Discrete partitioning of HIV-1 Env forms revealed by viral capture

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Stieh, Daniel J ^a   King, Deborah F ^b   Klein, Katja ^b   Aldon, Yoann ^b   McKay, Paul F ^b   Shattock, Robin J ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Envelope glycoprotein; HIV 1; Monoclonal antibody; Viral heterogeneity

Indexed keywords

GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; NON NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; GLYCOPROTEIN GP 160; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PROTEIN BINDING;

ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; ASSAY; CONTROLLED STUDY; DEPLETION; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNO BEAD VIRAL CAPTURE ASSAY; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; VIRION; VIRUS NEUTRALIZATION; VIRUS PARTICLE; CHEMISTRY; HUMAN; IMMUNOASSAY; IMMUNOLOGY; ISOLATION AND PURIFICATION; PHYSIOLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP160; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; IMMUNOASSAY; PROTEIN BINDING; VIRION;

EID: 84960315866     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-015-0207-z     Document Type: Article

References (60)

1. Haynes BF, Moody MA, Liao HX, Verkoczy L, Tomaras GD. B cell responses to HIV-1 infection and vaccination: pathways to preventing infection. Trends Mol Med. 2011;17(2):108-16.
2. McMichael AJ, Rowland-Jones SL. Cellular immune responses to HIV. Nature. 2001;410(6831):980-7.
3. 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.
4. Levesque MC, Moody MA, Hwang KK, Marshall DJ, Whitesides JF, Amos JD, Gurley TC, Allgood S, Haynes BB, Vandergrift NA, et al. Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLoS Med. 2009;6(7):e1000107.
5. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, Chavez LL, Decamp AC, Parks RJ, Ashley VC, Lucas JT, et al. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J Virol. 2008;82(24):12449-63.
6. Davis KL, Gray ES, Moore PL, Decker JM, Salomon A, Montefiori DC, Graham BS, Keefer MC, Pinter A, Morris L, et al. High titer HIV-1 V3-specific antibodies with broad reactivity but low neutralizing potency in acute infection and following vaccination. Virology. 2009;387(2):414-26.
7. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science. 2009;326(5950):285-9.
8. Finzi A, Xiang SH, Pacheco B, Wang L, Haight J, Kassa A, Danek B, Pancera M, Kwong PD, Sodroski J. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol Cell. 2010;37(5):656-67.
9. Earl PL, Moss B, Doms RW. Folding, interaction with Grp78-Bip, assembly, and transport of the human-immunodeficiency-virus type-1 envelope protein. J Virol. 1991;65(4):2047-55.
10. Fenouillet E, Gluckman JC. Immunological analysis of human-immunodeficiency-virus type-1 envelope glycoprotein proteolytic cleavage. Virology. 1992;187(2):825-8.
11. Dubay JW, Shin HJ, Dong JY, Roberts S, Hunter E. Structure-function analysis of the HIV glycoprotein. Adv Exp Med Biol. 1991;303:39-46.
12. Hunter E, Swanstrom R. Retrovirus envelope glycoproteins. Curr Top Microbiol Immunol. 1990;157:187-253.
13. Moore PL, Crooks ET, Porter L, Zhu P, Cayanan CS, Grise H, Corcoran P, Zwick MB, Franti M, Morris L, et al. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J Virol. 2006;80(5):2515-28.
14. Herrera C, Klasse PJ, Kibler CW, Michael E, Moore JP, Beddows S. Dominant-negative effect of hetero-oligomerization on the function of the human immunodeficiency virus type 1 envelope glycoprotein complex. Virology. 2006;351(1):121-32.
15. Poignard P, Moulard M, Golez E, Vivona V, Franti M, Venturini S, Wang M, Parren PW, Burton DR. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J Virol. 2003;77(1):353-65.
16. Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, Burton DR, Crispin M, Scanlan CN. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci USA. 2010;107(31):13800-5.
17. Li H, Xu CF, Blais S, Wan Q, Zhang HT, Landry SJ, Hioe CE. Proximal glycans outside of the epitopes regulate the presentation of HIV-1 envelope gp120 helper epitopes. J Immunol. 2009;182(10):6369-78.
