Amino Acid Changes in the HIV-1 gp41 Membrane Proximal Region Control Virus Neutralization Sensitivity

EBioMedicine

Volumn 12, Issue , 2016, Pages 196-207

  Bradley, Todd ^a   Trama, Ashley ^a   Tumba, Nancy ^b   Gray, Elin ^b   Lu, Xiaozhi ^a   Madani, Navid ^c,d   Jahanbakhsh, Fatemeh ^c   Eaton, Amanda ^a   Xia, Shi Mao ^a   Parks, Robert ^a   Lloyd, Krissey E ^a   Sutherland, Laura L ^a   Scearce, Richard M ^a   Bowman, Cindy M ^a   Barnett, Susan ^e   Abdool Karim, Salim S ^f,g   Boyd, Scott D ^h   Melillo, Bruno ⁱ   Smith, Amos B ⁱ   Sodroski, Joseph ^c,d   Kepler, Thomas B ^j   Alam, S Munir ^a   Gao, Feng ^a   Bonsignori, Mattia ^a   Liao, Hua Xin ^a   Moody, M Anthony ^a   Montefiori, David ^a   Santra, Sampa ^d   Morris, Lynn ^b,f,k   Haynes, Barton F ^a   more..

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Novartis Vaccines and Diagnostics Inc   (United States)

^f UNIVERSITY OF KWAZULU NATAL   (South Africa)

^g Columbia University ^*  (United States)

^h STANFORD UNIVERSITY   (United States)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

^j BOSTON UNIVERSITY   (United States)

^k UNIVERSITY OF THE WITWATERSRAND   (South Africa)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; NEUTRALIZING ANTIBODY; RECOMBINANT GLYCOPROTEIN GP 41; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; BLOCKING ANTIBODY; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

AMINO ACID SEQUENCE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC TRANSFECTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; MEMBRANE PROXIMAL EXTERNAL REGION; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEIC ACID STRUCTURE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS NEUTRALIZATION; AMINO ACID SUBSTITUTION; ANIMAL; ANTIGENIC VARIATION; CHEMISTRY; DISEASE MODEL; GENETICS; HIV INFECTIONS; IMMUNIZATION; IMMUNOLOGY; MUTATION; PROTEIN DOMAIN; RHESUS MONKEY; SERODIAGNOSIS; VIROLOGY;

AIDS VACCINES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, NEUTRALIZING; ANTIGENIC VARIATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; IMMUNIZATION; MACACA MULATTA; MUTATION; NEUTRALIZATION TESTS; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84992593349     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.08.045     Document Type: Article

References (59)

