Particulate Array of Well-Ordered HIV Clade C Env Trimers Elicits Neutralizing Antibodies that Display a Unique V2 Cap Approach

Immunity

Volumn 46, Issue 5, 2017, Pages 804-817.e7

  Martinez Murillo, Paola ^a   Tran, Karen ^b   Guenaga, Javier ^b   Lindgren, Gustaf ^a   Àdori, Monika ^a   Feng, Yu ^b   Phad, Ganesh E ^a   Vázquez Bernat, Néstor ^a   Bale, Shridhar ^b   Ingale, Jidnyasa ^b   Dubrovskaya, Viktoriya ^b   O'Dell, Sijy ^c   Pramanik, Lotta ^a   Spångberg, Mats ^a   Corcoran, Martin ^a   Loré, Karin ^a   Mascola, John R ^c   Wyatt, Richard T ^b   Karlsson Hedestam, Gunilla B ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

B cell responses; clade C; envelope glycoproteins; epitope; germinal centers; HIV 1; liposome; monoclonal antibody; trimers; vaccine

Indexed keywords

ENVELOPE PROTEIN; GLYCAN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; LIPOSOME; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PEPTIDE FRAGMENT; PROTEIN BINDING; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; DNA MODIFICATION; ELECTRON MICROSCOPY; EPITOPE MAPPING; FEMALE; GERMINAL CENTER; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE C; IMMUNIZATION; IMMUNOFLUORESCENCE; NONHUMAN; PARTICULATE MATTER; PRIORITY JOURNAL; PROTEIN TARGETING; RHESUS MONKEY; VIRUS NEUTRALIZATION; VIRUS STRAIN; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; MOLECULAR DOCKING; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE; VIRION;

ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPE MAPPING; EPITOPES; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNIZATION; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; VIRION;

EID: 85019421746     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.04.021     Document Type: Article

References (48)

