CD4-induced antibodies promote association of the HIV-1 envelope glycoprotein with CD4-binding site antibodies

Journal of Virology

Volumn 90, Issue 17, 2016, Pages 7822-7832

  Gardner, Matthew R ^a   Fellinger, Christoph H ^a   Prasad, Neha R ^a   Zhou, Amber S ^a   Kondur, Hema R ^a   Joshi, Vinita R ^a   Quinlan, Brian D ^a   Farzan, Michael ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CD4 BINDING SITE ANTIBODY VRC01; CD4 INDUCED ANTIBODY 412D; CD4 INDUCED ANTIBODY E51; EPITOPE; GLYCOPROTEIN GP 120; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PROTEIN BINDING; VIRUS ENVELOPE PROTEIN;

ANTIBODY SPECIFICITY; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; COMBINATION CHEMOTHERAPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; IC50; MONOTHERAPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN QUATERNARY STRUCTURE; VIRUS ISOLATION; CD4+ T LYMPHOCYTE; CELL LINE; HUMAN; IMMUNOLOGY; PHYSIOLOGY; VIRUS ATTACHMENT;

ANTIBODIES, NEUTRALIZING; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV ANTIBODIES; HIV-1; HUMANS; PROTEIN BINDING; VIRUS ATTACHMENT;

EID: 84983483250     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00803-16     Document Type: Article

References (45)