1. Andre, S., Seed, B., Eberle, J., Schraut, W., Bultmann, A., Haas, J., Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J. Virol. 72 (1998), 1497–1503.
2. Back, N.K., Smit, L., Schutten, M., Nara, P.L., Tersmette, M., Goudsmit, J., Mutations in human immunodeficiency virus type 1 gp41 affect sensitivity to neutralization by gp120 antibodies. J. Virol. 67 (1993), 6897–6902.
3. Berger, E.A., HIV entry and tropism: the chemokine receptor connection. AIDS 11:Suppl A (1997), S3–16.
4. Blish, C.A., Nguyen, M.A., Overbaugh, J., Enhancing exposure of HIV-1 neutralization epitopes through mutations in gp41. PLoS Med., 5, 2008, e9.
5. Bonsignori, M., Hwang, K.K., Chen, X., Tsao, C.Y., Morris, L., Gray, E., Marshall, D.J., Crump, J.A., Kapiga, S.H., Sam, N.E., Sinangil, F., Pancera, M., Yongping, Y., Zhang, B., Zhu, J., Kwong, P.D., O'dell, S., Mascola, J.R., Wu, L., Nabel, G.J., Phogat, S., Seaman, M.S., Whitesides, J.F., Moody, M.A., Kelsoe, G., Yang, X., Sodroski, J., Shaw, G.M., Montefiori, D.C., Kepler, T.B., Tomaras, G.D., Alam, S.M., Liao, H.X., Haynes, B.F., Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 85 (2011), 9998–10009.
6. Boyd, S.D., Marshall, E.L., Merker, J.D., Maniar, J.M., Zhang, L.N., Sahaf, B., Jones, C.D., Simen, B.B., Hanczaruk, B., Nguyen, K.D., Nadeau, K.C., Egholm, M., Miklos, D.B., Zehnder, J.L., Fire, A.Z., Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med., 1, 2009, 12ra23.
7. Bradley, T., Fera, D., Bhiman, J., Eslamizar, L., Lu, X.Z., Anasti, K., Zhang, R.J., Sutherland, L.L., Scearce, R.M., Bowman, C.M., Stolarchuk, C., Lloyd, K.E., Parks, R., Eaton, A., Foulger, A., Nie, X.Y., Karim, S.S.A., Barnett, S., Kelsoe, G., Kepler, T.B., Alam, S.M., Montefiori, D.C., Moody, M.A., Liao, H.X., Morris, L., Santra, S., Harrison, S.C., Haynes, B.F., Structural constraints of vaccine-induced tier-2 autologous HIV neutralizing antibodies targeting the receptor-binding site. Cell Rep. 14 (2016), 43–54.
8. Burton, D.R., Mascola, J.R., Antibody responses to envelope glycoproteins in HIV-1 infection. Nat. Immunol. 16 (2015), 571–576.
9. Colleton, B.A., Huang, X.L., Melhem, N.M., Fan, Z., Borowski, L., Rappocciolo, G., Rinaldo, C.R., Primary human immunodeficiency virus type 1-specific CD8 + T-cell responses induced by myeloid dendritic cells. J. Virol. 83 (2009), 6288–6299.
10. de Taeye, S.W., Moore, J.P., Sanders, R.W., HIV-1 Envelope Trimer Design and Immunization Strategies to Induce Broadly Neutralizing Antibodies. 2016 Trends Immunol.
11. Dennison, S.M., Stewart, S.M., Stempel, K.C., Liao, H.X., Haynes, B.F., Alam, S.M., Stable docking of neutralizing human immunodeficiency virus type 1 gp41 membrane-proximal external region monoclonal antibodies 2F5 and 4E10 is dependent on the membrane immersion depth of their epitope regions. J. Virol. 83 (2009), 10211–10223.
12. Derdeyn, C.A., Moore, P.L., Morris, L., Development of broadly neutralizing antibodies from autologous neutralizing antibody responses in HIV infection. Curr. Opin. HIV AIDS 9 (2014), 210–216.
13. Ewing, B., Green, P., Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8 (1998), 186–194.
14. Frey, G., Chen, J., Rits-Volloch, S., Freeman, M.M., Zolla-Pazner, S., Chen, B., Distinct conformational states of HIV-1 gp41 are recognized by neutralizing and non-neutralizing antibodies. Nat. Struct. Mol. Biol. 17 (2010), 1486–1491.
