eCD4-Ig promotes ADCC activity of sera from HIV-1-infected patients

PLoS Pathogens

Volumn 13, Issue 12, 2017, Pages

  Davis Gardner, Meredith E ^a   Gardner, Matthew R ^a   Alfant, Barnett ^a   Farzan, Michael ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; EPITOPE; IMMUNOGLOBULIN G1; INTERLEUKIN 2; TUMOR NECROSIS FACTOR; CD4 IMMUNOGLOBULIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CYTOTOXICITY; DNA EXTRACTION; FLOW CYTOMETRY; HEK293T CELL LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE SYSTEM; LUCIFERASE ASSAY; MOUSE; NONHUMAN; ANIMAL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BLOOD; CELL LINE; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; PATHOGENICITY; PHYSIOLOGY; RHESUS MONKEY; VIROLOGY; VIRUS ACTIVATION; VIRUS LATENCY;

ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CD4 ANTIGENS; CD4 IMMUNOADHESINS; CELL LINE; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; HEK293 CELLS; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 85039904890     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006786     Document Type: Article

References (54)

1. Berger CT, Alter G, (2011) Natural killer cells in spontaneous control of HIV infection. Curr Opin HIV AIDS6: 208–213. doi: 10.1097/COH.0b013e3283457798 21399495
2. Bonsignori M, Pollara J, Moody MA, Alpert MD, Chen X, et al. (2012) Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J Virol86: 11521–11532. doi: 10.1128/JVI.01023-12 22896626
3. Scully E, Alter G, (2016) NK Cells in HIV Disease. Curr HIV/AIDS Rep13: 85–94. doi: 10.1007/s11904-016-0310-3 27002078
4. Nimmerjahn F, Gordan S, Lux A, (2015) FcgammaR dependent mechanisms of cytotoxic, agonistic, and neutralizing antibody activities. Trends Immunol36: 325–336. doi: 10.1016/j.it.2015.04.005 25981969
5. Boesch AW, Brown EP, Ackerman ME, (2015) The role of Fc receptors in HIV prevention and therapy. Immunol Rev268: 296–310. doi: 10.1111/imr.12339 26497529
6. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, et al. (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med366: 1275–1286. doi: 10.1056/NEJMoa1113425 22475592
7. Yates NL, Liao HX, Fong Y, deCamp A, Vandergrift NA, et al. (2014) Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med6: 228ra239.
8. Horwitz JA, Bar-On Y, Lu CL, Fera D, Lockhart AAK, et al. (2017) Non-neutralizing Antibodies Alter the Course of HIV-1 Infection In Vivo. Cell.
9. Alter G, Altfeld M, (2009) NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med265: 29–42. doi: 10.1111/j.1365-2796.2008.02045.x 19093958
10. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ, et al. (2007) Fc receptor but not complement binding is important in antibody protection against HIV. Nature449: 101–104. doi: 10.1038/nature06106 17805298
11. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, et al. (2013) Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature503: 224–228. doi: 10.1038/nature12744 24172905
12. Margolis DM, Garcia JV, Hazuda DJ, Haynes BF, (2016) Latency reversal and viral clearance to cure HIV-1. Science353: aaf6517. doi: 10.1126/science.aaf6517 27463679
13. Chun TW, Fauci AS, (2012) HIV reservoirs: pathogenesis and obstacles to viral eradication and cure. AIDS26: 1261–1268. doi: 10.1097/QAD.0b013e328353f3f1 22472858
14. Gardner MR, Farzan M, (2017) Engineering antibody-like inhibitors to prevent and treat HIV-1 infection. Curr Opin HIV AIDS12: 294–301. doi: 10.1097/COH.0000000000000367 28422793
15. Gardner MR, Kattenhorn LM, Kondur HR, von Schaewen M, Dorfman T, et al. (2015) AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges. Nature519: 87–91. doi: 10.1038/nature14264 25707797
16. Chiang JJ, Gardner MR, Quinlan BD, Dorfman T, Choe H, et al. (2012) Enhanced recognition and neutralization of HIV-1 by antibody-derived CCR5-mimetic peptide variants. J Virol86: 12417–12421. doi: 10.1128/JVI.00967-12 22933279
