Thermostability of Well-Ordered HIV Spikes Correlates with the Elicitation of Autologous Tier 2 Neutralizing Antibodies

PLoS Pathogens

Volumn 12, Issue 8, 2016, Pages

  Feng, Yu ^a,b   Tran, Karen ^a   Bale, Shridhar ^b   Kumar, Shailendra ^a   Guenaga, Javier ^a   Wilson, Richard ^a   de Val, Natalia ^b   Arendt, Heather ^c   DeStefano, Joanne ^c   Ward, Andrew B ^a,b   Wyatt, Richard T ^a,b  

^a Department of Integrative Structural and Computational Biology   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16055 SOSIP ANTIBODY; BG505 NFL ANTIBODY; BG505 SOSIP ANTIBODY; F105 ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; JRFL NFL ANTIBODY; JRFL SOSIP ANTIBODY; NEUTRALIZING ANTIBODY; PG16 ANTIBODY; PGT145 ANTIBODY; UNCLASSIFIED DRUG; VRC06 ANTIBODY; X LINK BG505 NFL ANTIBODY; X LINK JRFL NFL ANTIBODY; GLUTARALDEHYDE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; VIRUS ENVELOPE PROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN BINDING; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; CROSS LINKING; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; GUINEA PIG; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMAGE RECONSTRUCTION; IMMUNOGENICITY; NONHUMAN; SIZE EXCLUSION CHROMATOGRAPHY; THERMOSTABILITY; TRANSMISSION ELECTRON MICROSCOPY; VIRUS NEUTRALIZATION; ANIMAL; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; VACCINE IMMUNOGENICITY;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GLUTARAL; GUINEA PIGS; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNOGENICITY, VACCINE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

EID: 84984852104     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005767     Document Type: Article

References (48)

1. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 2002;420(6916):678–82. 12478295.
2. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, Molecular architecture of native HIV-1 gp120 trimers. Nature. 2008;455(7209):109–13. Epub 2008/08/01. doi: 10.1038/nature0715918668044; PubMed Central PMCID: PMC2610422.
3. Wyatt R, Sodroski J, The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science. 1998;280(5371):1884–8. 9632381.
4. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science. 2013;342(6165):1477–83. doi: 10.1126/science.124562524179159; PubMed Central PMCID: PMC3886632.
5. Sanders RW, Derking R, Cupo A, Julien JP, Yasmeen A, de Val N, 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(9):e1003618. doi: 10.1371/journal.ppat.100361824068931; PubMed Central PMCID: PMC3777863.
6. Guenaga J, de Val N, Tran K, Feng Y, Satchwell K, Ward AB, et al. Well-Ordered Trimeric HIV-1 Subtype B and C Soluble Spike Mimetics Generated by Negative Selection Display Native-like Properties. PLoS Pathog. 2015;11(1):e1004570. doi: 10.1371/journal.ppat.100457025569572; PubMed Central PMCID: PMC4287557.
7. Sharma SK, de Val N, Bale S, Guenaga J, Tran K, Feng Y, et al. Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Rep. 2015;11(4):539–50. doi: 10.1016/j.celrep.2015.03.04725892233; PubMed Central PMCID: PMCPMC4637274.
8. Lyumkis D, Julien JP, de Val N, Cupo A, Potter CS, Klasse PJ, et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science. 2013;342(6165):1484–90. doi: 10.1126/science.124562724179160; PubMed Central PMCID: PMC3954647.
9. Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature. 2014;514(7523):455–61. doi: 10.1038/nature1380825296255.
10. Sanders RW, van Gils MJ, Derking R, Sok D, Ketas TJ, Burger JA, et al. HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science. 2015;349(6244):aac4223. doi: 10.1126/science.aac422326089353; PubMed Central PMCID: PMCPMC4498988.
11. Schiffner T, de Val N, Russell RA, de Taeye SW, Torrents de la Pena A, Ozorowski G, et al. Chemical Cross-linking Stabilizes Native-Like HIV-1 Envelope Glycoprotein Trimer Antigens. J Virol. 2015. doi: 10.1128/JVI.01942-1526512083.
12. Schiffner T, Kong L, Duncan CJ, Back JW, Benschop JJ, Shen X, et al. Immune focusing and enhanced neutralization induced by HIV-1 gp140 chemical cross-linking. J Virol. 2013;87(18):10163–72. doi: 10.1128/JVI.01161-1323843636; PubMed Central PMCID: PMCPMC3754013.
13. Leaman DP, Lee JH, Ward AB, Zwick MB, Immunogenic Display of Purified Chemically Cross-Linked HIV-1 Spikes. J Virol. 2015;89(13):6725–45. doi: 10.1128/JVI.03738-1425878116; PubMed Central PMCID: PMCPMC4468504.
14. Yuan W, Bazick J, Sodroski J, Characterization of the multiple conformational States of free monomeric and trimeric human immunodeficiency virus envelope glycoproteins after fixation by cross-linker. J Virol. 2006;80(14):6725–37. doi: 10.1128/JVI.00118-0616809278; PubMed Central PMCID: PMCPMC1489074.
15. Guenaga J, Dubrovskaya V, de Val N, Sharma SK, Carrette B, Ward AB, et al. Structure-Guided Redesign Increases the Propensity of HIV Env To Generate Highly Stable Soluble Trimers. J Virol. 2015;90(6):2806–17. doi: 10.1128/JVI.02652-1526719252.
16. de Taeye SW, Ozorowski G, Torrents de la Pena A, Guttman M, Julien JP, van den Kerkhof TL, et al. Immunogenicity of Stabilized HIV-1 Envelope Trimers with Reduced Exposure of Non-neutralizing Epitopes. Cell. 2015;163(7):1702–15. doi: 10.1016/j.cell.2015.11.05626687358; PubMed Central PMCID: PMCPMC4732737.
17. Chakrabarti BK, Feng Y, Sharma SK, McKee K, Karlsson Hedestam GB, Labranche CC, et al. Robust neutralizing antibodies elicited by HIV-1 JRFL envelope glycoprotein trimers in nonhuman primates. J Virol. 2013;87(24):13239–51. doi: 10.1128/JVI.01247-1324067980; PubMed Central PMCID: PMC3838230.
18. Feng Y, Mckee K, Tran K, O'Dell S, Schmidt SD, Phogat A, et al. Biochemically Defined HIV-1 Envelope Glycoprotein Variant Immunogens Display Differential Binding and Neutralizing Specificities to the CD4-binding Site. J Biol Chem. 2012;287(8):5673–86. doi: 10.1074/jbc.M111.317776ISI:000300638000044.
19. Ingale J, Tran K, Kong L, Dey B, McKee K, Schief W, et al. Hyperglycosylated stable core immunogens designed to present the CD4 binding site are preferentially recognized by broadly neutralizing antibodies. J Virol. 2014;88(24):14002–16. doi: 10.1128/JVI.02614-1425253346; PubMed Central PMCID: PMCPMC4249138.
20. Sundling C, Forsell MN, O'Dell S, Feng Y, Chakrabarti B, Rao SS, et al. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. The J Exp Med. 2010;207(9):2003–17. Epub 2010/08/04. doi: 10.1084/jem.2010002520679401; PubMed Central PMCID: PMC2931166.
21. Habeeb AJ, Hiramoto R, Reaction of proteins with glutaraldehyde. Arch Biochem Biophys. 1968;126(1):16–26. 4174905.
22. Binley JM, Sanders RW, Master A, Cayanan CS, Wiley CL, Schiffner L, et al. Enhancing the proteolytic maturation of human immunodeficiency virus type 1 envelope glycoproteins. J Virol. 2002;76(6):2606–16. 11861826.
23. Phad GE, Vazquez Bernat N, Feng Y, Ingale J, Martinez Murillo PA, O'Dell S, et al. Diverse antibody genetic and recognition properties revealed following HIV-1 envelope glycoprotein immunization. J Immunol. 2015;194(12):5903–14. doi: 10.4049/jimmunol.150012225964491; PubMed Central PMCID: PMCPMC4458414.
