Improving the Immunogenicity of Native-like HIV-1 Envelope Trimers by Hyperstabilization

Cell Reports

Volumn 20, Issue 8, 2017, Pages 1805-1817

  Torrents de la Peña, Alba ^a   Julien, Jean Philippe ^b,i,j   de Taeye, Steven W ^a   Garces, Fernando ^b,k   Guttman, Miklos ^c   Ozorowski, Gabriel ^b   Pritchard, Laura K ^d   Behrens, Anna Janina ^d   Go, Eden P ^e   Burger, Judith A ^a   Schermer, Edith E ^a   Sliepen, Kwinten ^a   Ketas, Thomas J ^f   Pugach, Pavel ^f   Yasmeen, Anila ^f   Cottrell, Christopher A ^b   Torres, Jonathan L ^b   Vavourakis, Charlotte D ^g   van Gils, Marit J ^a   LaBranche, Celia ^h   Montefiori, David C ^h   Desaire, Heather ^e   Crispin, Max ^d   Klasse, Per Johan ^f   Lee, Kelly K ^c   Moore, John P ^f   Ward, Andrew B ^b   Wilson, Ian A ^b   Sanders, Rogier W ^a,f   more..

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF KANSAS   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

^g UNIVERSITY OF AMSTERDAM   (Netherlands)

^h DUKE UNIVERSITY MEDICAL CENTER   (United States)

ⁱ HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^j UNIVERSITY OF TORONTO   (Canada)

^k AMGEN INC   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY TITER; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; VIRUS ENVELOPE; ANIMAL; HUMAN; IMMUNOLOGY; LEPORIDAE;

ANIMALS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; RABBITS;

EID: 85028346224     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.07.077     Document Type: Article

References (38)

