorporation of viral antigens as a vaccine candidate against HIV. J. Liposome Res. 17 3-4 (2007) 139-154
60. Walker B.D., and Burton D.R. Toward an AIDS vaccine. Science 320 5877 (2008) 760-764
61. Weissenhorn W., Calder L.J., Dessen A., Laue T., Skehel J.J., and Wiley D.C. Assembly of a rod-shaped chimera of a trimeric GCN4 zipper and the HIV-1 gp41 ectodomain expressed in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 94 12 (1997) 6065-6069
62. 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 6631 (1997) 426-430
63. Weissenhorn W., Hinz A., and Gaudin Y. Virus membrane fusion. FEBS Lett. 581 11 (2007) 2150-2155
64. Xu J.Y., Gorny M.K., Palker T., Karwowska S., and Zolla-Pazner S. Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of human immunodeficiency virus type 1, using ten human monoclonal antibodies. J. Virol. 65 9 (1991) 4832-4838
65. Zhang M.Y., Vu B.K., Choudhary A., Lu H., Humbert M., Ong H., Alam M., Ruprecht R.M., Quinnan G., Jiang S., Montefiori D.C., Mascola J.R., Broder C.C., Haynes B.F., and Dimitrov D.S. Cross-reactive human immunodeficiency virus type 1-neutralizing human monoclonal antibody that recognizes a novel conformational epitope on gp41 and lacks reactivity against self-antigens. J. Virol. 82 14 (2008) 6869-6879
66. Zwick M.B. The membrane-proximal external region of HIV-1 gp41: a vaccine target worth exploring. AIDS 19 16 (2005) 1725-1737
67. Zwick M.B., Labrijn A.F., Wang M., Spenlehauer C., Saphire E.O., Binley J.M., Moore J.P., Stiegler G., Katinger H., Burton D.R., and Parren P.W. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75 22 (2001) 10892-10905
68. Zwick M.B., Komori H.K., Stanfield R.L., Church S., Wang M., Parren P.W., Kunert R., Katinger H., Wilson I.A., and Burton D.R. The long third complementarity-determining region of the heavy chain is important in the activity of the broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2F5. J. Virol. 78 6 (2004) 3155-3161