15. Gao, F., Bonsignori, M., Liao, H.X., Kumar, A., Xia, S.M., Lu, X., Cai, F., Hwang, K.K., Song, H., Zhou, T., Lynch, R.M., Alam, S.M., Moody, M.A., Ferrari, G., Berrong, M., Kelsoe, G., Shaw, G.M., Hahn, B.H., Montefiori, D.C., Kamanga, G., Cohen, M.S., Hraber, P., Kwong, P.D., Korber, B.T., Mascola, J.R., Kepler, T.B., Haynes, B.F., Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell 158 (2014), 481–491.
16. 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. 83 (2009), 11265–11274.
17. Haim, H., Strack, B., Kassa, A., Madani, N., Wang, L., Courter, J.R., Princiotto, A., Mcgee, K., Pacheco, B., Seaman, M.S., Smith, A.B. III, Sodroski, J., Contribution of intrinsic reactivity of the HIV-1 envelope glycoproteins to CD4-independent infection and global inhibitor sensitivity. PLoS Pathog., 7, 2011, e1002101.
18. Haynes, B.F., Kelsoe, G., Harrison, S.C., Kepler, T.B., B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat. Biotechnol. 30 (2012), 423–433.
19. Huang, J., Ofek, G., Laub, L., Louder, M.K., Doria-Rose, N.A., Longo, N.S., Imamichi, H., Bailer, R.T., Chakrabarti, B., Sharma, S.K., Alam, S.M., Wang, T., Yang, Y., Zhang, B., Migueles, S.A., Wyatt, R., Haynes, B.F., Kwong, P.D., Mascola, J.R., Connors, M., Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491 (2012), 406–412.
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., Wei, X., Jiang, C., Kirchherr, J.L., Gao, F., Anderson, J.A., Ping, L.H., Swanstrom, R., Tomaras, G.D., Blattner, W.A., Goepfert, P.A., Kilby, J.M., Saag, M.S., Delwart, E.L., Busch, M.P., Cohen, M.S., Montefiori, D.C., Haynes, B.F., Gaschen, B., Athreya, G.S., Lee, H.Y., Wood, N., Seoighe, C., Perelson, A.S., Bhattacharya, T., Korber, B.T., Hahn, B.H., Shaw, G.M., Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 7552–7557.
21. Kepler, T.B., Munshaw, S., Wiehe, K., Zhang, R.J., Yu, J.S., Woods, C.W., Denny, T.N., Tomaras, G.D., Alam, S.M., Moody, M.A., Kelsoe, G., Liao, H.X., Haynes, B.F., Reconstructing a B-cell clonal lineage. II. Mutation, selection, and affinity maturation. Front. Immunol., 5, 2014.
22. Kundu, S.K., Dupuis, M., Sette, A., Celis, E., Dorner, F., Eibl, M., Merigan, T.C., Role of preimmunization virus sequences in cellular immunity in HIV-infected patients during HIV type 1 MN recombinant gp160 immunization. AIDS Res. Hum. Retrovir. 14 (1998), 1669–1678.
23. Liao, H.X., Sutherland, L.L., Xia, S.M., Brock, M.E., Scearce, R.M., Vanleeuwen, S., Alam, S.M., Mcadams, M., Weaver, E.A., Camacho, Z., Ma, B.J., Li, Y., Decker, J.M., Nabel, G.J., Montefiori, D.C., Hahn, B.H., Korber, B.T., Gao, F., Haynes, B.F., A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353 (2006), 268–282.
24. Liao, H.X., Levesque, M.C., Nagel, A., Dixon, A., Zhang, R., Walter, E., Parks, R., Whitesides, J., Marshall, D.J., Hwang, K.K., Yang, Y., Chen, X., Gao, F., Munshaw, S., Kepler, T.B., Denny, T., Moody, M.A., Haynes, B.F., High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 158 (2009), 171–179.
25. 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., Gao, F., Markowitz, M., Heath, S.L., Bar, K.J., Goepfert, P.A., Montefiori, D.C., Shaw, G.C., Alam, S.M., Margolis, D.M., Denny, T.N., Boyd, S.D., Marshal, E., Egholm, M., Simen, B.B., Hanczaruk, B., Fire, A.Z., Voss, G., Kelsoe, G., Tomaras, G.D., Moody, M.A., Kepler, T.B., Haynes, B.F., Initial antibodies binding to HIV-1 gp41 in acutely infected subjects are polyreactive and highly mutated. J. Exp. Med. 208 (2011), 2237–2249.