18. Bonomelli C, Doores KJ, Dunlop DC, Thaney V, Dwek RA, Burton DR, Crispin M, Scanlan CN. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One. 2011;6(8):e23521.
19. Kwong PD, Wyatt R, Sattentau QJ, Sodroski J, Hendrickson WA. Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J Virol. 2000;74(4):1961-72.
20. 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.
21. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, Kong L, Kwon YD, Stuckey J, Zhou T, Robinson JE, et al. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci USA. 2010;107(3):1166-71.
22. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, Zwick MB, Phogat SK, Poignard P, Burton DR. A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog. 2010;6(8):e1001028.
23. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science. 2010;329(5993):856-61.
24. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, Xiang SH, Yang X, Zhang MY, Zwick MB, Arthos J, et al. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature. 2007;445(7129):732-7.
25. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, Finzi A, Kwon YD, Scheid JF, Shi W, Xu L, et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science. 2010;329(5993):811-7.
26. Klein F, Gaebler C, Mouquet H, Sather DN, Lehmann C, Scheid JF, Kraft Z, Liu Y, Pietzsch J, Hurley A, et al. Broad neutralization by a combination of antibodies recognizing the CD4 binding site and a new conformational epitope on the HIV-1 envelope protein. J Exp Med. 2012;209(8):1469-79.
27. Burton DR, Mascola JR. Antibody responses to envelope glycoproteins in HIV-1 infection. Nat Immunol. 2015;16(6):571-6.
28. Muster T, Guinea R, Trkola A, Purtscher M, Klima A, Steindl F, Palese P, Katinger H. Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J Virol. 1994;68(6):4031-4.
29. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, Xia SM, Rits-Volloch S, Sun L, Harrison SC, Haynes BF, et al. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc Natl Acad Sci USA. 2009;106(48):20234-9.
30. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, Steenbeke TD, Venturi M, Chaiken I, Fung M, et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 2002;420(6916):678-82.
31. Huang JH, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature. 2012;491(7424):406-12.
32. Parren PWHI, Gauduin MC, Koup RA, Poignard P, Fisicaro P, Burton DR, Sattentau QJ. Relevance of the antibody response against human immunodeficiency virus type 1 envelope to vaccine design. Immunol Lett. 1997;57(1-3):105-12.
33. Ackerman ME, Dugast AS, McAndrew EG, Tsoukas S, Licht AF, Irvine DJ, Alter G. Enhanced phagocytic activity of hiv-specific antibodies correlates with natural production of immunoglobulins with skewed affinity for Fc gamma R2a and Fc gamma R2b. J Virol. 2013;87(10):5468-76.
34. Kramberger P, Ciringer M, Strancar A, Peterka M. Evaluation of nanoparticle tracking analysis for total virus particle determination. Virol J. 2012;9:265.
35. Leaman DP, Kinkead H, Zwick MB. In-solution virus capture assay helps deconstruct heterogeneous antibody recognition of human immunodeficiency virus type 1. J Virol. 2010;84(7):3382-95.
36. Liu P, Williams LD, Shen X, Bonsignori M, Vandergrift NA, Overman RG, Moody MA, Liao HX, Stieh DJ, McCotter KL, et al. Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity. J Virol. 2014;88(9):5165-70.
37. Hulme EC, Trevethick MA. Ligand binding assays at equilibrium: validation and interpretation. Br J Pharmacol. 2010;161(6):1219-37.
38. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, Ratner L, Kappes JC, Shaw GM, Hunter E. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol. 2000;74(18):8358-67.
39. Trubey CM, Chertova E, Coren LV, Hilburn JM, Hixson CV, Nagashima K, Lifson JD, Ott DE. Quantitation of HLA class II protein incorporated into human immunodeficiency type 1 virions purified by anti-CD45 immunoaffinity depletion of microvesicles. J Virol. 2003;77(23):12699-709.
40. Cantin R, Martin G, Tremblay MJ. A novel virus capture assay reveals a differential acquisition of host HLA-DR by clinical isolates of human immunodeficiency virus type 1 expanded in primary human cells depending on the nature of producing cells and the donor source. J Gen Virol. 2001;82:2979-87.
