Conformation-specific Display of 4E10 and 2F5 Epitopes on Self-assembling Protein Nanoparticles as a Potential HIV Vaccine

Chemical Biology and Drug Design

Volumn 80, Issue 3, 2012, Pages 349-357

  Wahome, Newton ^a   Pfeiffer, Tanya ^b   Ambiel, Ina ^c   Yang, Yongkun ^a   Keppler, Oliver T ^c   Bosch, Valerie ^b   Burkhard, Peter ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Membrane proximal external region (MPER); Repetitive antigen display; Self assembling protein nanoparticle (SAPN)

Indexed keywords

EPITOPE; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MOLECULAR SCAFFOLD; MONOCLONAL ANTIBODY; NANOPARTICLE; SELF ASSEMBLING PROTEIN NANOPARTICLE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; HUMORAL IMMUNITY; IMMUNIZATION; MEMBRANE PROXIMAL EXTERNAL REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; EPITOPES; FEMALE; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, HUMORAL; IMMUNIZATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NANOPARTICLES; NEUTRALIZATION TESTS; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY;

HUMAN IMMUNODEFICIENCY VIRUS 1; RATTUS;

EID: 84864140552     PISSN: 17470277     EISSN: 17470285     Source Type: Journal    
DOI: 10.1111/j.1747-0285.2012.01423.x     Document Type: Article

References (39)

