Cross-neutralizing activity of human anti-V3 monoclonal antibodies derived from non-B clade HIV-1 infected individuals

Virology

Volumn 439, Issue 2, 2013, Pages 81-88

  Andrabi, Raiees ^a,c   Williams, Constance ^a   Wang, Xiao Hong ^b   Li, Liuzhe ^a   Choudhary, Alok K ^c   Wig, Naveet ^c   Biswas, Ashutosh ^c   Luthra, Kalpana ^c   Nadas, Arthur ^a   Seaman, Michael S ^d   Nyambi, Phillipe ^a,b   Zolla Pazner, Susan ^a,b   Gorny, Miroslaw K ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

HIV neutralizing antibodies; HIV 1; Human monoclonal antibodies; Immunoglobulin gene usage; Non B clade HIV 1; V3 region

Indexed keywords

GLYCOPROTEIN GP 120; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY V3; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CAMEROONIAN; CLADISTICS; CONTROLLED STUDY; CROSS REACTION; ETHNIC DIFFERENCE; ETHNIC GROUP; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENICITY; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOGLOBULIN LIGHT CHAIN GENE; INDIAN; MOLECULAR RECOGNITION; MUTATION RATE; PRIORITY JOURNAL; VIRUS NEUTRALIZATION;

ANTIBODIES, MONOCLONAL; CAMEROON; CROSS REACTIONS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; INDIA; NEUTRALIZATION TESTS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84875813058     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.12.010     Document Type: Article

References (38)

