Structural Constraints of Vaccine-Induced Tier-2 Autologous HIV Neutralizing Antibodies Targeting the Receptor-Binding Site

Cell Reports

Volumn 14, Issue 1, 2016, Pages 43-54

  Bradley, Todd ^b   Fera, Daniela ^c   Bhiman, Jinal ^b,j   Eslamizar, Leila ^e   Lu, Xiaozhi ^b   Anasti, Kara ^b   Zhang, Ruijung ^b   Sutherland, Laura L ^b   Scearce, Richard M ^b   Bowman, Cindy M ^b   Stolarchuk, Christina ^b   Lloyd, Krissey E ^b   Parks, Robert ^b   Eaton, Amanda ^b   Foulger, Andrew ^b   Nie, Xiaoyan ^b   Karim, Salim S Abdool ^f,g   Barnett, Susan ^h   Kelsoe, Garnett ^b   Kepler, Thomas B ⁱ   Alam, S Munir ^b   Montefiori, David C ^b   Moody, M Anthony ^b   Liao, Hua Xin ^b   Morris, Lynn ^a,b,f   Santra, Sampa ^e   Harrison, Stephen C ^c,d   Haynes, Barton F ^b   more..

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g Novartis Vaccines and Diagnostics Inc   (United States)

^h BOSTON UNIVERSITY   (United States)

ⁱ UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^j NONE

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN RECOGNITION; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE C; IMMUNIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RECEPTOR BINDING; RHESUS MONKEY; STRUCTURE ANALYSIS; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; ANIMAL; FEMALE; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; MALE; MOLECULAR GENETICS;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV ANTIBODIES; HIV-1; HUMANS; MACACA MULATTA; MALE; MOLECULAR SEQUENCE DATA;

EID: 84952980275     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.12.017     Document Type: Article

