Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles

Nature Communications

Volumn 7, Issue , 2016, Pages

  He, Linling ^a   De Val, Natalia ^a   Morris, Charles D ^a   Vora, Nemil ^a   Thinnes, Therese C ^a   Kong, Leopold ^a   Azadnia, Parisa ^a   Sok, Devin ^a   Zhou, Bin ^a   Burton, Dennis R ^a,b   Wilson, Ian A ^a   Nemazee, David ^a   Ward, Andrew B ^a   Zhu, Jiang ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROADLY NEUTRALIZING ANTIBODY; FERRITIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS 1 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MONOMER; NANOPARTICLE; NEUTRALIZING ANTIBODY; PROTEIN V1V2; UNCLASSIFIED DRUG; VACCINE;

ANTIBODY; ANTIGEN; ELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; NANOPARTICLE; VACCINE;

ANTIGENICITY; ARTICLE; B LYMPHOCYTE; CONFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOGENICITY; SPIKE; VIRUS LIKE AGENT; DRUG DESIGN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

DRUG DESIGN; HIV-1; NANOPARTICLES; VACCINES;

EID: 84976636170     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12041     Document Type: Article

References (69)

1. Burton, D. R. et al. A blueprint for HIV vaccine discovery. Cell Host Microbe 12, 396-407 (2012).
2. Burton, D. R., Mascola, J. R. Antibody responses to envelope glycoproteins in HIV-1 infection. Nat. Immunol. 16, 571-576 (2015).
3. Kwong, P. D., Mascola, J. R., Nabel, G. J. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13, 693-701 (2013).
4. Kwong, P. D., Mascola, J. R. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37, 412-425 (2012).
5. Wyatt, R., Sodroski, J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1884-1888 (1998).
6. Sanders, R. W. 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, e1003618 (2013).
7. Yasmeen, A. et al. Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits. Retrovirology 11, 41 (2014).
8. Derking, R. et al. Comprehensive antigenic map of a cleaved soluble HIV-1 envelope trimer. PLoS Pathog. 11, e1004767 (2015).
9. Julien, J.-P. et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342, 1477-1483 (2013).
10. Lyumkis, D. et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484-1490 (2013).
11. Pancera, M. et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455-461 (2014).
12. Julien, J.-P. et al. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc. Natl Acad. Sci. USA 110, 4351-4356 (2013).
13. Falkowska, E. et al. Broadly neutralizing HIV antibodies define a glycandependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40, 657-668 (2014).
14. Blattner, C. et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40, 669-680 (2014).
15. Scharf, L. et al. Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 envelope spike. Cell Rep 7, 785-795 (2014).
16. Huang, J. et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491, 406-412 (2012).
17. Sok, D. et al. Recombinant HIV envelope trimer selects for quaternarydependent antibodies targeting the trimer apex. Proc. Natl Acad. Sci. USA 111, 17624-17629 (2014).
18. Pugach, P. et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B Env gene. J. Virol. 89, 3380-3395 (2015).
19. Julien, J.-P. 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, 11947-11952 (2015).
20. Do Kwon, Y. et al. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat. Struct. Mol. Biol. 22, 522-531 (2015).
21. Sanders, R. W. et al. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 349, aac4223 (2015).
22. Sharma, S. K. et al. Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Rep. 11, 539-550 (2015).
23. Georgiev, I. S. et al. Single-chain soluble BG505.SOSIP gp140 trimers as structural and antigenic mimics of mature closed HIV-1 Env. J. Virol. 89, 5318-5329 (2015).
24. Ludwig, C., Wagner, R. Virus-like particles-universal molecular toolboxes. Curr. Opin. Biotechnol. 18, 537-545 (2007).
25. Jennings, G. T., Bachmann, M. F. Coming of age of virus-like particle vaccines. Biol. Chem. 389, 521-536 (2008).
26. Kushnir, N., Streatfield, S. J., Yusibov, V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 31, 58-83 (2012).
27. Rodriguez-Limas, W. A., Sekar, K., Tyo, K. E. J. Virus-like particles: the future of microbial factories and cell-free systems as platforms for vaccine development. Curr. Opin. Biotechnol. 24, 1089-1093 (2013).
28. Zhao, Q., Li, S., Yu, H., Xia, N., Modis, Y. Virus-like particle-based human vaccines: quality assessment based on structural and functional properties. Trends Biotechnol. 31, 654-663 (2013).
29. Dintzis, R. Z., Vogelstein, B., Dintzis, H. M. Specific cellular stimulation in the primary immune response: experimental test of a quantized model. Proc. Natl Acad. Sci. USA 79, 884-888 (1982).
30. Schiller, J., Chackerian, B. Why HIV virions have low numbers of envelope spikes: implications for vaccine development. PLoS Pathog. 10, e1004254 (2014).
31. Lua, L. H. L. et al. Bioengineering virus-like particles as vaccines. Biotechnol. Bioeng. 111, 425-440 (2014).
32. Kanekiyo, M. et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499, 102-106 (2013).
