Cleavage-Independent HIV-1 Env Trimers Engineered as Soluble Native Spike Mimetics for Vaccine Design

Cell Reports

Volumn 11, Issue 4, 2015, Pages 539-550

  Sharma, Shailendra K ^a   deVal, Natalia ^a   Bale, Shridhar ^a   Guenaga, Javier ^a   Tran, Karen ^a   Feng, Yu ^a   Dubrovskaya, Viktoriya ^a   Ward, Andrew B ^a   Wyatt, Richard T ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BG505 ANTIBODY; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; JRFL ANTIBODY; NATIVE FLEXIBLY LINKED TRIMER; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; HYBRID PROTEIN;

AMINO TERMINAL SEQUENCE; ANTIBODY AFFINITY; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN PURIFICATION; ANTIGEN RECOGNITION; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; DRUG DESIGN; DRUG SCREENING; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMAGE RECONSTRUCTION; IMMUNOPRECIPITATION; INTERFEROMETRY; ISOTHERMAL TITRATION CALORIMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN MOTIF; THERMOSTABILITY; VIRUS SPIKE; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; MOLECULAR GENETICS; PROTEIN DEGRADATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AIDS VACCINES; AMINO ACID SEQUENCE; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HEK293 CELLS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS;

EID: 84928583366     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.047     Document Type: Article

References (31)