1. Checkley MA, Luttge BG, Freed EO. 2011. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J Mol Biol 410:582-608. http://dx.doi.org/10.1016/j.jmb.2011.04.042.
2. Dalgleish AG, Beverley PCL, Clapham PR, Crawford DH, Greaves MF, Weiss RA. 1984. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763-767. http://dx.doi.org /10.1038/312763a0.
3. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J. 1996. The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135-1148. http://dx.doi.org/10.1016/S0092-8674(00)81313-6.
4. Feng Y, Broder CC, Kennedy PE, Berger EA. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877. http://dx.doi.org/10.1126/science.272.5263.872.
5. 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. http://dx.doi.org/10.1038/31405.
6. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, Hendrickson WA, Sodroski JG. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711. http://dx.doi.org/10.1038/31514.
7. Burton D, Pyati J, Koduri R, Sharp S, Thornton G, Parren P, Sawyer L, Hendry R, Dunlop N, Nara P, et al 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027. http://dx.doi.org/10.1126/science.7973652.
8. Zhou T, Georgiev I, Wu X, Yang Z-Y, Dai K, Finzi A, Do Kwon Y, 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. http://dx.doi.org/10.1126/science.1192819.
9. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TYK, 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. http://dx.doi.org /10.1126/science.1207227.
10. Wu X, Yang Z-Y, Li Y, Hogerkorp C-M, 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. http://dx.doi.org/10.1126/science.1187659.
11. Diskin R, Scheid JF, Marcovecchio PM, West AP, Klein F, Gao H, Gnanapragasam PNP, Abadir A, Seaman MS, Nussenzweig MC, Bjorkman PJ. 2011. Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334:1289-1293. http://dx .doi.org/10.1126/science.1213782.
12. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, Stephenson KE, Chang H-W, Shekhar K, Gupta S, Nkolola JP, Seaman MS, Smith KM, Borducchi EN, Cabral C, Smith JY, Blackmore S, Sanisetty S, Perry JR, Beck M, Lewis MG, Rinaldi W, Chakraborty AK, Poignard P, Nussenzweig MC, Burton DR. 2013. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIVinfected rhesus monkeys. Nature 503:224-228. http://dx.doi.org/10.1038/nature12744.
13. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, Dunlop DC, Poignard P, Doyle LA, Cavacini L, Veazey RS, Moore JP. 2011. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A 108:11181-11186. http://dx.doi .org/10.1073/pnas.1103012108.
14. Horwitz JA, Halper-Stromberg A, Mouquet H, Gitlin AD, Tretiakova A, Eisenreich TR, Malbec M, Gravemann S, Billerbeck E, Dorner M, Büning H, Schwartz O, Knops E, Kaiser R, Seaman MS, Wilson JM, Rice CM, Ploss A, Bjorkman PJ, Klein F, Nussenzweig MC. 2013. HIV-1 suppression and durable control by combining single broadly neutralizing antibodies and antiretroviral drugs in humanized mice. Proc Natl Acad Sci U S A 110:16538-16543. http://dx.doi.org/10.1073/pnas.1315295110.
15. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, Buckler-White A, Seaman M, Piatak M, Lifson JD, Dimitrov D, Nussenzweig MC, Martin MA. 2013. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503:277-280. http://dx.doi.org/10.1038/nature12746.
16. Caskey M, Klein F, Lorenzi JCC, Seaman MS, West Jr, AP, Buckley N, Kremer G, Nogueira L, Braunschweig M, Scheid JF, Horwitz JA, Shimeliovich I, Ben-Avraham S, Witmer-Pack M, Platten M, Lehmann C, Burke LA, Hawthorne T, Gorelick RJ, Walker BD, Keler T, Gulick RM, Fatkenheuer G, Schlesinger SJ, Nussenzweig MC. 2015. Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117. Nature 522:487-491. http://dx.doi.org/10.1038/nature14411.
17. Lynch RM, Boritz E, Coates EE, DeZure A, Madden P, Costner P, Enama ME, Plummer S, Holman L, Hendel CS, Gordon I, Casazza J, Conan-Cibotti M, Migueles SA, Tressler R, Bailer RT, McDermott A, Narpala S, O'Dell S, Wolf G, Lifson JD, Freemire BA, Gorelick RJ, Pandey JP, Mohan S, Chomont N, Fromentin R, Chun T-W, Fauci AS, Schwartz RM, Koup RA, Douek DC, Hu Z, Capparelli E, Graham BS, Mascola JR, Ledgerwood JE. 2015. Virologic effects of broadly neutralizing antibody VRC01 administration during chronic HIV-1 infection. Sci Transl Med 7:319ra206-319ra206. http://dx.doi .org/10.1126/scitranslmed.aad5752.
18. Thali M, Moore JP, Furman C, Charles M, Ho DD, Robinson J, Sodroski J. 1993. Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J Virol 67:3978-3988.
19. Xiang SH, Doka N, Choudhary RK, Sodroski J, Robinson JE. 2002. Characterization of CD4-induced epitopes on the HIV type 1 gp120 envelope glycoprotein recognized by neutralizing human monoclonal antibodies. AIDS Res Hum Retroviruses 18:1207-1217. http://dx.doi.org/10.1089/08892220260387959.
20. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, Moore JP, Nabel GJ, Sodroski J, Wilson IA, Wyatt RT. 2004. HIV vaccine design and the neutralizing antibody problem. Nat Immunol 5:233-236. http://dx.doi.org/10.1038/ni0304-233.
21. Labrijn AF, Poignard P, Raja A, Zwick MB, Delgado K, Franti M, Binley J, Vivona V, Grundner C, Huang C-C, 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. http://dx.doi.org/10.1128/JVI.77.19.10557-10565.2003.