17. Kwong PD, Mascola JR, (2012) Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity37: 412–425. doi: 10.1016/j.immuni.2012.08.012 22999947
18. Williams KL, Cortez V, Dingens AS, Gach JS, Rainwater S, et al. (2015) HIV-specific CD4-induced Antibodies Mediate Broad and Potent Antibody-dependent Cellular Cytotoxicity Activity and Are Commonly Detected in Plasma From HIV-infected humans. EBioMedicine2: 1464–1477. doi: 10.1016/j.ebiom.2015.09.001 26629541
19. Tomaras GD, Haynes BF, (2009) HIV-1-specific antibody responses during acute and chronic HIV-1 infection. Curr Opin HIV AIDS4: 373–379. doi: 10.1097/COH.0b013e32832f00c0 20048700
20. Richard J, Veillette M, Brassard N, Iyer SS, Roger M, et al. (2015) CD4 mimetics sensitize HIV-1-infected cells to ADCC. Proc Natl Acad Sci U S A112: E2687–2694. doi: 10.1073/pnas.1506755112 25941367
21. Veillette M, Coutu M, Richard J, Batraville LA, Dagher O, et al. (2015) The HIV-1 gp120 CD4-bound conformation is preferentially targeted by antibody-dependent cellular cytotoxicity-mediating antibodies in sera from HIV-1-infected individuals. J Virol89: 545–551. doi: 10.1128/JVI.02868-14 25339767
22. Quinlan BD, Gardner MR, Joshi VR, Chiang JJ, Farzan M, (2013) Direct expression and validation of phage-selected peptide variants in mammalian cells. J Biol Chem288: 18803–18810. doi: 10.1074/jbc.M113.452839 23667257
23. Quinlan BD, Joshi VR, Gardner MR, Ebrahimi KH, Farzan M, (2014) A double-mimetic peptide efficiently neutralizes HIV-1 by bridging the CD4- and coreceptor-binding sites of gp120. J Virol88: 3353–3358. doi: 10.1128/JVI.03800-13 24390333
24. Lee WS, Richard J, Lichtfuss M, Smith AB, 3rdPark J, et al. (2015) Antibody-Dependent Cellular Cytotoxicity against Reactivated HIV-1-Infected Cells. J Virol90: 2021–2030. doi: 10.1128/JVI.02717-15 26656700
25. Bogers W, Barnett SW, Oostermeijer H, Nieuwenhuis IG, Beenhakker N, et al. (2017) Increased, durable B-cell and ADCC Responses Associated with T-helper Responses to HIV-1 Envelope in Macaques Vaccinated with gp140 Occluded at the CD4 Receptor Binding Site. J Virol.
26. 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 immunodeficiency virus type 1. J Virol83: 8289–8292. doi: 10.1128/JVI.00709-09 19474095
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. Journal of Virology72: 2855–2864. 9525605
28. Takeuchi Y, McClure MO, Pizzato M, (2008) Identification of gammaretroviruses constitutively released from cell lines used for human immunodeficiency virus research. J Virol82: 12585–12588. doi: 10.1128/JVI.01726-08 18842727
29. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, et al. (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother46: 1896–1905. doi: 10.1128/AAC.46.6.1896-1905.2002 12019106
30. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O’Brien WA, et al. (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 Virol74: 8358–8367. 10954535
31. Alpert MD, Harvey JD, Lauer WA, Reeves RK, Piatak M, Jr.et al. (2012) ADCC develops over time during persistent infection with live-attenuated SIV and is associated with complete protection against SIV(mac)251 challenge. PLoS Pathog8: e1002890. doi: 10.1371/journal.ppat.1002890 22927823
32. Alpert MD, Heyer LN, Williams DE, Harvey JD, Greenough T, et al. (2012) A novel assay for antibody-dependent cell-mediated cytotoxicity against HIV-1- or SIV-infected cells reveals incomplete overlap with antibodies measured by neutralization and binding assays. J Virol86: 12039–12052. doi: 10.1128/JVI.01650-12 22933282
33. Trkola A, Matthews J, Gordon C, Ketas T, Moore JP, (1999) A cell line-based neutralization assay for primary human immunodeficiency virus type 1 isolates that use either the CCR5 or the CXCR4 coreceptor. J Virol73: 8966–8974. 10516002
34. Lyerly HK, Reed DL, Matthews TJ, Langlois AJ, Ahearne PA, et al. (1987) Anti-GP 120 antibodies from HIV seropositive individuals mediate broadly reactive anti-HIV ADCC. AIDS Res Hum Retroviruses3: 409–422. doi: 10.1089/aid.1987.3.409 2833917