41. Chakrabarti BK, Pancera M, Phogat S, O'Dell S, McKee K, Guenaga J, Robinson J, Mascola J, Wyatt RT. HIV type 1 env precursor cleavage state affects recognition by both neutralizing and nonneutralizing gp41 antibodies. Aids Res Hum Retrovir. 2011;27(8):877-87.
42. Chakrabarti BK, Walker LM, Guenaga JF, Ghobbeh A, Poignard P, Burton DR, Wyatt RT. Direct antibody access to the HIV-1 membrane-proximal external region positively correlates with neutralization sensitivity. J Virol. 2011;85(16):8217-26.
43. Ruprecht CR, Krarup A, Reynell L, Mann AM, Brandenberg OF, Berlinger L, Abela IA, Regoes RR, Gunthard HF, Rusert P, et al. MPER-specific antibodies induce gp120 shedding and irreversibly neutralize HIV-1. J Exp Med. 2011;208(3):439-54.
44. Chertova E, Bess JW Jr, Crise BJ, Sowder IR, Schaden TM, Hilburn JM, Hoxie JA, Benveniste RE, Lifson JD, Henderson LE, et al. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol. 2002;76(11):5315-25.
45. Agrawal N, Leaman DP, Rowcliffe E, Kinkead H, Nohria R, Akagi J, Bauer K, Du SX, Whalen RG, Burton DR, et al. Functional stability of unliganded envelope glycoprotein spikes among isolates of human immunodeficiency virus type 1 (HIV-1). PLoS One. 2011;6(6):e21339.
46. Joyner AS, Willis JR, Crowe JE, Aiken C. Maturation-induced cloaking of neutralization epitopes on HIV-1 particles. Plos Pathogens 2011;7(9):e1002234.
47. Chojnacki J, Staudt T, Glass B, Bingen P, Engelhardt J, Anders M, Schneider J, Muller B, Hell SW, Krausslich HG. Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science. 2012;338(6106):524-8.
48. Crooks ET, Tong T, Osawa K, Binley JM. Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected. J Virol. 2011;85(12):5825-39.
49. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse PJ, Burton DR, Sanders RW, Moore JP, et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science. 2013;342(6165):1477-83.
50. Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, Huang J, Acharya P, Chuang GY, Ofek G, et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature. 2014;514(7523):455-61.
51. Yasmeen A, Ringe R, Derking R, Cupo A, Julien JP, Burton DR, Ward AB, Wilson IA, Sanders RW, Moore JP, 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. 2014;11:41.
52. Alsahafi N, Debbeche O, Sodroski J, Finzi A. Effects of the I559P gp41 change on the conformation and function of the human immunodeficiency virus (HIV-1) membrane envelope glycoprotein trimer. PLoS One. 2015;10(4):e0122111.
53. Pugach P, Ozorowski G, Cupo A, Ringe R, Yasmeen A, de Val N, Derking R, Kim HJ, Korzun J, Golabek M M, et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B Env gene. J Virol. 2015;89(6):3380-95.
54. Tong T, Crooks ET, Osawa K, Binley JM. HIV-1 virus-like particles bearing pure env trimers expose neutralizing epitopes but occlude nonneutralizing epitopes. J Virol. 2012;86(7):3574-87.
55. Crooks ET, Tong T, Chakrabarti B, Narayan K, Georgiev IS, Menis S, Huang X, Kulp D, Osawa K, Muranaka J, 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. 2015;11(5):e1004932.
56. Excler JL, Ake J, Robb ML, Kim JH, Plotkin SA. Nonneutralizing functional antibodies: a new "old" paradigm for HIV vaccines. Clin Vaccine Immunol. 2014;21(8):1023-36.
57. Schmaljohn AL. Protective antiviral antibodies that lack neutralizing activity: precedents and evolution of concepts. Curr HIV Res. 2013;11(5):345-53.
58. Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM, Bess JW Jr, Sowder RC 2nd, Barsov E, Hood BL, Fisher RJ, et al. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol. 2006;80(18):9039-52.
59. Mahmood N, Hay AJ. An ELISA utilizing immobilised snowdrop lectin GNA for the detection of envelope glycoproteins of HIV and SIV. J Immunol Methods. 1992;151(1-2):9-13.
60. Yuan W, Li X, Kasterka M, Gorny MK, Zolla-Pazner S, Sodroski J. Oligomer-specific conformations of the human immunodeficiency virus (HIV-1) gp41 envelope glycoprotein ectodomain recognized by human monoclonal antibodies. AIDS Res Hum Retrovir. 2009;25(3):319-28.