22. Choe H, Li W, Wright PL, Vasilieva N, Venturi M, Huang C-C, Grundner C, Dorfman T, Zwick MB, Wang L, Rosenberg ES, Kwong PD, Burton DR, Robinson JE, Sodroski JG, Farzan M. 2003. Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell 114:161-170. http://dx.doi.org/10.1016/S0092-8674(03)00508-7.
23. Farzan M, Mirzabekov T, Kolchinsky P, Wyatt R, Cayabyab M, Gerard NP, Gerard C, Sodroski J, Choe H. 1999. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 Entry. Cell 96:667-676. http://dx.doi .org/10.1016/S0092-8674(00)80577-2.
24. Chiang JJ, Gardner MR, Quinlan BD, Dorfman T, Choe H, Farzan M. 2012. Enhanced recognition and neutralization of HIV-1 by antibodyderived CCR5-mimetic peptide variants. J Virol 86:12417-12421. http://dx.doi.org/10.1128/JVI.00967-12.
25. Dorfman T, Moore MJ, Guth AC, Choe H, Farzan M. 2006. A tyrosinesulfated peptide derived from the heavy-chain CDR3 region of an HIV-1-neutralizing antibody binds gp120 and inhibits HIV-1 infection. J Biol Chem 281:28529-28535. http://dx.doi.org/10.1074/jbc.M602732200.
26. Huang C-c, Lam SN, Acharya P, Tang M, Xiang S-H, Hussan SS-u, 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. http://dx.doi.org/10.1126/science.1145373.
27. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72:2855-2864.
28. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, Ratner L, Kappes JC, Shaw GM, Hunter E. 2000. 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 74:8358-8367. http://dx.doi.org/10.1128/JVI.74.18.8358-8367.2000.
29. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896-1905. http://dx.doi.org /10.1128/AAC.46.6.1896-1905.2002.
30. Takeuchi Y, McClure MO, Pizzato M. 2008. Identification of gammaretroviruses constitutively released from cell lines used for human immunodeficiency virus research. J Virol 82:12585-12588. http://dx.doi.org/10.1128/JVI.01726-08.
31. Platt EJ, Bilska M, Kozak SL, Kabat D, Montefiori DC. 2009. Evidence that ecotropic murine leukemia virus contamination in TZM-bl cells does not affect the outcome of neutralizing antibody assays with human immu-nodeficiency virus type 1. J Virol 83:8289-8292. http://dx.doi.org/10.1128/JVI.00709-09.
32. Kwong JA, Dorfman T, Quinlan BD, Chiang JJ, Ahmed AA, Choe H, Farzan M. 2011. A tyrosine-sulfated CCR5-mimetic peptide promotes conformational transitions in the HIV-1 envelope glycoprotein. J Virol 85:7563-7571. http://dx.doi.org/10.1128/JVI.00630-11.
33. Connor RI, Chen BK, Choe S, Landau NR. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944. http://dx.doi.org/10.1006/viro.1995.1016.
34. He J, Choe S, Walker R, Di Marzio P, Morgan DO, Landau NR. 1995. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J Virol 69:6705-6711.
35. Barouch DH, Yang Z-y, Kong W-p, Korioth-Schmitz B, Sumida SM, Truitt DM, Kishko MG, Arthur JC, Miura A, Mascola JR, Letvin NL, Nabel GJ. 2005. A human T-cell leukemia virus type 1 regulatory element enhances the immunogenicity of human immunodeficiency virus type 1 DNA vaccines in mice and nonhuman primates. J Virol 79:8828-8834. http://dx.doi.org/10.1128/JVI.79.14.8828-8834.2005.
36. 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. http://dx.doi .org/10.1038/nature11544.
37. 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. http://dx.doi.org/10.1128/JVI.79.16.10108-10125.2005.
38. Chen J, Kovacs JM, Peng H, Rits-Volloch S, Lu J, Park D, Zablowsky E, Seaman MS, Chen B. 2015. Effect of the cytoplasmic domain on antigenic characteristics of HIV-1 envelope glycoprotein. Science 349:191-195. http://dx.doi.org/10.1126/science.aaa9804.
39. Tran EEH, Borgnia MJ, Kuybeda O, Schauder DM, Bartesaghi A, Frank GA, Sapiro G, Milne JLS, Subramaniam S. 2012. Structural mechanism of trimeric HIV-1 envelope glycoprotein activation. PLoS Pathog 8:e1002797. http://dx.doi.org/10.1371/journal.ppat.1002797.
40. Meyerson JR, Tran EEH, Kuybeda O, Chen W, Dimitrov DS, Gorlani A, Verrips T, Lifson JD, Subramaniam S. 2013. Molecular structures of trimeric HIV-1 Env in complex with small antibody derivatives. Proc Natl Acad Sci U S A 110:513-518. http://dx.doi.org/10.1073/pnas.1214810110.
41. Bartesaghi A, Merk A, Borgnia MJ, Milne JLS, Subramaniam S. 2013. Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat Struct Mol Biol 20:1352-1357. http://dx .doi.org/10.1038/nsmb.2711.
42. Chen W, Feng Y, Wang Y, Zhu Z, Dimitrov DS. 2012. Fusion proteins of HIV-1 envelope glycoprotein gp120 with CD4-induced antibodies showed enhanced binding to CD4 and CD4 binding site antibodies. Biochem Biophys Res Commun 425:931-937. http://dx.doi.org/10.1016/j .bbrc.2012.08.013.
43. Haim H, Salas I, McGee K, Eichelberger N, Winter E, Pacheco B, Sodroski J. 2013. Modeling virus-and antibody-specific factors to predict human immunodeficiency virus neutralization efficiency. Cell Host Microbe 14:547-558. http://dx.doi.org/10.1016/j.chom.2013.10.006.
44. 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. http://dx.doi.org/10.1084/jem .20042510.
45. DeVico A, Fouts T, Lewis GK, Gallo RC, Godfrey K, Charurat M, Harris I, Galmin L, Pal R. 2007. Antibodies to CD4-induced sites in HIV gp120 correlate with the control of SHIV challenge in macaques vaccinated with subunit immunogens. Proc Natl Acad Sci U S A 104:17477-17482. http://dx.doi.org/10.1073/pnas.0707399104.