24. Forsell MNE, Dey B, Morner A, Svehla K, O'dell S, Hogerkorp CM, et al. B Cell Recognition of the Conserved HIV-1 Co-Receptor Binding Site Is Altered by Endogenous Primate CD4. PLoS Pathog. 2008;4(10). doi: 10.1371/journal.ppat.1000171ISI:000261481100005.
25. Li Y, Svehla K, Mathy NL, Voss G, Mascola JR, Wyatt R, Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants. J Virol. 2006;80(3):1414–26. 16415019.
26. Forsell MN, Schief WR, Wyatt RT, Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr Opin HIV AIDS. 2009;4(5):380–7. Epub 2010/01/06. doi: 10.1097/COH.0b013e32832edc1920048701.
27. Beddows S, Franti M, Dey AK, Kirschner M, Iyer SP, Fisch DC, et al. A comparative immunogenicity study in rabbits of disulfide-stabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120. Virology. 2007;360(2):329–40. Epub 2006/11/28. doi: 10.1016/j.virol.2006.10.03217126869.
28. Ringe RP, Sanders RW, Yasmeen A, Kim HJ, Lee JH, Cupo A, et al. Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation. Proc Natl Acad Sci USA. 2013;110(45):18256–61. doi: 10.1073/pnas.131435111024145402; PubMed Central PMCID: PMC3831437.
29. Tran K, Poulsen C, Guenaga J, de Val N, Wilson R, Sundling C, 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(7):E738–47. doi: 10.1073/pnas.131951211124550318; PubMed Central PMCID: PMC3932900.
30. Spoerl E, Wollensak G, Reber F, Pillunat L, Cross-linking of human amniotic membrane by glutaraldehyde. Ophthalmic Res. 2004;36(2):71–7. doi: 10.1159/00007688415017101.
31. Manji RA, Lee W, Cooper DK, Xenograft bioprosthetic heart valves: Past, present and future. Int J Surg. 2015. doi: 10.1016/j.ijsu.2015.07.00926190838.
32. Dardik H, Wengerter K, Qin F, Pangilinan A, Silvestri F, Wolodiger F, et al. Comparative decades of experience with glutaraldehyde-tanned human umbilical cord vein graft for lower limb revascularization: an analysis of 1275 cases. J Vasc Surg. 2002;35(1):64–71. 11802134.
33. Gupta RK, Sharma SB, Ahuja S, Saxena SN, Glutaraldehyde inactivated pertussis vaccine: a safe vaccine in the innocuity test. Vaccine. 1987;5(2):102–4. 2440196.
34. Garcia-Selles J, Pascual A, Funes E, Pagan JA, Lopez JD, Negro JM, et al. Clinical efficacy and safety of a depigmented and glutaraldehyde polymerized therapeutic vaccine of Parietaria judaica. Allergol Immunopathol (Madr). 2003;31(2):63–9. 12646120.
35. Riechelmann H, Schmutzhard J, van der Werf JF, Distler A, Kleinjans HA, Efficacy and safety of a glutaraldehyde-modified house dust mite extract in allergic rhinitis. Am J Rhinol Allergy. 2010;24(5):e104–9. doi: 10.2500/ajra.2010.24.350821244725.
36. Kwon YD, Pancera M, Acharya P, Georgiev IS, Crooks ET, Gorman J, et al. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat Struct Mol Biol. 2015;22(7):522–31. doi: 10.1038/nsmb.305126098315; PubMed Central PMCID: PMCPMC4706170.
37. Stamatatos L, Morris L, Burton DR, Mascola JR, Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine?Nat Med. 2009;15(8):866–70. Epub 2009/06/16. [pii] doi: 10.1038/nm.194919525964.
38. Landais E, Huang X, Havenar-Daughton C, Murrell B, Price MA, Wickramasinghe L, et al. Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort. PLoS Pathog. 2016;12(1):e1005369. doi: 10.1371/journal.ppat.100536926766578; PubMed Central PMCID: PMCPMC4713061.
39. Kong L, Lee JH, Doores KJ, Murin CD, Julien JP, McBride R, et al. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol. 2013;20(7):796–803. doi: 10.1038/nsmb.259423708606; PubMed Central PMCID: PMC3823233.
40. Suloway C, Pulokas J, Fellmann D, Cheng A, Guerra F, Quispe J, et al. Automated molecular microscopy: the new Leginon system. J Struct Biol. 2005;151(1):41–60. doi: 10.1016/j.jsb.2005.03.01015890530.
41. Lander GC, Stagg SM, Voss NR, Cheng A, Fellmann D, Pulokas J, et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J Struct Biol. 2009;166(1):95–102. 19263523; PubMed Central PMCID: PMCPMC2775544.
42. Voss NR, Yoshioka CK, Radermacher M, Potter CS, Carragher B, DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J Struct Biol. 2009;166(2):205–13. 19374019; PubMed Central PMCID: PMCPMC2768396.
43. Sorzano CO, Bilbao-Castro JR, Shkolnisky Y, Alcorlo M, Melero R, Caffarena-Fernandez G, et al. A clustering approach to multireference alignment of single-particle projections in electron microscopy. J Struct Biol. 2010;171(2):197–206. doi: 10.1016/j.jsb.2010.03.01120362059; PubMed Central PMCID: PMCPMC2893300.
44. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M, A new generation of the IMAGIC image processing system. J Struct Biol. 1996;116(1):17–24. doi: 10.1006/jsbi.1996.00048742718.
45. Pugach P, Ozorowski G, Cupo A, Ringe R, Yasmeen A, de Val N, et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env gene. J Virol. 2015;89(6):3380–95. doi: 10.1128/JVI.03473-1425589637; PubMed Central PMCID: PMCPMC4337520.
46. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, et al. EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol. 2007;157(1):38–46. doi: 10.1016/j.jsb.2006.05.00916859925.
47. Ludtke SJ, Baldwin PR, Chiu W, EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol. 1999;128(1):82–97. doi: 10.1006/jsbi.1999.417410600563.
48. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–12. doi: 10.1002/jcc.2008415264254.