Heavy chain-only IgG2b llama antibody effects near-pan HIV-1 neutralization by recognizing a CD4-induced epitope that includes elements of coreceptor-and CD4-binding sites

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10173-10181

  Acharya, Priyamvada ^a   Luongo, Timothy S ^a   Georgiev, Ivelin S ^a   Matz, Julie ^b   Schmidt, Stephen D ^a   Louder, Mark K ^a   Kessler, Pascal ^c   Yang, Yongping ^a   McKee, Krisha ^a   O'Dell, Sijy ^a   Chen, Lei ^a   Baty, Daniel ^b   Chames, Patrick ^b   Martin, Loïc ^c   Mascola, John R ^a   Kwong, Peter D ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b AIX MARSEILLE UNIVERSITY   (France)

^c SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3 ANTIBODY; NEUTRALIZING ANTIBODY;

ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN BOND; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; VIRUS ISOLATION; VIRUS NEUTRALIZATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIBODIES, NEUTRALIZING; BINDING SITES; CAMELIDS, NEW WORLD; CRYSTALLOGRAPHY, X-RAY; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNOGLOBULIN G; NEUTRALIZATION TESTS; SURFACE PLASMON RESONANCE;

EID: 84883304048     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01332-13     Document Type: Article

References (49)

1. Wyatt R, Sodroski J. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
2. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, Xiang SH, Yang X, Zhang MY, Zwick MB, Arthos J, Burton DR, Dimitrov DS, Sodroski J, Wyatt R, Nabel GJ, Kwong PD. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445:732-737.
3. Lynch RM, Tran L, Louder MK, Schmidt SD, Cohen M, Dersimonian R, Euler Z, Gray ES, Abdool Karim S, Kirchherr J, Montefiori DC, Sibeko S, Soderberg K, Tomaras G, Yang ZY, Nabel GJ, Schuitemaker H, Morris L, Haynes BF, Mascola JR. 2012. The development of CD4 binding site antibodies during HIV-1 infection. J. Virol. 86:7588-7595.
4. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, Steenbeke TD, Venturi M, Chaiken I, Fung M, Katinger H, Parren PW, Robinson J, Van Ryk D, Wang L, Burton DR, Freire E, Wyatt R, Sodroski J, Hendrickson WA, Arthos J. 2002. HIV-1 evades antibodymediated neutralization through conformational masking of receptorbinding sites. Nature 420:678-682.
5. Labrijn AF, Poignard P, Raja A, Zwick MB, Delgado K, Franti M, Binley J, Vivona V, Grundner C, Huang CC, Venturi M, Petropoulos CJ, Wrin T, Dimitrov DS, Robinson J, Kwong PD, Wyatt RT, Sodroski J, Burton DR. 2003. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J. Virol. 77:10557-10565.
6. Decker JM, Bibollet-Ruche F, Wei X, Wang S, Levy DN, Wang W, Delaporte E, Peeters M, Derdeyn CA, Allen S, Hunter E, Saag MS, Hoxie JA, Hahn BH, Kwong PD, Robinson JE, Shaw GM. 2005. Antigenic conservation and immunogenicity of the HIV coreceptor binding site. J. Exp. Med. 201:1407-1419.
7. Dey AK, Burke B, Sun Y, Sirokman K, Nandi A, Hartog K, Lian Y, Geonnotti AR, Montefiori D, Franti M, Martin G, Carfi A, Kessler P, Martin L, Srivastava IK, Barnett SW. 2012. Elicitation of neutralizing antibodies directed against CD4-induced epitope(s) using a CD4 mimetic cross-linked to a HIV-1 envelope glycoprotein. PLoS One 7:e30233. doi: 10.1371/journal.pone.0030233.
8. Dey B, Del Castillo CS, Berger EA. 2003. Neutralization of human immunodeficiency virus type 1 by sCD4-17b, a single-chain chimeric protein, based on sequential interaction of gp120 with CD4 and coreceptor. J. Virol. 77:2859-2865.
9. Rizzuto CD, Wyatt R, Hernandez-Ramos N, Sun Y, Kwong PD, Hendrickson WA, Sodroski J. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
10. Matz J, Kessler P, Bouchet J, Combes O, Ramos OH, Barin F, Baty D, Martin L, Benichou S, Chames P. 2013. Straightforward selection of broadly neutralizing single-domain antibodies targeting the conserved CD4 and coreceptor binding sites of HIV-1 gp120. J. Virol. 87:1137-1149.
11. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. 2000. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8:1329-1339.
12. Huang CC, Stricher F, Martin L, Decker JM, Majeed S, Barthe P, Hendrickson WA, Robinson J, Roumestand C, Sodroski J, Wyatt R, Shaw GM, Vita C, Kwong PD. 2005. Scorpion-toxin mimics of CD4 in complex with human immunodeficiency virus gp120 crystal structures, molecular mimicry, and neutralization breadth. Structure 13:755-768.
