Broadly neutralizing antibodies that inhibit HIV-1 cell to cell transmission

Journal of Experimental Medicine

Volumn 210, Issue 13, 2013, Pages 2813-2821

  Malbec, Marine ^a,b,c   Porrot, Françoise ^a,b   Rua, Rejane ^a,b,c   Horwitz, Joshua ^d   Klein, Florian ^d   Halper Stromberg, Ari ^d   Scheid, Johannes F ^d   Eden, Caroline ^d   Mouquet, Hugo ^a,b,d   Nussenzweig, Michel C ^d   Schwartz, Olivier ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROADLY NEUTRALIZING ANTIBODY; EPITOPE; GAG PROTEIN; GLYCAN; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; INTERFERON; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOSE RESPONSE; FLOW CYTOMETRY; HELA CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; LYMPHOBLASTOID CELL; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; TARGET CELL; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS TRANSMISSION;

ANTIBODIES, NEUTRALIZING; CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; DENDRITIC CELLS; HEK293 CELLS; HELA CELLS; HIV; HIV ANTIBODIES; HIV INFECTIONS; HUMANS; INHIBITORY CONCENTRATION 50; MICROSCOPY, FLUORESCENCE; TIME FACTORS; VIRION;

EID: 84890824652     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131244     Document Type: Article

References (42)