1. Andrabi, R., Voss, J.E., Liang, C.H., Briney, B., McCoy, L.E., Wu, C.Y., Wong, C.H., Poignard, P., Burton, D.R., Identification of Common Features in Prototype Broadly Neutralizing Antibodies to HIV Envelope V2 Apex to Facilitate Vaccine Design. Immunity 43 (2015), 959–973.
2. Arthos, J., Cicala, C., Martinelli, E., Macleod, K., Van Ryk, D., Wei, D., Xiao, Z., Veenstra, T.D., Conrad, T.P., Lempicki, R.A., et al. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9 (2008), 301–309.
3. Batista, F.D., Neuberger, M.S., Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8 (1998), 751–759.
4. Burton, D.R., Mascola, J.R., Antibody responses to envelope glycoproteins in HIV-1 infection. Nat. Immunol. 16 (2015), 571–576.
5. Carpenter, A.E., Jones, T.R., Lamprecht, M.R., Clarke, C., Kang, I.H., Friman, O., Guertin, D.A., Chang, J.H., Lindquist, R.A., Moffat, J., et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol., 7, 2006, R100.
6. Corcoran, M.M., Phad, G.E., Néstor, V.B., Stahl-Hennig, C., Sumida, N., Persson, M.A., Martin, M., Karlsson Hedestam, G.B., Production of individualized V gene databases reveals high levels of immunoglobulin genetic diversity. Nat. Commun., 7, 2016, 13642.
7. Decker, J.M., Bibollet-Ruche, F., Wei, X., Wang, S., Levy, D.N., Wang, W., Delaporte, E., Peeters, M., Derdeyn, C.A., Allen, S., et al. Antigenic conservation and immunogenicity of the HIV coreceptor binding site. J. Exp. Med. 201 (2005), 1407–1419.
8. 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., NISC Comparative Sequencing Program. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509 (2014), 55–62.
9. Dosenovic, P., von Boehmer, L., Escolano, A., Jardine, J., Freund, N.T., Gitlin, A.D., McGuire, A.T., Kulp, D.W., Oliveira, T., Scharf, L., et al. Immunization for HIV-1 Broadly Neutralizing Antibodies in Human Ig Knockin Mice. Cell 161 (2015), 1505–1515.
10. Escolano, A., Steichen, J.M., Dosenovic, P., Kulp, D.W., Golijanin, J., Sok, D., Freund, N.T., Gitlin, A.D., Oliveira, T., Araki, T., et al. Sequential Immunization Elicits Broadly Neutralizing Anti-HIV-1 Antibodies in Ig Knockin Mice. Cell 166 (2016), 1445–1458.
11. Feng, Y., McKee, K., Tran, K., O'Dell, S., Schmidt, S.D., Phogat, A., Forsell, M.N., Karlsson Hedestam, G.B., Mascola, J.R., Wyatt, R.T., Biochemically defined HIV-1 envelope glycoprotein variant immunogens display differential binding and neutralizing specificities to the CD4-binding site. J. Biol. Chem. 287 (2012), 5673–5686.
12. Forsell, M.N., Dey, B., Mörner, A., Svehla, K., O'dell, S., Högerkorp, C.M., Voss, G., Thorstensson, R., Shaw, G.M., Mascola, J.R., et al. B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathog., 4, 2008, e1000171.
13. Garces, F., Lee, J.H., de Val, N., de la Pena, A.T., Kong, L., Puchades, C., Hua, Y., Stanfield, R.L., Burton, D.R., Moore, J.P., et al. Affinity Maturation of a Potent Family of HIV Antibodies Is Primarily Focused on Accommodating or Avoiding Glycans. Immunity 43 (2015), 1053–1063.
14. Georgiev, I.S., Joyce, M.G., Yang, Y., Sastry, M., Zhang, B., Baxa, U., Chen, R.E., Druz, A., Lees, C.R., Narpala, S., et al. Single-Chain Soluble BG505.SOSIP gp140 Trimers as Structural and Antigenic Mimics of Mature Closed HIV-1 Env. J. Virol. 89 (2015), 5318–5329.
15. Goddard, T.D., Huang, C.C., Ferrin, T.E., Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157 (2007), 281–287.
16. Guenaga, J., Dubrovskaya, V., de Val, N., Sharma, S.K., Carrette, B., Ward, A.B., Wyatt, R.T., Structure-Guided Redesign Increases the Propensity of HIV Env To Generate Highly Stable Soluble Trimers. J. Virol. 90 (2015), 2806–2817.
17. Guenaga, J., Garces, F., de Val, N., Stanfield, R.L., Dubrovskaya, V., Higgins, B., Carrette, B., Ward, A.B., Wilson, I.A., Wyatt, R.T., Glycine substitution at helix-to-coil transitions facilitates the structural determination of a stabilized subtype C HIV envelope glycoprotein. Immunity 46 (2017), 792–803 this issue.
18. Havenar-Daughton, C., Carnathan, D.G., Torrents de la Peña, A., Pauthner, M., Briney, B., Reiss, S.M., Wood, J.S., Kaushik, K., van Gils, M.J., Rosales, S.L., et al. Direct Probing of Germinal Center Responses Reveals Immunological Features and Bottlenecks for Neutralizing Antibody Responses to HIV Env Trimer. Cell Rep. 17 (2016), 2195–2209.
19. Haynes, B.F., Gilbert, P.B., McElrath, M.J., Zolla-Pazner, S., Tomaras, G.D., Alam, S.M., Evans, D.T., Montefiori, D.C., Karnasuta, C., Sutthent, R., et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366 (2012), 1275–1286.
20. Ingale, J., Tran, K., Kong, L., Dey, B., McKee, K., Schief, W., Kwong, P.D., Mascola, J.R., Wyatt, R.T., Hyperglycosylated stable core immunogens designed to present the CD4 binding site are preferentially recognized by broadly neutralizing antibodies. J. Virol. 88 (2014), 14002–14016.
21. Ingale, J., Stano, A., Guenaga, J., Sharma, S.K., Nemazee, D., Zwick, M.B., Wyatt, R.T., High-Density Array of Well-Ordered HIV-1 Spikes on Synthetic Liposomal Nanoparticles Efficiently Activate B Cells. Cell Rep. 15 (2016), 1986–1999.
22. Jiang, X., Totrov, M., Li, W., Sampson, J.M., Williams, C., Lu, H., Wu, X., Lu, S., Wang, S., Zolla-Pazner, S., Kong, X.P., Rationally Designed Immunogens Targeting HIV-1 gp120 V1V2 Induce Distinct Conformation-Specific Antibody Responses in Rabbits. J. Virol. 90 (2016), 11007–11019.