26. Liao, H.X., Bonsignori, M., Alam, S.M., Mclellan, J.S., Tomaras, G.D., Moody, M.A., Kozink, D.M., Hwang, K.K., Chen, X., Tsao, C.Y., Liu, P., Lu, X., Parks, R.J., Montefiori, D.C., Ferrari, G., Pollara, J., Rao, M., Peachman, K.K., Santra, S., Letvin, N.L., Karasavvas, N., Yang, Z.Y., Dai, K., Pancera, M., Gorman, J., Wiehe, K., Nicely, N.I., Rerks-Ngarm, S., Nitayaphan, S., Kaewkungwal, J., Pitisuttithum, P., Tartaglia, J., Sinangil, F., Kim, J.H., Michael, N.L., Kepler, T.B., Kwong, P.D., Mascola, J.R., Nabel, G.J., Pinter, A., Zolla-Pazner, S., Haynes, B.F., Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38 (2013), 176–186.
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., Zhu, J., Shapiro, L., Program, N.C.S., Mullikin, J.C., Gnanakaran, S., Hraber, P., Wiehe, K., Kelsoe, G., Yang, G., Xia, S.M., Montefiori, D.C., Parks, R., Lloyd, K.E., Scearce, R.M., Soderberg, K.A., Cohen, M., Kamanga, G., Louder, M.K., Tran, L.M., Chen, Y., Cai, F., Chen, S., Moquin, S., Du, X., Joyce, M.G., Srivatsan, S., Zhang, B., Zheng, A., Shaw, G.M., Hahn, B.H., Kepler, T.B., Korber, B.T., Kwong, P.D., Mascola, J.R., Haynes, B.F., Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496 (2013), 469–476.
28. Mascola, J.R., Haynes, B.F., HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 254 (2013), 225–244.
29. Mascola, J.R., Montefiori, D.C., The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28 (2010), 413–444.
30. Mccoy, L.E., Weiss, R.A., Neutralizing antibodies to HIV-1 induced by immunization. J. Exp. Med. 210 (2013), 209–223.
31. Melillo, B., Liang, S., Park, J., Schon, A., Courter, J.R., Lalonde, J.M., Wendler, D.J., Princiotto, A.M., Seaman, M.S., Freire, E., Sodroski, J., Madani, N., Hendrickson, W.A., Smith, A.B. III, Small-Molecule CD4-Mimics: Structure-Based Optimization of HIV-1 Entry Inhibition. ACS Med. Chem. Lett. 7 (2016), 330–334.
32. Montefiori, D.C., Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol., Chapter 12(Unit 12), 2005, 11.
33. Montero, M., Van Houten, N.E., Wang, X., Scott, J.K., The membrane-proximal external region of the human immunodeficiency virus type 1 envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol. Mol. Biol. Rev. 72 (2008), 54–84 (table of contents).
34. Moody, M.A., Gao, F., Gurley, T.C., Amos, J.D., Kumar, A., Hora, B., Marshall, D.J., Whitesides, J.F., Xia, S.M., Parks, R., Lloyd, K.E., Hwang, K.K., Lu, X., Bonsignori, M., Finzi, A., Vandergrift, N.A., Alam, S.M., Ferrari, G., Shen, X., Tomaras, G.D., Kamanga, G., Cohen, M.S., Sam, N.E., Kapiga, S., Gray, E.S., Tumba, N.L., Morris, L., Zolla-Pazner, S., Gorny, M.K., Mascola, J.R., Hahn, B.H., Shaw, G.M., Sodroski, J.G., Liao, H.X., Montefiori, D.C., Hraber, P.T., Korber, B.T., Haynes, B.F., Strain-specific V3 and CD4 binding site autologous HIV-1 neutralizing antibodies select neutralization-resistant viruses. Cell Host Microbe 18 (2015), 354–362.
35. Moore, P.L., Ranchobe, N., Lambson, B.E., Gray, E.S., Cave, E., Abrahams, M.R., Bandawe, G., Mlisana, K., Abdool Karim, S.S., Williamson, C., Morris, L., STUDY, C., IMMUNOLOGY, N. C. F. H. A. V, Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog., 5, 2009, e1000598.
36. Morris, L., Chen, X., Alam, M., Tomaras, G., Zhang, R., Marshall, D.J., Chen, B., Parks, R., Foulger, A., Jaeger, F., Donathan, M., Bilska, M., Gray, E.S., Abdool Karim, S.S., Kepler, T.B., Whitesides, J., Montefiori, D., Moody, M.A., Liao, H.X., Haynes, B.F., Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One, 6, 2011, e23532.
37. Munoz-Barroso, I., Salzwedel, K., Hunter, E., Blumenthal, R., Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J. Virol. 73 (1999), 6089–6092.