References (53)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Alam S.M., Liao H.X., Dennison S.M., Jaeger F., Parks R., Anasti K., Foulger A., Donathan M., Lucas J., Verkoczy L., et al. Differential reactivity of germ line allelic variants of a broadly neutralizing HIV-1 antibody to a gp41 fusion intermediate conformation. J. Virol. 2011, 85:11725-11731.
3. Ariyoshi K., Harwood E., Chiengsong-Popov R., Weber J. Is clearance of HIV-1 viraemia at seroconversion mediated by neutralising antibodies?. Lancet 1992, 340:1257-1258.
4. Bar K.J., Tsao C.Y., Iyer S.S., Decker J.M., Yang Y., Bonsignori M., Chen X., Hwang K.K., Montefiori D.C., Liao H.X., et al. Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathog. 2012, 8:e1002721.
5. Burton D.R., Poignard P., Stanfield R.L., Wilson I.A. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 2012, 337:183-186.
6. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
7. Doria-Rose N.A., Klein R.M., Daniels M.G., O'Dell S., Nason M., Lapedes A., Bhattacharya T., Migueles S.A., Wyatt R.T., Korber B.T., et al. Breadth of human immunodeficiency virus-specific neutralizing activity in sera: clustering analysis and association with clinical variables. J. Virol. 2010, 84:1631-1636.
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. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 2014, 509:55-62. NISC Comparative Sequencing Program.
9. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
10. Fera D., Schmidt A.G., Haynes B.F., Gao F., Liao H.X., Kepler T.B., Harrison S.C. Affinity maturation in an HIV broadly neutralizing B-cell lineage through reorientation of variable domains. Proc. Natl. Acad. Sci. USA 2014, 111:10275-10280.
11. Gao F., Bonsignori M., Liao H.X., Kumar A., Xia S.M., Lu X., Cai F., Hwang K.K., Song H., Zhou T., et al. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell 2014, 158:481-491.
12. Gomez T.S., Billadeau D.D. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 2009, 17:699-711.
13. Gray E.S., Moore P.L., Choge I.A., Decker J.M., Bibollet-Ruche F., Li H., Leseka N., Treurnicht F., Mlisana K., Shaw G.M., et al. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. 2007, 81:6187-6196. CAPRISA 002 Study Team.
14. Gray E.S., Madiga M.C., Moore P.L., Mlisana K., Abdool Karim S.S., Binley J.M., Shaw G.M., Mascola J.R., Morris L. Broad neutralization of human immunodeficiency virus type 1 mediated by plasma antibodies against the gp41 membrane proximal external region. J. Virol. 2009, 83:11265-11274.
15. Gray E.S., Taylor N., Wycuff D., Moore P.L., Tomaras G.D., Wibmer C.K., Puren A., DeCamp A., Gilbert P.B., Wood B., et al. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 2009, 83:8925-8937.
16. Gray E.S., Madiga M.C., Hermanus T., Moore P.L., Wibmer C.K., Tumba N.L., Werner L., Mlisana K., Sibeko S., Williamson C., et al. The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J. Virol. 2011, 85:4828-4840. CAPRISA002 Study Team.
17. Haynes B.F., Verkoczy L. AIDS/HIV. Host controls of HIV neutralizing antibodies. Science 2014, 344:588-589.
18. 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 2013, 342:1477-1483.
19. Kabsch W. Xds. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:125-132.
20. Keele B.F., Giorgi E.E., Salazar-Gonzalez J.F., Decker J.M., Pham K.T., Salazar M.G., Sun C., Grayson T., Wang S., Li H., et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 2008, 105:7552-7557.
21. Kepler T.B. Reconstructing a B-cell clonal lineage. I. Statistical inference of unobserved ancestors. F1000Res. 2013, 2:103.
22. Kepler T.B., Liao H.X., Alam S.M., Bhaskarabhatla R., Zhang R., Yandava C., Stewart S., Anasti K., Kelsoe G., Parks R., et al. Immunoglobulin gene insertions and deletions in the affinity maturation of HIV-1 broadly reactive neutralizing antibodies. Cell Host Microbe 2014, 16:304-313.
23. Kwong P.D., Mascola J.R. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 2012, 37:412-425.
24. 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. 2013, 13:693-701.
25. Liao H.X., Levesque M.C., Nagel A., Dixon A., Zhang R., Walter E., Parks R., Whitesides J., Marshall D.J., Hwang K.K., et al. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 2009, 158:171-179.
26. Liao H.X., Chen X., Munshaw S., Zhang R., Marshall D.J., Vandergrift N., Whitesides J.F., Lu X., Yu J.S., Hwang K.K., et al. Initial antibodies binding to HIV-1 gp41 in acutely infected subjects are polyreactive and highly mutated. J. Exp. Med. 2011, 208:2237-2249.
27. Liao H.X., Lynch R., Zhou T., Gao F., Alam S.M., Boyd S.D., Fire A.Z., Roskin K.M., Schramm C.A., Zhang Z., et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 2013, 496:469-476. NISC Comparative Sequencing Program.