1. Burton D.R., Stanfield R.L., Wilson I.A. (2005) Antibody vs. HIV in a clash of evolutionary titans. Proc Nat Acad Sci USA;102:14943-14948.
2. Zwick M.B. (2005) The membrane-proximal external region of HIV-1 gp41: a vaccine target worth exploring. AIDS;19:1725-1737.
3. Mascola J.R., Montefiori D.C. (2010) The role of antibodies in HIV vaccines. Annu Rev Immunol;28:413-444.
4. Hoxie J.A. (2010) Toward an antibody-based HIV-1 vaccine. Annu Rev Med;61:135-152.
5. Hessell A.J., Rakasz E.G., Tehrani D.M., Huber M., Weisgrau K.L., Landucci G. Forthal D. N., Koff W. C., Poignard P., Watkins D. I., Burton D. R. (2010) Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by Simian-Human immunodeficiency virus SHIVBa-L. J Virol;84:1302-1313.
6. 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., Parren P.W. (2001) Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol;75:10892-10905.
7. Vishwanathan S.A., Hunter E. (2008) The Membrane-Proximal External Region (MPER) of HIV-1 gp41-importance of its membrane-perturbing properties to viral fusion. J Virol;82:5118-5126.
8. Apellàniz B., Nir S., Nieva J.L. (2009) Distinct mechanisms of lipid bilayer perturbation induced by peptides derived from the membrane-proximal external region of HIV-1 gp41. Biochemistry;48:5320-5331.
9. Alam S.M., Morelli M., Dennison S.M., Liao H.X., Zhang R., Xia S.M., Rits-Volloch S., Sun L., Harrison S.C., Haynes B.F., Chen B. (2009) Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc Nat Acad Sci;106:20234-20239.
10. Frey G., Peng H., Rits-Volloch S., Morelli M., Cheng Y., Chen B. (2008) A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc Nat Acad Sci;105:3739-3744.
11. Liu J., Deng Y., Dey A.K., Moore J.P., Lu M. (2009) Structure of the HIV-1 gp41 membrane-proximal ectodomain region in a putative prefusion conformation. Biochemistry;48:2915-2923.
12. O'Rourke S.M., Schweighardt B., Scott W.G., Wrin T., Fonseca D.P., Sinangil F., Berman P.W. (2009) Novel ring structure in the gp41 trimer of HIV-1 that modulates sensitivity and resistance to broadly neutralizing antibodies. J Virol;83:7728-7738.
13. Hinz A., Schoehn G., Quendler H., Hulsik D.L., Stiegler G., Katinger H., Seaman M.S., Montefiori D., Weissenhorn W. (2009) Characterization of a trimeric MPER containing HIV-1 gp41 antigen. Virology;390:221-227.
14. Ofek G., Guenaga F.J., Schief W.R., Skinner J., Baker D., Wyatt R., Kwong P.D. (2010) Elicitation of structure-specific antibodies by epitope scaffolds. Proc Nat Acad Sci;107:17880.
15. Guenaga J., Dosenovic P., Ofek G., Baker D., Schief W.R., Kwong P.D., Karlsson Hedestam G.B., Wyatt R.T. (2011) Heterologous epitope-scaffold prime boosting immuno-focuses B cell responses to the HIV-1 gp41 2F5 neutralization determinant. PLoS ONE;6:e16074.
16. Keppler O.T., Welte F.J., Ngo T.A., Chin P.S., Patton K.S., Tsou C.-L., Abbey N.W. (2002) Progress toward a human CD4/CCR5 transgenic rat model for de novo infection by human immunodeficiency virus type 1. J Exp Med;195:719-736.
17. Goffinet C., Allespach I., Keppler O.T. (2007) HIV-susceptible transgenic rats allow rapid preclinical testing of antiviral compounds targeting virus entry or reverse transcription. Proc Nat Acad Sci;104:1015-1020.
18. Raman S., Machaidze G., Lustig A., Aebi U., Burkhard P. (2006) Structure-based design of peptides that self-assemble into regular polyhedral nanoparticles. Nanomed Nanotechnol Biol Med;2:95-102.
19. Kaba S.A., Brando C., Guo Q., Mittelholzer C., Raman S., Tropel D., Aebi U., Burkhard P., Lanar D.E. (2009) A nonadjuvanted polypeptide nanoparticle vaccine confers long-lasting protection against rodent malaria. J Immunol;183:7268-7277.
20. Burkhard P., Ivaninskii S., Lustig A. (2002) Improving coiled-coil stability by optimizing ionic interactions. J Mol Biol;318:901-910.
21. Schroeder U., Graff A., Buchmeier S., Rigler P., Silvan U., Tropel D., Jockusch B.M., Aebi U., Burkhard P., Schoenenberger C.-A. (2009) Peptide nanoparticles serve as a powerful platform for the immunogenic display of poorly antigenic actin determinants. J Mol Biol;386:1368-1381.
22. Pimentel T.A.P.F., Yan Z., Jeffers S.A., Holmes K.V., Hodges R.S., Burkhard P. (2009) Peptide nanoparticles as novel immunogens: design and analysis of a prototypic severe acute respiratory syndrome vaccine. Chem Biol Drug Des;73:53-61.
23. Raman S., Machaidze G., Lustig A., Olivieri V., Aebi U., Burkhard P. (2009) Design of peptide nanoparticles using simple protein oligomerization domains. Open Nanomed J;2:15-26.
24. Buchacher A., Predl R., Strutzenberger K., Steinfellner W., Trkola A., Purtscher M., Gruber G., Tauer C., Steindl F., Jungbauer A., Katinger H. (1994) Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res Hum Retroviruses;10:359-369.
25. Stiegler G., Kunert R., Purtscher M., Wolbank S., Voglauer R., Steindl F., Katinger H. (2001) A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses;17:1757-1765.
26. Burton D.R., Barbas C.F., Persson M.A., Koenig S., Chanock R.M., Lerner R.A. (1991) A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc Nat Acad Sci USA;88:10134-10137.
27. Chesebro B., Wehrly K. (1988) Development of a sensitive quantitative focal assay for human immunodeficiency virus infectivity. J Virol;62:3779-3788.
28. Bosch V., Pfeiffer T., Devitt G., Allespach I., Ebensen T., Emerson V., Guzman C.A., Keppler O.T. (2009) HIV pseudovirion vaccine exposing Env "fusion intermediates"- response to immunisation in human CD4/CCR5-transgenic rats. Vaccine;27:2202-2212.
29. Scherer E.M., Leaman D.P., Zwick M.B., McMichael A.J., Burton D.R. (2010) Aromatic residues at the edge of the antibody combining site facilitate viral glycoprotein recognition through membrane interactions. Proc Nat Acad Sci;107:1529-1534.
30. Sun Z.-Y.J., Oh K.J., Kim M., Yu J., Brusic V., Song L., Qiao Z., Wang J.-h., Wagner G., Reinherz E.L. (2008) HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity;28:52-63.
31. Ruprecht C., Berlinger L., Trkola A. (2009) P04-37. Kinetic and thermodynamic factors determine HIV-1 neutralizing potency of MPER-specific antibodies. Retrovirology;6:P65.
32. Ofek G., McKee K., Yang Y., Yang Z.Y., Skinner J., Guenaga F.J., Wyatt R., Zwick M.B., Nabel G.J., Mascola J.R., Kwong P.D. (2010) Relationship between antibody 2F5 neutralization of HIV-1 and hydrophobicity of its heavy chain third complementarity-determining region. J Virol;84:2955-2962.
33. Julien J.P., Huarte N., Maeso R., Taneva S.G., Cunningham A., Nieva J.L., Pai E.F. (2010) Ablation of the CDR H3 apex of the anti-HIV-1 broadly neutralizing antibody 2F5 abrogates neutralizing capacity without affecting core epitope binding. J Virol;84:4136-4147.
34. a-restricted B cell receptor interactions with the HIV-1 envelope gp41 membrane proximal external region. PLoS ONE;4:e7215.
35. Verkoczy L., Diaz M., Holl T.M., Ouyang Y.-B., Bouton-Verville H., Alam S.M., Liao H.-X., Kelsoe G., Haynes B.F. (2010) Autoreactivity in an HIV-1 broadly reactive neutralizing antibody variable region heavy chain induces immunologic tolerance. Proc Nat Acad Sci;107:181-186.
36. Ebensen T., Guzmán C.A. (2009) Immune Modulators with Defined Molecular Targets: Cornerstone to Optimize Rational Vaccine Design. Adv Exp Med Biol;655:171-188.
37. Matyas G.R., Wieczorek L., Beck Z., Ochsenbauer-Jambor C., Kappes J.C., Michael N.L., Polonis V.R., Alving C.R. (2009) Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS;23:2069-2077.
38. Walker L.M., Phogat S.K., Chan-Hui P.Y., Wagner D., Phung P., Goss J.L., Wrin T. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science;326:285-289.
39. Zolla-Pazner S. (2005) Improving on nature: focusing the immune response on the V3 loop. Hum Antibodies;14:69-72.