13. Xiang SH, Wang L, Abreu M, Huang CC, Kwong PD, Rosenberg E, Robinson JE, Sodroski J. 2003. Epitope mapping and characterization of a novel CD4-induced human monoclonal antibody capable of neutralizing primary HIV-1 strains. Virology 315:124-134.
14. Kwon YD, Finzi A, Wu X, Dogo-Isonagie C, Lee LK, Moore LR, Schmidt SD, Stuckey J, Yang Y, Zhou T, Zhu J, Vicic DA, Debnath AK, Shapiro L, Bewley CA, Mascola JR, Sodroski JG, Kwong PD. 2012. Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc. Natl. Acad. Sci. U. S. A. 109:5663-5668.
15. Van Herrewege Y, Morellato L, Descours A, Aerts L, Michiels J, Heyndrickx L, Martin L, Vanham G. 2008. CD4 mimetic miniproteins: potent anti-HIV compounds with promising activity as microbicides. J. Antimicrob. Chemother. 61:818-826.
16. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
17. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
18. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
19. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
20. Lütteke T, von der Lieth CW. 2004. pdb-care (PDB carbohydrate residue check): a program to support annotation of complex carbohydrate structures in PDB files. BMC Bioinformatics 5:69. doi:10.1186 /1471-2105-5-69.
21. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774-797.
22. Hubbard SJ, Thornton JM. 1993. 'NACCESS,' computer program. Department of Biochemistry and Molecular Biology, University College London, London, United Kingdom.
23. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM, Bilska M, Kothe DL, Salazar-Gonzalez JF, Wei X, Decker JM, Hahn BH, Montefiori DC. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
24. Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C, Giri A, Coffey RT, Harris L, Wood B, Daniels MG, Bhattacharya T, Lapedes A, Polonis VR, McCutchan FE, Gilbert PB, Self SG, Korber BT, Montefiori DC, Mascola JR. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84: 1439-1452.
25. Li Y, O'Dell S, Wilson R, Wu X, Schmidt SD, Hogerkorp CM, Louder MK, Longo NS, Poulsen C, Guenaga J, Chakrabarti BK, Doria-Rose N, Roederer M, Connors M, Mascola JR, Wyatt RT. 2012. HIV-1 neutralizing antibodies display dual recognition of the primary and coreceptor binding sites and preferential binding to fully cleaved envelope glycoproteins. J. Virol. 86:11231-11241.
26. Georgiev IS, Doria-Rose NA, Zhou T, Kwon YD, Staupe RP, Moquin S, Chuang GY, Louder MK, Schmidt SD, Altae-Tran HR, Bailer RT, McKee K, Nason M, O'Dell S, Ofek G, Pancera M, Srivatsan S, Shapiro L, Connors M, Migueles SA, Morris L, Nishimura Y, Martin MA, Mascola JR, Kwong PD. 2013. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340:751-756.
27. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, Stanfield RL, Dimitrov DS, Korber B, Sodroski J, Wilson IA, Wyatt R, Kwong PD. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310:1025-1028.
28. Huang CC, Lam SN, Acharya P, Tang M, Xiang SH, Hussan SS, Stanfield RL, Robinson J, Sodroski J, Wilson IA, Wyatt R, Bewley CA, Kwong PD. 2007. Structures of the CCR5 N terminus and of a tyrosinesulfated antibody with HIV-1 gp120 and CD4. Science 317:1930-1934.
29. Huang CC, Venturi M, Majeed S, Moore MJ, Phogat S, Zhang MY, Dimitrov DS, Hendrickson WA, Robinson J, Sodroski J, Wyatt R, Choe H, Farzan M, Kwong PD. 2004. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptorbinding site on gp120. Proc. Natl. Acad. Sci. U. S. A. 101:2706-2711.
30. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
31. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, Kong L, Kwon YD, Stuckey J, Zhou T, Robinson JE, Schief WR, Sodroski J, Wyatt R, Kwong PD. 2010. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. U. S. A. 107:1166-1171.
32. Chen L, Kwon YD, Zhou T, Wu X, O'Dell S, Cavacini L, Hessell AJ, Pancera M, Tang M, Xu L, Yang ZY, Zhang MY, Arthos J, Burton DR, Dimitrov DS, Nabel GJ, Posner MR, Sodroski J, Wyatt R, Mascola JR, Kwong PD. 2009. Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326:1123-1127.
33. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, Finzi A, Kwon YD, Scheid JF, Shi W, Xu L, Yang Y, Zhu J, Nussenzweig MC, Sodroski J, Shapiro L, Nabel GJ, Mascola JR, Kwong PD. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329:811-817.
34. Chen W, Zhu Z, Feng Y, Dimitrov DS. 2008. Human domain antibodies to conserved sterically restricted regions on gp120 as exceptionally potent cross-reactive HIV-1 neutralizers. Proc. Natl. Acad. Sci. U. S. A. 105: 17121-17126.
35. Vu KB, Ghahroudi MA, Wyns L, Muyldermans S. 1997. Comparison of llama VH sequences from conventional and heavy chain antibodies. Mol. Immunol. 34:1121-1131.
36. Dey B, Pancera M, Svehla K, Shu Y, Xiang SH, Vainshtein J, Li Y, Sodroski J, Kwong PD, Mascola JR, Wyatt R. 2007. Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J. Virol. 81:5579-5593.
37. McCoy LE, Quigley AF, Strokappe NM, Bulmer-Thomas B, Seaman MS, Mortier D, Rutten L, Chander N, Edwards CJ, Ketteler R, Davis D, Verrips T, Weiss RA. 2012. Potent and broad neutralization of HIV-1 by a llama antibody elicited by immunization. J. Exp. Med. 209:1091-1103.
38. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TY, Pietzsch J, Fenyo D, Abadir A, Velinzon K, Hurley A, Myung S, Boulad F, Poignard P, Burton DR, Pereyra F, Ho DD, Walker BD, Seaman MS, Bjorkman PJ, Chait BT, Nussenzweig MC. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637.
39. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, Lehrman JK, Priddy FH, Olsen OA, Frey SM, Hammond PW, Kaminsky S, Zamb T, Moyle M, Koff WC, Poignard P, Burton DR. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
40. Klein F, Gaebler C, Mouquet H, Sather DN, Lehmann C, Scheid JF, Kraft Z, Liu Y, Pietzsch J, Hurley A, Poignard P, Feizi T, Morris L, Walker BD, Fatkenheuer G, Seaman MS, Stamatatos L, Nussenzweig MC. 2012. 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. 209:1469-1479.
41. Klein F, Halper-Stromberg A, Horwitz JA, Gruell H, Scheid JF, Bournazos S, Mouquet H, Spatz LA, Diskin R, Abadir A, Zang T, Dorner M, Billerbeck E, Labitt RN, Gaebler C, Marcovecchio PM, Incesu RB, Eisenreich TR, Bieniasz PD, Seaman MS, Bjorkman PJ, Ravetch JV, Ploss A, Nussenzweig MC. 2012. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492:118-122.
42. Poignard P, Sabbe R, Picchio GR, Wang M, Gulizia RJ, Katinger H, Parren PW, Mosier DE, Burton DR. 1999. Neutralizing antibodies have limited effects on the control of established HIV-1 infection in vivo. Immunity 10:431-438.
43. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, Salazar-Gonzalez JF, Salazar MG, Kilby JM, Saag MS, Komarova NL, Nowak MA, Hahn BH, Kwong PD, Shaw GM. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
44. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang KK, Tsao CY, Kozink DM, Parks RJ, Tomaras GD, Crump JA, Kapiga SH, Sam NE, Kwong PD, Kepler TB, Liao HX, Mascola JR, Haynes BF. 2012. Two distinct broadly neutralizing antibody specificities of different clonal lineages in a single HIV-1-infected donor: implications for vaccine design. J. Virol. 86:4688-4692.
45. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Alam SM, Wang T, Yang Y, Zhang B, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, Connors M. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406-412.
46. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, Wang SK, Stanfield RL, Julien JP, Ramos A, Crispin M, Depetris R, Katpally U, Marozsan A, Cupo A, Maloveste S, Liu Y, McBride R, Ito Y, Sanders RW, Ogohara C, Paulson JC, Feizi T, Scanlan CN, Wong CH, Moore JP, Olson WC, Ward AB, Poignard P, Schief WR, Burton DR, Wilson IA. 2011. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334:1097-1103.
47. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, Wycuff DL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
48. Acharya P, Dogo-Isonagie C, LaLonde JM, Lam SN, Leslie GJ, Louder MK, Frye LL, Debnath AK, Greenwood JR, Luongo TS, Martin L, Watts KS, Hoxie JA, Mascola JR, Bewley CA, Kwong PD. 2011. Structurebased identification and neutralization mechanism of tyrosine sulfate mimetics that inhibit HIV-1 entry. ACS Chem. Biol. 6:1069-1077.
49. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Cryst. D Biol. Crystallogr. 67(Pt. 4):235-242.