38. Munro, J.B., Gorman, J., Ma, X., Zhou, Z., Arthos, J., Burton, D.R., Koff, W.C., Courter, J.R., Smith, A.B. III, Kwong, P.D., Blanchard, S.C., Mothes, W., Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346 (2014), 759–763.
39. Munshaw, S., Kepler, T.B., SoDA2: a hidden Markov model approach for identification of immunoglobulin rearrangements. Bioinformatics 26 (2010), 867–872.
40. Nakamura, K.J., Gach, J.S., Jones, L., Semrau, K., Walter, J., Bibollet-Ruche, F., Decker, J.M., Heath, L., Decker, W.D., Sinkala, M., Kankasa, C., Thea, D., Mullins, J., Kuhn, L., Zwick, M.B., Aldrovandi, G.M., 4E10-resistant HIV-1 isolated from four subjects with rare membrane-proximal external region polymorphisms. PLoS One, 5, 2010, e9786.
41. Perez, L.G., Costa, M.R., Todd, C.A., Haynes, B.F., Montefiori, D.C., Utilization of immunoglobulin G Fc receptors by human immunodeficiency virus type 1: a specific role for antibodies against the membrane-proximal external region of gp41. J. Virol. 83 (2009), 7397–7410.
42. Permar, S.R., Fong, Y., Vandergrift, N., Fouda, G.G., Gilbert, P., Parks, R., Jaeger, F.H., Pollara, J., Martelli, A., Liebl, B.E., Lloyd, K., Yates, N.L., Overman, R.G., Shen, X., Whitaker, K., Chen, H., Pritchett, J., Solomon, E., Friberg, E., Marshall, D.J., Whitesides, J.F., Gurley, T.C., Von Holle, T., Martinez, D.R., Cai, F., Kumar, A., Xia, S.M., Lu, X., Louzao, R., Wilkes, S., Datta, S., Sarzotti-Kelsoe, M., Liao, H.X., Ferrari, G., Alam, S.M., Montefiori, D.C., Denny, T.N., Moody, M.A., Tomaras, G.D., Gao, F., Haynes, B.F., Maternal HIV-1 envelope-specific antibody responses and reduced risk of perinatal transmission. J. Clin. Invest. 125 (2015), 2702–2706.
43. Reinis, M., Weiser, B., Kuiken, C., Dong, T., Lang, D., Nachman, S., Zhang, Y., Rowland-Jones, S., Burger, H., Genomic analysis of HIV type 1 strains derived from a mother and child pair of long-term nonprogressors. AIDS Res. Hum. Retrovir. 23 (2007), 309–315.
44. 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. U. S. A. 100 (2003), 4144–4149.
45. Ringe, R., Bhattacharya, J., Association of enhanced HIV-1 neutralization by a single Y681H substitution in gp41 with increased gp120-CD4 interaction and macrophage infectivity. PLoS One, 7, 2012, e37157.
46. 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., Arendt, H., Kim, H.J., Lee, J.H., Pugach, P., Williams, M., Debnath, G., Moldt, B., Van Breemen, M.J., ISIK, G., Medina-Ramirez, M., Back, J.W., Koff, W.C., Julien, J.P., Rakasz, E.G., Seaman, M.S., Guttman, M., Lee, K.K., Klasse, P.J., Labranche, C., Schief, W.R., Wilson, I.A., Overbaugh, J., Burton, D.R., Ward, A.B., Montefiori, D.C., Dean, H., Moore, J.P., HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science, 349, 2015, aac4223.
47. Seaman, M.S., Janes, H., Hawkins, N., Grandpre, L.E., Devoy, C., Giri, A., Coffey, R.T., Harris, L., Wood, B., Daniels, M.G., Bhattacharya, T., Lapedes, A., Polonis, V.R., Mccutchan, F.E., Gilbert, P.B., Self, S.G., Korber, B.T., Montefiori, D.C., Mascola, J.R., Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84 (2010), 1439–1452.
48. Shen, X., Parks, R.J., Montefiori, D.C., Kirchherr, J.L., Keele, B.F., Decker, J.M., Blattner, W.A., Gao, F., Weinhold, K.J., Hicks, C.B., Greenberg, M.L., Hahn, B.H., Shaw, G.M., Haynes, B.F., Tomaras, G.D., In vivo gp41 antibodies targeting the 2F5 monoclonal antibody epitope mediate human immunodeficiency virus type 1 neutralization breadth. J. Virol. 83 (2009), 3617–3625.