1. Binley J.M., Sanders R.W., Clas B., Schuelke N., Master A., Guo Y., Kajumo F., Anselma D.J., Maddon P.J., Olson W.C., Moore J.P. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J.Virol. 2000, 74:627-643.
2. Blattner C., Lee J.H., Sliepen K., Derking R., Falkowska E., de la Peña A.T., Cupo A., Julien J.P., van Gils M., Lee P.S., et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 2014, 40:669-680.
3. Checkley M.A., Luttge B.G., Freed E.O. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J.Mol. Biol. 2011, 410:582-608.
4. Chow Y.H., Wei O.L., Phogat S., Sidorov I.A., Fouts T.R., Broder C.C., Dimitrov D.S. Conserved structures exposed in HIV-1 envelope glycoproteins stabilized by flexible linkers as potent entry inhibitors and potential immunogens. Biochemistry 2002, 41:7176-7182.
5. Doria-Rose N.A., Schramm C.A., Gorman J., Moore P.L., Bhiman J.N., DeKosky B.J., Ernandes M.J., Georgiev I.S., Kim H.J., Pancera M., et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 2014, 509:55-62. NISC Comparative Sequencing Program.
6. Falkowska E., Le K.M., Ramos A., Doores K.J., Lee J.H., Blattner C., Ramirez A., Derking R., van Gils M.J., Liang C.H., et al. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 2014, 40:657-668.
7. Forsell M.N., Schief W.R., Wyatt R.T. Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr Opin HIV AIDS 2009, 4:380-387.
8. Guenaga J., de Val N., Tran K., Feng Y., Satchwell K., Ward A.B., Wyatt R.T. Well-ordered trimeric HIV-1 subtype B and C soluble spike mimetics generated by negative selection display native-like properties. PLoS Pathog. 2015, 11:e1004570.
9. Herrera C., Klasse P.J., Michael E., Kake S., Barnes K., Kibler C.W., Campbell-Gardener L., Si Z., Sodroski J., Moore J.P., Beddows S. The impact of envelope glycoprotein cleavage on the antigenicity, infectivity, and neutralization sensitivity of Env-pseudotyped human immunodeficiency virus type 1 particles. Virology 2005, 338:154-172.
10. Huang J., Kang B.H., Pancera M., Lee J.H., Tong T., Feng Y., Imamichi H., Georgiev I.S., Chuang G.Y., Druz A., et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 2014, 515:138-142.
11. Julien J.P., Cupo A., Sok D., Stanfield R.L., Lyumkis D., Deller M.C., Klasse P.J., Burton D.R., Sanders R.W., Moore J.P., et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 2013, 342:1477-1483.
12. Khayat R., Lee J.H., Julien J.P., Cupo A., Klasse P.J., Sanders R.W., Moore J.P., Wilson I.A., Ward A.B. Structural characterization of cleaved, soluble HIV-1 envelope glycoprotein trimers. J.Virol. 2013, 87:9865-9872.
13. Kong L., Lee J.H., Doores K.J., Murin C.D., Julien J.P., McBride R., Liu Y., Marozsan A., Cupo A., Klasse P.J., et al. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat. Struct. Mol. Biol. 2013, 20:796-803.
14. Li Y., O'Dell S., Walker L.M., Wu X., Guenaga J., Feng Y., Schmidt S.D., McKee K., Louder M.K., Ledgerwood J.E., et al. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J.Virol. 2011, 85:8954-8967.
15. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J.Struct. Biol. 1999, 128:82-97.
16. Lyumkis D., Julien J.P., de Val N., Cupo A., Potter C.S., Klasse P.J., Burton D.R., Sanders R.W., Moore J.P., Carragher B., et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 2013, 342:1484-1490.
17. McCune J.M., Rabin L.B., Feinberg M.B., Lieberman M., Kosek J.C., Reyes G.R., Weissman I.L. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 1988, 53:55-67.
18. McLellan J.S., Chen M., Joyce M.G., Sastry M., Stewart-Jones G.B., Yang Y., Zhang B., Chen L., Srivatsan S., Zheng A., et al. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 2013, 342:592-598.
19. Murin C.D., Julien J.P., Sok D., Stanfield R.L., Khayat R., Cupo A., Moore J.P., Burton D.R., Wilson I.A., Ward A.B. Structure of 2G12 Fab2 in complex with soluble and fully glycosylated HIV-1 Env by negative-stain single-particle electron microscopy. J.Virol. 2014, 88:10177-10188.
20. Pancera M., Wyatt R. Selective recognition of oligomeric HIV-1 primary isolate envelope glycoproteins by potently neutralizing ligands requires efficient precursor cleavage. Virology 2005, 332:145-156.
21. Pancera M., Zhou T., Druz A., Georgiev I.S., Soto C., Gorman J., Huang J., Acharya P., Chuang G.Y., Ofek G., et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 2014, 514:455-461.
22. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J.Comput. Chem. 2004, 25:1605-1612.
23. Ringe R.P., Sanders R.W., Yasmeen A., Kim H.J., Lee J.H., Cupo A., Korzun J., Derking R., van Montfort T., Julien J.P., et al. Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation. Proc. Natl. Acad. Sci. USA 2013, 110:18256-18261.
24. Sanders R.W., Vesanen M., Schuelke N., Master A., Schiffner L., Kalyanaraman R., Paluch M., Berkhout B., Maddon P.J., Olson W.C., et al. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J.Virol. 2002, 76:8875-8889.
25. Sanders R.W., Derking R., Cupo A., Julien J.P., Yasmeen A., de Val N., Kim H.J., Blattner C., de la Peña A.T., Korzun J., et al. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 2013, 9:e1003618.
26. Scharf L., Scheid J.F., Lee J.H., West A.P., Chen C., Gao H., Gnanapragasam P.N., Mares R., Seaman M.S., Ward A.B., et al. Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 envelope spike. Cell Rep. 2014, 7:785-795.
27. Sok D., van Gils M.J., Pauthner M., Julien J.P., Saye-Francisco K.L., Hsueh J., Briney B., Lee J.H., Le K.M., Lee P.S., et al. Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex. Proc. Natl. Acad. Sci. USA 2014, 111:17624-17629.
28. Stamatatos L., Morris L., Burton D.R., Mascola J.R. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine?. Nat. Med. 2009, 15:866-870.
29. Tran K., Poulsen C., Guenaga J., de Val N., Wilson R., Sundling C., Li Y., Stanfield R.L., Wilson I.A., Ward A.B., et al. Vaccine-elicited primate antibodies use a distinct approach to the HIV-1 primary receptor binding site informing vaccine redesign. Proc. Natl. Acad. Sci. USA 2014, 111:E738-E747.
30. West A.P., Scharf L., Scheid J.F., Klein F., Bjorkman P.J., Nussenzweig M.C. Structural insights on the role of antibodies in HIV-1 vaccine and therapy. Cell 2014, 156:633-648.
31. Wu X., Yang Z.Y., Li Y., Hogerkorp C.M., Schief W.R., Seaman M.S., Zhou T., Schmidt S.D., Wu L., Xu L., et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 2010, 329:856-861.