1. Abela, I.A., L. Berlinger, M. Schanz, L. Reynell, H.F. Günthard, P. Rusert, and A. Trkola. 2012. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog. 8:e1002634. http://dx.doi.org/10.1371/journal.ppat.1002634
2. Balazs, A.B., J. Chen, C.M. Hong, D.S. Rao, L. Yang, and D. Baltimore. 2012. Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature. 481:81-84. http://dx.doi.org/10.1038/nature10660
3. Bonsignori, M., D.C. Montefiori, X. Wu, X. Chen, K.K. Hwang, C.Y. Tsao, D.M. Kozink, R.J. Parks, G.D. Tomaras, J.A. Crump, et al. 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. http://dx.doi.org/10.1128/JVI.07163-11
4. Burton, D.R., R. Ahmed, D.H. Barouch, S.T. Butera, S. Crotty, A. Godzik, D.E. Kaufmann, M.J. McElrath, M.C. Nussenzweig, B. Pulendran, et al. 2012. A blueprint for HIV vaccine discovery. Cell Host Microbe. 12:396-407. http://dx.doi.org/10.1016/j.chom.2012.09.008
5. Chen, P., W. Hübner, M.A. Spinelli, and B.K. Chen. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595. http://dx.doi.org/10.1128/JVI.00381-07
6. Dale, B.M., R.A. Alvarez, and B.K. Chen. 2013. Mechanisms of enhanced HIV spread through T-cell virological synapses. Immunol. Rev. 251:113-124. http://dx.doi.org/10.1111/imr.12022
7. Dimitrov, D.S., R.L. Willey, H. Sato, L.J. Chang, R. Blumenthal, and M.A. Martin. 1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182-2190.
8. Diskin, R., J.F. Scheid, P.M. Marcovecchio, A.P. West Jr., F. Klein, H. Gao, P.N. Gnanapragasam, A. Abadir, M.S. Seaman, M.C. Nussenzweig, and P.J. Bjorkman. 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
9. Ganesh, L., K. Leung, K. Loré, R. Levin, A. Panet, O. Schwartz, R.A. Koup, and G.J. Nabel. 2004. Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cell-mediated transmission of virus resistant to broadly neutralizing antibodies. J. Virol. 78:11980-11987. http://dx.doi.org/10.1128/JVI.78.21.11980-11987.2004
10. Georgiev, I.S., N.A. Doria-Rose, T. Zhou, Y.D. Kwon, R.P. Staupe, S. Moquin, G.Y. Chuang, M.K. Louder, S.D. Schmidt, H.R. Altae-Tran, et al. 2013. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science. 340:751-756. http://dx.doi.org/10.1126/science.1233989
11. Haynes, B.F., P.B. Gilbert, M.J. McElrath, S. Zolla-Pazner, G.D. Tomaras, S.M. Alam, D.T. Evans, D.C. Montefiori, C. Karnasuta, R. Sutthent, et al. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366:1275-1286. http://dx.doi.org/10.1056/NEJMoa1113425
12. Hessell, A.J., P. Poignard, M. Hunter, L. Hangartner, D.M. Tehrani, W.K. Bleeker, P.W. Parren, P.A. Marx, and D.R. Burton. 2009. Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat. Med. 15:951-954. http://dx.doi.org/10.1038/nm.1974
13. Heyndrickx, L., A. Heath, E. Sheik-Khalil, J. Alcami, V. Bongertz, M. Jansson, M. Malnati, D. Montefiori, C. Moog, L. Morris, et al. 2012. International network for comparison of HIV neutralization assays: the NeutNet report II. PLoS ONE. 7:e36438. http://dx.doi.org/10.1371/journal.pone.0036438
14. Klein, F., C. Gaebler, H. Mouquet, D.N. Sather, C. Lehmann, J.F. Scheid, Z. Kraft, Y. Liu, J. Pietzsch, A. Hurley, et al. 2012a. 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. http://dx.doi.org/10.1084/jem.20120423
15. Klein, F., A. Halper-Stromberg, J.A. Horwitz, H. Gruell, J.F. Scheid, S. Bournazos, H. Mouquet, L.A. Spatz, R. Diskin, A. Abadir, et al. 2012b. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature. 492:118-122. http://dx.doi.org/10.1038/nature11604
16. Kwong, P.D., and J.R. Mascola. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity. 37:412-425. http://dx.doi.org/10.1016/j.immuni.2012.08.012
17. Lepelley, A., S. Louis, M. Sourisseau, H.K. Law, J. Pothlichet, C. Schilte, L. Chaperot, J. Plumas, R.E. Randall, M. Si-Tahar, et al. 2011. Innate sensing of HIV-infected cells. PLoS Pathog. 7:e1001284. http://dx.doi.org/10.1371/journal.ppat.1001284
18. Liao, H.X., R. Lynch, T. Zhou, F. Gao, S.M. Alam, S.D. Boyd, A.Z. Fire, K.M. Roskin, C.A. Schramm, Z. Zhang, et al; NISC Comparative Sequencing Program. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 496:469-476. http://dx.doi.org/10.1038/nature12053
19. Martin, N., S. Welsch, C. Jolly, J.A. Briggs, D. Vaux, and Q.J. Sattentau. 2010. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J. Virol. 84:3516-3527. http://dx.doi.org/10.1128/JVI.02651-09
20. Massanella, M., I. Puigdomènech, C. Cabrera, M.T. Fernandez-Figueras, A. Aucher, G. Gaibelet, D. Hudrisier, E. García, M. Bofill, B. Clotet, and J. Blanco. 2009. Antigp41 antibodies fail to block early events of virological synapses but inhibit HIV spread between T cells. AIDS. 23:183-188. http://dx.doi.org/10.1097/QAD.0b013e32831ef1a3
21. McCoy, L.E., and R.A. Weiss. 2013. Neutralizing antibodies to HIV-1 induced by immunization. J. Exp. Med. 210:209-223. http://dx.doi.org/10.1084/jem.20121827