33. Yassine, H. M. et al. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat. Med. 21, 1065-1070 (2015).
34. Zhou, T. et al. Transplanting supersites of HIV-1 vulnerability. PLoS ONE 9, e00991 (2014).
35. He, L. et al. Approaching rational epitope vaccine design for hepatitis C virus with meta-server and multivalent scaffolding. Sci. Rep. 5, 12501 (2015).
36. Sliepen, K. et al. Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology 12, 82 (2015).
37. Jardine, J. G. et al. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science 349, 156-161 (2015).
38. Jardine, J. et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340, 711-716 (2013).
39. Krebs, S. J. et al. Multimeric scaffolds displaying the HIV-1 envelope MPER induce MPER-specific antibodies and cross-neutralizing antibodies when co-immunized with gp160 DNA. PLoS ONE 9, e113463 (2014).
40. Bachmann, M. F., Zinkernagel, R. M. The influence of virus structure on antibody responses and virus serotype formation. Immunol. Today 17, 553-558 (1996).
41. Bachmann, M. F., Hengartner, H., Zinkernagel, R. M. T helper cellindependent neutralizing B cell response against vesicular stomatitis virus: role of antigen patterns in B cell induction? Eur. J. Immunol. 25, 3445-3451 (1995).
42. Thyagarajan, R., Arunkumar, N., Song, W. X. Polyvalent antigens stabilize B cell antigen receptor surface signaling microdomains. J. Immunol. 170, 6099-6106 (2003).
43. Kong, L. et al. Uncleaved prefusion-optimized gp140 trimers derived from analysis of HIV-1 envelope metastability. Nat. Commun. 7, 12040 (2016).
44. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
45. Walker, L. M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
46. Bonsignori, M. et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 85, 9998-10009 (2011).
47. Walker, L. M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
48. Doria-Rose, N. A. et al. A short segment of the HIV-1 gp120 V1/V2 region is a major determinant of resistance to V1/V2 neutralizing antibodies. J. Virol. 86, 8319-8323 (2012).
49. Andrabi, R. et al. Identification of common features in prototype broadly neutralizing antibodies to HIV envelope V2 apex to facilitate vaccine design. Immunity 43, 959-973 (2015).
50. Pancera, M. et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat. Struct. Mol. Biol. 20, 804-813 (2013).
51. Wu, X. et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
52. Falkowska, E. et al. PGV04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce conformational changes characteristic of CD4. J. Virol. 86, 4394-4403 (2012).
53. Dosenovic, P. et al. Immunization for HIV-1 broadly neutralizing antibodies in human Ig knockin mice. Cell 161, 1505-1515 (2015).
54. Zhang, X. F., Meining, W., Fischer, M., Bacher, A., Ladenstein, R. X-ray structure analysis and crystallographic refinement of lumazine synthase from the hyperthermophile Aquifex aeolicus at 1.6 angstrom resolution: determinants of thermostability revealed from structural comparisons. J. Mol. Biol. 306, 1099-1114 (2001).
55. Izard, T. et al. Principles of quasi-equivalence and Euclidean geometry govern the assembly of cubic and dodecahedral cores of pyruvate dehydrogenase complexes. Proc. Natl Acad. Sci. USA 96, 1240-1245 (1999).
56. Fifis, T. et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J. Immunol. 173, 3148-3154 (2004).
57. Smith, D. H. et al. Comparative immunogenicity of HIV-1 clade C envelope proteins for prime/boost studies. PLoS ONE 5, e12076 (2010).
58. Zhao, D. et al. Enterovirus71 virus-like particles produced from insect cells and purified by multistep chromatography elicit strong humoral immune responses in mice. J. Appl. Microbiol. 119, 1196-1205 (2015).
59. Huang, J. et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 515, 138-142 (2014).
60. Zhou, T. et al. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39, 245-258 (2013).
61. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
62. Ota, T. et al. Anti-HIV B cell lines as candidate vaccine biosensors. J. Immunol. 189, 4816-4824 (2012).
63. Mascola, J. R. The modern era of HIV-1 vaccine development. Science 349, 139-140 (2015).
64. Crooks, E. T. et al. Vaccine-elicited tier 2 HIV-1 neutralizing antibodies bind to quaternary epitopes involving glycan-deficient patches proximal to the CD4 binding site. PLoS Pathog. 11, e1004932 (2015).
65. Tong, T., Crooks, E. T., Osawa, K., Binley, J. M. HIV-1 virus-like particles bearing pure Env trimers expose neutralizing epitopes but occlude nonneutralizing epitopes. J. Virol. 86, 3574-3587 (2012).
66. Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41-60 (2005).
67. Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95-102 (2009).
68. Sorzano, C. O. S. et al. A clustering approach to multireference alignment of single-particle projections in electron microscopy. J. Struct. Biol. 171, 197-206 (2010).
69. vanHeel,M., Harauz, G., Orlova, E. V., Schmidt, R., Schatz,M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).