35. Howell DN, Andreotti PE, Dawson JR, Cresswell P, (1985) Natural killing target antigens as inducers of interferon: studies with an immunoselected, natural killing-resistant human T lymphoblastoid cell line. J Immunol134: 971–976. 3871222
36. Butera ST, Perez VL, Besansky NJ, Chan WC, Wu BY, et al. (1991) Extrachromosomal human immunodeficiency virus type-1 DNA can initiate a spreading infection of HL-60 cells. J Cell Biochem45: 366–373. doi: 10.1002/jcb.240450410 2045430
37. Butera ST, Perez VL, Wu BY, Nabel GJ, Folks TM, (1991) Oscillation of the human immunodeficiency virus surface receptor is regulated by the state of viral activation in a CD4+ cell model of chronic infection. J Virol65: 4645–4653. 1678437
38. Butera ST, Roberts BD, Folks TM, (1993) Regulation of HIV-1 expression by cytokine networks in a CD4+ model of chronic infection. J Immunol150: 625–634. 8380428
39. Butera ST, Roberts BD, Lam L, Hodge T, Folks TM, (1994) Human immunodeficiency virus type 1 RNA expression by four chronically infected cell lines indicates multiple mechanisms of latency. J Virol68: 2726–2730. 7511177
40. Butera ST, Roberts BD, Leung K, Nabel GJ, Folks TM, (1993) Tumor necrosis factor receptor expression and signal transduction in HIV-1-infected cells. Aids7: 911–918. 8395188
41. Clouse KA, Powell D, Washington I, Poli G, Strebel K, et al. (1989) Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J Immunol142: 431–438. 2463307
42. Folks TM, Clouse KA, Justement J, Rabson A, Duh E, et al. (1989) Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc Natl Acad Sci U S A86: 2365–2368. 2784570
43. Gardner MR, Fellinger CH, Prasad NR, Zhou AS, Kondur HR, et al. (2016) CD4-Induced Antibodies Promote Association of the HIV-1 Envelope Glycoprotein with CD4-Binding Site Antibodies. J Virol90: 7822–7832. doi: 10.1128/JVI.00803-16 27334589
44. Pancera M, McLellan JS, Wu X, Zhu J, Changela A, et al. (2010) Crystal structure of PG16 and chimeric dissection with somatically related PG9: structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J Virol84: 8098–8110. doi: 10.1128/JVI.00966-10 20538861
45. Barouch DH, Yang Z-y, Kong W-p, Korioth-Schmitz B, Sumida SM, et al. (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. Journal of Virology79: 8828–8834. doi: 10.1128/JVI.79.14.8828-8834.2005 15994776
46. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, et al. (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature491: 406–412. doi: 10.1038/nature11544 23151583
47. Huang J, Kang BH, Pancera M, Lee JH, Tong T, et al. (2014) Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature515: 138–142. doi: 10.1038/nature13601 25186731
48. Dorfman T, Moore MJ, Guth AC, Choe H, Farzan M, (2006) A tyrosine-sulfated peptide derived from the heavy-chain CDR3 region of an HIV-1-neutralizing antibody binds gp120 and inhibits HIV-1 infection. J Biol Chem281: 28529–28535. doi: 10.1074/jbc.M602732200 16849323
49. Collman R, Balliet JW, Gregory SA, Friedman H, Kolson DL, et al. (1992) An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J Virol66: 7517–7521. 1433527
50. Doranz BJ, Rucker J, Yi YJ, Smyth RJ, Samson M, et al. (1996) A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell85: 1149–1158. 8674120
51. Kim FM, Kolson DL, Balliet JW, Srinivasan A, Collman RG, (1995) V3-independent determinants of macrophage tropism in a primary human immunodeficiency virus type 1 isolate. J Virol69: 1755–1761. 7853514
52. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, et al. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol59: 284–291. 3016298
53. Li Y, Hui H, Burgess CJ, Price RW, Sharp PM, et al. (1992) Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J Virol66: 6587–6600. 1404605
54. Li Y, Kappes JC, Conway JA, Price RW, Shaw GM, et al. (1991) Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J Virol65: 3973–3985. 1830110