49. Shen, X., Dennison, S.M., Liu, P., Gao, F., Jaeger, F., Montefiori, D.C., Verkoczy, L., Haynes, B.F., Alam, S.M., Tomaras, G.D., Prolonged exposure of the HIV-1 gp41 membrane proximal region with L669S substitution. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 5972–5977.
50. Sun, Z.Y., Oh, K.J., Kim, M., Yu, J., Brusic, V., Song, L., Qiao, Z., Wang, J.H., Wagner, G., Reinherz, E.L., HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28 (2008), 52–63.
51. Tiller, T., Meffre, E., Yurasov, S., Tsuiji, M., Nussenzweig, M.C., Wardemann, H., Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329 (2008), 112–124.
52. Tomaras, G.D., Yates, N.L., Liu, P., Qin, L., Fouda, G.G., Chavez, L.L., Decamp, A.C., Parks, R.J., Ashley, V.C., Lucas, J.T., Cohen, M., Eron, J., Hicks, C.B., Liao, H.X., Self, S.G., Landucci, G., Forthal, D.N., Weinhold, K.J., Keele, B.F., Hahn, B.H., Greenberg, M.L., Morris, L., Karim, S.S., Blattner, W.A., Montefiori, D.C., Shaw, G.M., Perelson, A.S., Haynes, B.F., Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82 (2008), 12449–12463.
53. Vishwanathan, S.A., Hunter, E., Importance of the membrane-perturbing properties of the membrane-proximal external region of human immunodeficiency virus type 1 gp41 to viral fusion. J. Virol. 82 (2008), 5118–5126.
54. Watkins, B.A., Buge, S., Aldrich, K., Davis, A.E., Robinson, J., Reitz, M.S. JR., Robert-Guroff, M., Resistance of human immunodeficiency virus type 1 to neutralization by natural antisera occurs through single amino acid substitutions that cause changes in antibody binding at multiple sites. J. Virol. 70 (1996), 8431–8437.
55. 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., Komarova, N.L., Nowak, M.A., Hahn, B.H., Kwong, P.D., Shaw, G.M., Antibody neutralization and escape by HIV-1. Nature 422 (2003), 307–312.
56. Wiehe, K., Easterhoff, D., Luo, K., Nicely, N.I., Bradley, T., Jaeger, F.H., Dennison, S.M., Zhang, R.J., Lloyd, K.E., Stolarchuk, C., Parks, R., Sutherland, L.L., Scearce, R.M., Morris, L., Kaewkungwal, J., Nitayaphan, S., Pitisuttithum, P., Rerks-Ngarm, S., Sinangil, F., Phogat, S., Michael, N.L., Kim, J.H., Kelsoe, G., Montefiori, D.C., Tomaras, G.D., Bonsignori, M., Santra, S., Kepler, T.B., Alam, S.M., Moody, M.A., Liao, H.X., Haynes, B.F., Antibody light-chain-restricted recognition of the site of immune pressure in the RV144 HIV-1 vaccine trial is phylogenetically conserved. Immunity 41 (2014), 909–918.
57. Wu, X., Yang, Z.Y., Li, Y., Hogerkorp, C.M., Schief, W.R., seaman, M.S., Zhou, T., Schmidt, S.D., Wu, L., Xu, L., Longo, N.S., Mckee, K., O'dell, S., Louder, M.K., Wycuff, D.L., Feng, Y., Nason, M., Doria-Rose, N., Connors, M., Kwong, P.D., Roederer, M., Wyatt, R.T., Nabel, G.J., Mascola, J.R., Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329 (2010), 856–861.
58. Wyatt, R., Sodroski, J., The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 (1998), 1884–1888.
59. Zhang, R., Verkoczy, L., Wiehe, K., Munir Alam, S., Nicely, N.I., Santra, S., Bradley, T., Pemble, C.W.T., Zhang, J., Gao, F., Montefiori, D.C., Bouton-Verville, H., Kelsoe, G., Larimore, K., Greenberg, P.D., Parks, R., Foulger, A., Peel, J.N., Luo, K., Lu, X., Trama, A.M., Vandergrift, N., Tomaras, G.D., Kepler, T.B., Moody, M.A., Liao, H.X., Haynes, B.F., Initiation of immune tolerance-controlled HIV gp41 neutralizing B cell lineages. Sci. Transl. Med., 8, 2016, 336ra62.