22. Moldt, B., E.G. Rakasz, N. Schultz, P.-Y. Chan-Hui, K. Swiderek, K.L. Weisgrau, S.M. Piaskowski, Z. Bergman, D.I. Watkins, P. Poignard, and D.R. Burton. 2012. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc. Natl. Acad. Sci. USA. 109:18921-18925. http://dx.doi.org/10.1073/pnas.1214785109
23. Mouquet, H., L. Scharf, Z. Euler, Y. Liu, C. Eden, J.F. Scheid, A. Halper-Stromberg, P.N. Gnanapragasam, D.I. Spencer, M.S. Seaman, et al. 2012. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc. Natl. Acad. Sci. USA. 109:E3268-E3277. http://dx.doi.org/10.1073/pnas.1217207109
24. Murooka, T.T., M. Deruaz, F. Marangoni, V.D. Vrbanac, E. Seung, U.H. von Andrian, A.M. Tager, A.D. Luster, and T.R. Mempel. 2012. HIV-infected T cells are migratory vehicles for viral dissemination. Nature. 490:283-287. http://dx.doi.org/10.1038/nature11398
25. Ochsenbauer, C., T.G. Edmonds, H. Ding, B.F. Keele, J. Decker, M.G. Salazar, J.F. Salazar-Gonzalez, R. Shattock, B.F. Haynes, G.M. Shaw, et al. 2012. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J. Virol. 86:2715-2728. http://dx.doi.org/10.1128/JVI.06157-11
26. Pietzsch, J., H. Gruell, S. Bournazos, B.M. Donovan, F. Klein, R. Diskin, M.S. Seaman, P.J. Bjorkman, J.V. Ravetch, A. Ploss, and M.C. Nussenzweig. 2012. A mouse model for HIV-1 entry. Proc. Natl. Acad. Sci. USA. 109:15859-15864. http://dx.doi.org/10.1073/pnas.1213409109
27. Puigdomènech, I., N. Casartelli, F. Porrot, and O. Schwartz. 2013. SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells. J. Virol. 87:2846-2856. http://dx.doi.org/10.1128/JVI.02514-12
28. Rudnicka, D., J. Feldmann, F. Porrot, S. Wietgrefe, S. Guadagnini, M.C. Prévost, J. Estaquier, A.T. Haase, N. Sol-Foulon, and O. Schwartz. 2009. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 83:6234-6246. http://dx.doi.org/10.1128/JVI.00282-09
29. Salazar-Gonzalez, J.F., M.G. Salazar, B.F. Keele, G.H. Learn, E.E. Giorgi, H. Li, J.M. Decker, S. Wang, J. Baalwa, M.H. Kraus, et al. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 206:1273-1289. http://dx.doi.org/10.1084/jem.20090378
30. Sather, D.N., J. Armann, L.K. Ching, A. Mavrantoni, G. Sellhorn, Z. Caldwell, X. Yu, B. Wood, S. Self, S. Kalams, and L. Stamatatos. 2009. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83:757-769. http://dx.doi.org/10.1128/JVI.02036-08
31. Sattentau, Q.J. 2011. The direct passage of animal viruses between cells. Curr. Opin. Virol. 1:396-402. http://dx.doi.org/10.1016/j.coviro.2011.09.004
32. Scheid, J.F., H. Mouquet, N. Feldhahn, M.S. Seaman, K. Velinzon, J. Pietzsch, R.G. Ott, R.M. Anthony, H. Zebroski, A. Hurley, et al. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature. 458:636-640. http://dx.doi.org/10.1038/nature07930
33. Scheid, J.F., H. Mouquet, B. Ueberheide, R. Diskin, F. Klein, T.Y. Oliveira, J. Pietzsch, D. Fenyo, A. Abadir, K. Velinzon, et al. 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
34. Schwartz, O., M. Alizon, J.M. Heard, and O. Danos. 1994. Impairment of T cell receptor-dependent stimulation in CD4+ lymphocytes after contact with membrane-bound HIV-1 envelope glycoprotein. Virology. 198:360-365. http://dx.doi.org/10.1006/viro.1994.1042
35. Seaman, M.S., H. Janes, N. Hawkins, L.E. Grandpre, C. Devoy, A. Giri, R.T. Coffey, L. Harris, B. Wood, M.G. Daniels, et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84:1439-1452. http://dx.doi.org/10.1128/JVI.02108-09
36. Sigal, A., J.T. Kim, A.B. Balazs, E. Dekel, A. Mayo, R. Milo, and D. Baltimore. 2011. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature. 477:95-98. http://dx.doi.org/10.1038/nature10347
37. Simek, M.D., W. Rida, F.H. Priddy, P. Pung, E. Carrow, D.S. Laufer, J.K. Lehrman, M. Boaz, T. Tarragona-Fiol, G. Miiro, et al. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83:7337-7348. http://dx.doi.org/10.1128/JVI.00110-09
38. Sourisseau, M., N. Sol-Foulon, F. Porrot, F. Blanchet, and O. Schwartz. 2007. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81:1000-1012. http://dx.doi.org/10.1128/JVI.01629-06
39. Stamatatos, L., L. Morris, D.R. Burton, and J.R. Mascola. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15:866-870.
40. Walker, L.M., M. Huber, K.J. Doores, E. Falkowska, R. Pejchal, J.P. Julien, S.K. Wang, A. Ramos, P.Y. Chan-Hui, M. Moyle, et al; Protocol G Principal Investigators. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature. 477:466-470. http://dx.doi.org/10.1038/nature10373
41. West, A.P. Jr., R. Diskin, M.C. Nussenzweig, and P.J. Bjorkman. 2012. Structural basis for germ-line gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc. Natl. Acad. Sci. USA. 109:E2083-E2090. http://dx.doi.org/10.1073/pnas.1208984109
42. Wu, X., T. Zhou, J. Zhu, B. Zhang, I. Georgiev, C. Wang, X. Chen, N.S. Longo, M. Louder, K. McKee, et al; NISC Comparative Sequencing Program. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science. 333:1593-1602. http://dx.doi.org/10.1126/science.1207532