23. Källberg, M., Wang, H., Wang, S., Peng, J., Wang, Z., Lu, H., Xu, J., Template-based protein structure modeling using the RaptorX web server. Nat. Protoc. 7 (2012), 1511–1522.
24. Karlsson Hedestam, G.B., Guenaga, J., Corcoran, M., Wyatt, R.T., Evolution of B cell analysis and Env trimer redesign. Immunol. Rev. 275 (2017), 183–202.
25. Klausen, M.S., Anderson, M.V., Jespersen, M.C., Nielsen, M., Marcatili, P., LYRA, a webserver for lymphocyte receptor structural modeling. Nucleic Acids Res. 43:W1 (2015), W349–W355.
26. Lefranc, M.P., Giudicelli, V., Ginestoux, C., Bodmer, J., Müller, W., Bontrop, R., Lemaitre, M., Malik, A., Barbié, V., Chaume, D., IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 27 (1999), 209–212.
27. Li, M., Gao, F., Mascola, J.R., Stamatatos, L., Polonis, V.R., Koutsoukos, M., Voss, G., Goepfert, P., Gilbert, P., Greene, K.M., et al. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79 (2005), 10108–10125.
28. Liao, H.-X.X., Bonsignori, M., Alam, S.M., McLellan, J.S., Tomaras, G.D., Moody, M.A., Kozink, D.M., Hwang, K.-K.K., Chen, X., Tsao, C.-Y.Y., et al. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38 (2013), 176–186.
29. Lyskov, S., Chou, F.C., Conchúir, S.O., Der, B.S., Drew, K., Kuroda, D., Xu, J., Weitzner, B.D., Renfrew, P.D., Sripakdeevong, P., et al. Serverification of molecular modeling applications: the Rosetta Online Server that Includes Everyone (ROSIE). PLoS ONE, 8, 2013, e63906.
30. Mayr, L.M., Cohen, S., Spurrier, B., Kong, X.P., Zolla-Pazner, S., Epitope mapping of conformational V2-specific anti-HIV human monoclonal antibodies reveals an immunodominant site in V2. PLoS ONE, 8, 2013, e70859.
31. McCoy, L.E., van Gils, M.J., Ozorowski, G., Messmer, T., Briney, B., Voss, J.E., Kulp, D.W., Macauley, M.S., Sok, D., Pauthner, M., et al. Holes in the Glycan Shield of the Native HIV Envelope Are a Target of Trimer-Elicited Neutralizing Antibodies. Cell Rep. 16 (2016), 2327–2338.
32. McLellan, J.S., Pancera, M., Carrico, C., Gorman, J., Julien, J.-P., Khayat, R., Louder, R., Pejchal, R., Sastry, M., Dai, K., et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480 (2011), 336–343.
33. Mörner, A., Douagi, I., Forsell, M.N., Sundling, C., Dosenovic, P., O'Dell, S., Dey, B., Kwong, P.D., Voss, G., Thorstensson, R., et al. Human immunodeficiency virus type 1 env trimer immunization of macaques and impact of priming with viral vector or stabilized core protein. J. Virol. 83 (2009), 540–551.
34. Navis, M., Tran, K., Bale, S., Phad, G.E., Guenaga, J., Wilson, R., Soldemo, M., McKee, K., Sundling, C., Mascola, J., et al. HIV-1 receptor binding site-directed antibodies using a VH1-2 gene segment orthologue are activated by Env trimer immunization. PLoS Pathog., 10, 2014, e1004337.
35. Phad, G.E., Vázquez Bernat, N., Feng, Y., Ingale, J., Martinez Murillo, P.A., O'Dell, S., Li, Y., Mascola, J.R., Sundling, C., Wyatt, R.T., Karlsson Hedestam, G.B., Diverse antibody genetic and recognition properties revealed following HIV-1 envelope glycoprotein immunization. J. Immunol. 194 (2015), 5903–5914.
36. Poulsen, T.R., Jensen, A., Haurum, J.S., Andersen, P.S., Limits for antibody affinity maturation and repertoire diversification in hypervaccinated humans. J. Immunol. 187 (2011), 4229–4235.
37. Pritchard, L.K., Spencer, D.I., Royle, L., Bonomelli, C., Seabright, G.E., Behrens, A.J., Kulp, D.W., Menis, S., Krumm, S.A., Dunlop, D.C., et al. Glycan clustering stabilizes the mannose patch of HIV-1 and preserves vulnerability to broadly neutralizing antibodies. Nat. Commun., 6, 2015, 7479.
38. 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., 9, 2013, e1003618.
39. Sharma, S.K., de Val, N., Bale, S., Guenaga, J., Tran, K., Feng, Y., Dubrovskaya, V., Ward, A.B., Wyatt, R.T., Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Rep. 11 (2015), 539–550.
40. 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. 15 (2009), 866–870.
41. Stewart-Jones, G.B., Soto, C., Lemmin, T., Chuang, G.Y., Druz, A., Kong, R., Thomas, P.V., Wagh, K., Zhou, T., Behrens, A.J., et al. Trimeric HIV-1-Env Structures Define Glycan Shields from Clades A, B, and G. Cell 165 (2016), 813–826.
42. Sundling, C., Li, Y., Huynh, N., Poulsen, C., Wilson, R., O'Dell, S., Feng, Y., Mascola, J.R., Wyatt, R.T., Karlsson Hedestam, G.B., High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci. Transl. Med., 4, 2012, 142ra96.
43. Sundling, C., Phad, G., Douagi, I., Navis, M., Karlsson Hedestam, G.B., Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J. Immunol. Methods 386 (2012), 85–93.
44. Tiller, T., Meffre, E., Yurasov, S., Tsuiji, M., Nussenzweig, M.C., Wardemann, H., Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329 (2008), 112–124.
45. 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 111 (2014), E738–E747.
46. Voss, N.R., Yoshioka, C.K., Radermacher, M., Potter, C.S., Carragher, B., DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166 (2009), 205–213.
47. Walker, L.M., Phogat, S.K., Chan-Hui, P.Y., Wagner, D., Phung, P., Goss, J.L., Wrin, T., Simek, M.D., Fling, S., Mitcham, J.L., et al., Protocol G Principal Investigators. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (2009), 285–289.
48. Wei, X., Decker, J.M., Wang, S., Hui, H., Kappes, J.C., Wu, X., Salazar-Gonzalez, J.F., Salazar, M.G., Kilby, J.M., Saag, M.S., et al. Antibody neutralization and escape by HIV-1. Nature 422 (2003), 307–312.