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., et al. 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. 74 (2000), 627–643.
2. Bulleid, N.J., van Lith, M., Redox regulation in the endoplasmic reticulum. Biochem. Soc. Trans. 42 (2014), 905–908.
3. Camacho, C.J., Thirumalai, D., Modeling the role of disulfide bonds in protein-folding: entropic barriers and pathways. Proteins 22 (1995), 27–40.
4. Cheng, C., Pancera, M., Bossert, A., Schmidt, S.D., Chen, R., Chen, X., Druz, A., Narpala, S., Doria-Rose, N.A., McDermott, A.B., et al. Immunogenicity of a prefusion HIV-1-envelope trimer in complex with a quaternary-specific antibody. J. Virol. 90 (2015), 2740–2755.
5. Creighton, T.E., Disulphide bonds and protein stability. BioEssays 8 (1988), 57–63.
6. de Taeye, S.W., Ozorowski, G., Torrents de la Peña, A., Guttman, M., Julien, J.P., van den Kerkhof, T.L.G.M., Burger, J.A., Pritchard, L.K., Pugach, P., Yasmeen, A., et al. Immunogenicity of stabilized HIV-1 Envelope trimers with reduced exposure of non-neutralizing epitopes. Cell 163 (2015), 1702–1715.
7. Derking, R., Ozorowski, G., Sliepen, K., Yasmeen, A., Cupo, A., Torres, J.L., Julien, J.P., Lee, J.H., van Montfort, T., de Taeye, S.W., et al. Comprehensive antigenic map of a cleaved soluble HIV-1 envelope trimer. PLoS Pathog., 11, 2015, e1004767.
8. Feng, Y., Tran, K., Bale, S., Kumar, S., Guenaga, J., Wilson, R., de Val, N., Arendt, H., DeStefano, J., Ward, A.B., et al. Thermostability of well-ordered HIV spikes correlates with the elicitation of autologous tier 2 neutralizing antibodies. PLoS Pathog., 12, 2016, e1005767.
9. Garces, F., Lee, J.H., de Val, N., Torrents de la Peña, A., 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.
10. Goo, L., Chohan, V., Nduati, R., Overbaugh, J., Early development of broadly neutralizing antibodies in HIV-1-infected infants. Nat. Med. 20 (2014), 655–658.
11. 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., 11, 2015, e1004570.
12. Guttman, M., Garcia, N.K., Cupo, A., Matsui, T., Julien, J.P., Sanders, R.W., Wilson, I.A., Moore, J.P., Lee, K.K., CD4-induced activation in a soluble HIV-1 Env trimer. Structure 22 (2014), 974–984.
13. Huang, J., Kang, B.H., Pancera, M., Lee, J.H., Tong, T., Feng, Y., Georgiev, I.S., Chuang, G.Y., Druz, A., Doria-Rose, N.A., et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-120 interface. Nature, 515, 2014, 138.
14. 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 342 (2013), 1477–1483.
15. Julien, J.P., Sok, D., Khayat, R., Lee, J.H., Doores, K.J., Walker, L.M., Ramos, A., Diwanji, D.C., Pejchal, R., Cupo, A., et al. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog., 9, 2013, e1003342.
16. Julien, J.P., Lee, J.H., Ozorowski, G., Hua, Y., Torrents de la Peña, A., de Taeye, S.W., Nieusma, T., Cupo, A., Yasmeen, A., Golabek, M., et al. Design and structure of two HIV-1 clade C SOSIP.664 trimers that increase the arsenal of native-like Env immunogens. Proc. Natl. Acad. Sci. USA 112 (2015), 1–6.
17. Karp, C.L., Lans, D., Esparza, J., Edson, E.B., Owen, K.E., Wilson, C.B., Heaton, P.M., Levine, O.S., Rao, R., Evaluating the value proposition for improving vaccine thermostability to increase vaccine impact in low and middle-income countries. Vaccine 33 (2015), 3471–3479.
18. Klasse, P.J., Labranche, C.C., Ketas, T.J., Ozorowski, G., Cupo, A., Pugach, P., Ringe, R.P., Golabek, M., van Gils, M.J., Guttman, M., et al. Sequential and simultaneous immunization of rabbits with HIV-1 envelope glycoprotein SOSIP.664 trimers from clades A, B and C. PLoS Pathog., 12, 2016, e1005864.
19. Kong, L., He, L., de Val, N., Vora, N., Morris, C.D., Azadnia, P., Sok, D., Zhou, B., Burton, D.R., Ward, A.B., et al. Uncleaved prefusion-optimized gp140 trimers derived from analysis of HIV-1 envelope metastability. Nat. Commun. 7 (2016), 1–15.
20. Kwon, Y.D., Pancera, M., Acharya, P., Georgiev, I.S., Crooks, E.T., Gorman, J., Joyce, M.G., Guttman, M., Ma, X., Narpala, S., et al. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat. Struct. Mol. Biol. 22 (2015), 522–531.
21. Lee, J.H., Ozorowski, G., Ward, A.B., Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351 (2016), 1043–1048.
22. Liszka, M.J., Clark, M.E., Schneider, E., Clark, D.S., Nature versus nurture: Developing enzymes that function under extreme conditions. Annu. Rev. Chem. Biomol. Eng. 3 (2012), 77–102.
23. 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 342 (2013), 1484–1490.
24. 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.
25. McLellan, J.S., Chen, M., Leung, S., Graepel, K.W., Du, X., Yang, Y., Zhou, T., Baxa, U., Yasuda, E., Beaumont, T., et al. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340 (2013), 1113–1117.
26. 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 514 (2014), 455–461.
27. Pritchard, L.K., Vasiljevic, S., Ozorowski, G., Seabright, G.E., Cupo, A., Ringe, R., Kim, H.J., Sanders, R.W., Doores, K.J., Burton, D.R., et al. Structural constraints determine the glycosylation of HIV-1 envelope trimers. Cell Rep. 11 (2015), 1604–1613.
28. Pritchard, L.K., Harvey, D.J., Bonomelli, C., Crispin, M., Doores, K.J., Cell- and protein-directed glycosylation of native cleaved HIV-1 envelope. J. Virol. 89 (2015), 8932–8944.
29. Pugach, P., Ozorowski, G., Cupo, A., Ringe, R., Yasmeen, A., de Val, N., Derking, R., Kim, H.J., Korzun, J., Golabek, M., et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env gene. J. Virol. 89 (2015), 3380–3395.
30. Sanders, R.W., Moore, J.P., HIV: A stamp on the envelope. Nature 514 (2014), 437–438.
31. Sanders, R.W., Vesanen, M., Schuelke, N., Schiffner, L., Kalyanaraman, R., Berkhout, B., Maddon, P.J., Olson, W.C., Lu, M., Moore, J.P., et al. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 76 (2002), 8875–8889.
32. 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.
33. Sanders, R.W., van Gils, M.J., Derking, R., Sok, D., Ketas, T.J., Burger, J.A., Ozorowski, G., Cupo, A., Simonich, C., Goo, L., et al. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science, 349, 2015, aac4223.
34. Scharf, L., Wang, H., Gao, H., Chen, S., McDowall, A.W., Bjorkman, P.J., Broadly neutralizing antibody 8ANC195 recognizes closed and open states of HIV-1 Env. Cell 162 (2015), 1379–1390.
35. Steichen, J.M., Kulp, D.W., Tokatlian, T., Escolano, A., Dosenovic, P., Stanfield, R.L., McCoy, L.E., Ozorowski, G., Hu, X., Kalyuzhniy, O., et al. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45 (2016), 483–496.
36. 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.
37. van Gils, M.J., Sanders, R.W., Broadly neutralizing antibodies against HIV-1: templates for a vaccine. Virology 435 (2013), 46–56.
38. Yasmeen, A., Ringe, R., Derking, R., Cupo, A., Julien, J.P., Burton, D.R., Ward, A.B., Wilson, I.A., Sanders, R.W., Moore, J.P., Klasse, J.P., Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits. Retrovirology, 11, 2014, 41.