28. Liao H.X., Tsao C.Y., Alam S.M., Muldoon M., Vandergrift N., Ma B.J., Lu X., Sutherland L.L., Scearce R.M., Bowman C., et al. Antigenicity and immunogenicity of transmitted/founder, consensus, and chronic envelope glycoproteins of human immunodeficiency virus type 1. J. Virol. 2013, 87:4185-4201.
29. Liu J., Bartesaghi A., Borgnia M.J., Sapiro G., Subramaniam S. Molecular architecture of native HIV-1 gp120 trimers. Nature 2008, 455:109-113.
30. Mascola J.R., Haynes B.F. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 2013, 254:225-244.
31. McCoy A.J. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 2007, 63:32-41.
32. McGuire A.T., Hoot S., Dreyer A.M., Lippy A., Stuart A., Cohen K.W., Jardine J., Menis S., Scheid J.F., West A.P., et al. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J. Exp. Med. 2013, 210:655-663.
33. Morris L., Chen X., Alam M., Tomaras G., Zhang R., Marshall D.J., Chen B., Parks R., Foulger A., Jaeger F., et al. Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS ONE 2011, 6:e23532.
34. Munshaw S., Kepler T.B. SoDA2: a Hidden Markov Model approach for identification of immunoglobulin rearrangements. Bioinformatics 2010, 26:867-872.
35. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
36. 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. 2015, 89:3380-3395.
37. Richman D.D., Wrin T., Little S.J., Petropoulos C.J. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 2003, 100:4144-4149.
38. 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 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 2015, 349:aac4223.
39. Sarzotti-Kelsoe M., Bailer R.T., Turk E., Lin C.L., Bilska M., Greene K.M., Gao H., Todd C.A., Ozaki D.A., Seaman M.S., et al. Optimization and validation of the TZM-bl assay for standardized assessments of neutralizing antibodies against HIV-1. J. Immunol. Methods 2014, 409:131-146.
40. Scheid J.F., Mouquet H., Feldhahn N., Seaman M.S., Velinzon K., Pietzsch J., Ott R.G., Anthony R.M., Zebroski H., Hurley A., et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 2009, 458:636-640.
41. Scheid J.F., Mouquet H., Ueberheide B., Diskin R., Klein F., Oliveira T.Y., Pietzsch J., Fenyo D., Abadir A., Velinzon K., et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 2011, 333:1633-1637.
42. Seaman M.S., Janes H., Hawkins N., Grandpre L.E., Devoy C., Giri A., Coffey R.T., Harris L., Wood B., Daniels M.G., et al. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 2010, 84:1439-1452.
43. Tomaras G.D., Binley J.M., Gray E.S., Crooks E.T., Osawa K., Moore P.L., Tumba N., Tong T., Shen X., Yates N.L., et al. Polyclonal B cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. J. Virol. 2011, 85:11502-11519.
44. Walker L.M., Huber M., Doores K.J., Falkowska E., Pejchal R., Julien J.P., Wang S.K., Ramos A., Chan-Hui P.Y., Moyle M., et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 2011, 477:466-470. Protocol G Principal Investigators.
45. 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 2003, 422:307-312.
46. Wibmer C.K., Bhiman J.N., Gray E.S., Tumba N., Abdool Karim S.S., Williamson C., Morris L., Moore P.L. Viral escape from HIV-1 neutralizing antibodies drives increased plasma neutralization breadth through sequential recognition of multiple epitopes and immunotypes. PLoS Pathog. 2013, 9:e1003738.
47. Wiehe K., Easterhoff D., Luo K., Nicely N.I., Bradley T., Jaeger F.H., Dennison S.M., Zhang R., Lloyd K.E., Stolarchuk C., et al. Antibody light-chain-restricted recognition of the site of immune pressure in the RV144 HIV-1 vaccine trial is phylogenetically conserved. Immunity 2014, 41:909-918.
48. Willey R.L., Byrum R., Piatak M., Kim Y.B., Cho M.W., Rossio J.L., Bess J., Igarashi T., Endo Y., Arthur L.O., et al. Control of viremia and prevention of simian-human immunodeficiency virus-induced disease in rhesus macaques immunized with recombinant vaccinia viruses plus inactivated simian immunodeficiency virus and human immunodeficiency virus type 1 particles. J. Virol. 2003, 77:1163-1174.
49. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., Keegan R.M., Krissinel E.B., Leslie A.G., McCoy A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:235-242.
50. Wyatt R., Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 1998, 280:1884-1888.
51. Yang G., Holl T.M., Liu Y., Li Y., Lu X., Nicely N.I., Kepler T.B., Alam S.M., Liao H.X., Cain D.W., et al. Identification of autoantigens recognized by the 2F5 and 4E10 broadly neutralizing HIV-1 antibodies. J. Exp. Med. 2013, 210:241-256.
52. Zhou T., Xu L., Dey B., Hessell A.J., Van Ryk D., Xiang S.H., Yang X., Zhang M.Y., Zwick M.B., Arthos J., et al. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 2007, 445:732-737.
53. Zhou T., Georgiev I., Wu X., Yang Z.Y., Dai K., Finzi A., Kwon Y.D., Scheid J.F., Shi W., Xu L., et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010, 329:811-817.