1. Almond D., Krachmarov C., Swetnam J., Zolla-Pazner S., Cardozo T. Resistance of subtype C HIV-1 strains to anti-V3 loop antibodies. Adv. Virol. 2012, 2012:803535.
2. Andrus L., Prince A.M., Bernal I., McCormack P., Lee D.H., Gorny M.K., Zolla-Pazner S. Passive immunization with a human immunodeficiency virus type-1 neutralizing monoclonal antibody in Hu-PBL-SCID mice: isolation of a neutralization escape variant. J. Infect. Dis. 1998, 177:889-897.
3. Corti D., Langedijk J.P., Hinz A., Seaman M.S., Vanzetta F., Fernandez-Rodriguez B.M., Silacci C., Pinna D., Jarrossay D., Balla-Jhagjhoorsingh S., Willems B., Zekveld M.J., Dreja H., O'Sullivan E., Pade C., Orkin C., Jeffs S.A., Montefiori D.C., Davis D., Weissenhorn W., McKnight A., Heeney J.L., Sallusto F., Sattentau Q.J., Weiss R.A., Lanzavecchia A. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PloS One 2010, 5:e8805.
4. Emini E.A., Schleif W.A., Nunberg J.H., Conley A.J., Eda Y., Tokiyoshi S., Putney S.D., Matsushita S., Cobb K.E., Jett C.M., Eichberg J.W., Murthy K.K. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 1992, 355:728-730.
5. Gigler A., Dorsch S., Hemauer A., Williams C., Kim S., Young N.S., Zolla-Pazner S., Wolf H., Gorny M.K., Modrow S. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 1999, 73:1974-1979.
6. Gorny M.K., Revesz K., Williams C., Volsky B., Louder M.K., Anyangwe C.A., Krachmarov C.P., Kayman S.C., Pinter A., Nadas A., Nyambi P.N., Mascola J.R., Zolla-Pazner S. The V3 loop is accessible on the surface of most human immunodeficiency virus type 1 primary isolates and serves as a neutralization epitope. J. Virol. 2004, 78:2394-2404.
7. Gorny M.K., Sampson J., Li H., Jiang X., Totrov M., Wang X.-H., Williams C., O'Neal T., Volsky B., Li L., Cardozo T., Nyambi P., Zolla-Pazner S., Kong X.-P. Human anti-V3 HIV-1 monoclonal antibodies encoded by the VH5-51/VL lambda genes define a conserved antigenic structure. PloS One 2011, 6:e27780.
8. Gorny M.K., VanCott T.C., Hioe C., Israel Z.R., Michael N.L., Conley A.J., Williams C., Kessler J.A., Chigurupati P., Burda S., Zolla-Pazner S. Human monoclonal antibodies to the V3 loop of HIV-1 with intra- and interclade cross-reactivity. J. Immunol. 1997, 159:5114-5122.
9. Gorny M.K., VanCott T.C., Williams C., Revesz K., Zolla-Pazner S. Effects of oligomerization on the epitopes of the human immunodeficiency virus type 1 envelope glycoproteins. Virology 2000, 267:220-228.
10. Gorny M.K., Wang X.H., Williams C., Volsky B., Revesz K., Witover B., Burda S., Urbanski M., Nyambi P., Krachmarov C., Pinter A., Zolla-Pazner S., Nadas A. Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol. Immunol. 2009, 46:917-926.
11. Gorny M.K., Williams C., Volsky B., Revesz K., Wang X.H., Burda S., Kimura T., Koning F.A., Nadas A., Anyangwe C., Nyambi P., Krachmarov C., Pinter A., Zolla-Pazner S. Cross-clade neutralizing activity of human anti-V3 monoclonal antibodies derived from the cells of individuals infected with non-B clades of HIV-1. J. Virol. 2006, 80:6865-6872.
12. Gorny M.K., Xu J.-Y., Gianakakos V., Karwowska S., Williams C., Sheppard H.W., Hanson C.V., Zolla-Pazner S. Production of site-selected neutralizing human monoclonal antibodies against the third variable domain of the HIV-1 envelope glycoprotein. Proc. Natl. Acad. Sci. USA 1991, 88:3238-3242.
13. Gorny M.K., Xu J.-Y., Karwowska S., Buchbinder A., Zolla-Pazner S. Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 1993, 150:635-643.
14. Haynes B.F., Gilbert P.B., McElrath M.J., Zolla-Pazner S., Tomaras G.D., Alam S.M., Evans D.T., Montefiori D.C., Karnasuta C., Sutthent R., Liao H.X., DeVico A.L., Lewis G.K., Williams C., Pinter A., Fong Y., Janes H., DeCamp A., Huang Y., Rao M., Billings E., Karasavvas N., Robb M.L., Ngauy V., de Souza M.S., Paris R., Ferrari G., Bailer R.T., Soderberg K.A., Andrews C., Berman P.W., Frahm N., De Rosa S.C., Alpert M.D., Yates N.L., Shen X., Koup R.A., Pitisuttithum P., Kaewkungwal J., Nitayaphan S., Rerks-Ngarm S., Michael N.L., Kim J.H. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 2012, 366:1275-1286.
15. Hioe C.E., Wrin T., Seaman M.S., Yu X., Wood B., Self S., Williams C., Gorny M.K., Zolla-Pazner S. Anti-V3 monoclonal antibodies display broad neutralizing activities against multiple HIV-1 subtypes. PloS One 2010, 5:e10254.
16. Jiang X., Burke V., Totrov M., Williams C., Cardozo T., Gorny M.K., Zolla-Pazner S., Kong X.-P. Conserved structural elements in the V3 crown of HIV-1 GP120. Nat. Struct. Mol. Biol. 2010, 17:955-961.
17. Letvin N.L., Robinson S., Rohne D., Axthelm M.K., Fanton J.W., Bilska M., Palker T.J., Liao H.X., Haynes B.F., Montefiori D.C. Vaccine-elicited V3 loop-specific antibodies in rhesus monkeys and control of a simian-human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate envelope. J. Virol. 2001, 75:4165-4175.
18. Li M., Gao F., Mascola J.R., Stamatatos L., Polonis V.R., Koutsoukos M., Voss G., Goepfert P., Gilbert P., Greene K.M., Bilska M., Kothe D.L., Salazar-Gonzalez J.F., Wei X., Decker J.M., Hahn B.H., Montefiori D.C. Human immunodeficiency virus type 1 env clones from acute and early subtype B Infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 2005, 79:10108-10125.
19. Montefiori D.C., Karnasuta C., Huang Y., Ahmed H., Gilbert P., de Souza M.S., McLinden R., Tovanabutra S., Laurence-Chenine A., Sanders-Buell E., Moody M.A., Bonsignori M., Ochsenbauer C., Kappes J., Tang H., Greene K., Gao H., Labranche C.C., Andrews C., Polonis V.R., Rerks-Ngarm S., Pitisuttithum P., Nitayaphan S., Kaewkungwal J., Self S.G., Berman P.W., Francis D., Sinangil F., Lee C., Tartaglia J., Robb M.L., Haynes B.F., Michael N.L., Kim J.H. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J. Infect. Dis. 2012, 206:431-441.
20. Moody M.A., Yates N.L., Amos J.D., Drinker M.S., Eudailey J.A., Gurley T.C., Marshall D.J., Whitesides J.F., Chen X., Foulger A., Yu J.S., Zhang R., Meyerhoff R.R., Parks R., Scull J.C., Wang L., Vandergrift N.A., Pickeral J., Pollara J., Kelsoe G., Alam S.M., Ferrari G., Montefiori D.C., Voss G., Liao H.X., Tomaras G.D., Haynes B.F. HIV-1 gp120 vaccine induces affinity maturation in both new and persistent antibody clonal lineages. J. Virol. 2012, 86:7496-7507.
21. Morris L., Cilliers T., Bredell H., Phoswa M., Martin D.J. CCR5 is the major coreceptor used by HIV-1 subtype C isolates from patients with active tuberculosis. AIDS Res. Hum. Retroviruses 2001, 17:697-701.
22. Osmanov S., Pattou C., Walker N., Schwardlander B., Esparza J. Estimated global distribution and regional spread of HIV-1 genetic subtypes in the year 2000. J. Acquir. Immune Defic. Syndr. 2002, 29:184-190.
23. Pantophlet R., Aguilar-Sino R.O., Wrin T., Cavacini L.A., Burton D.R. Analysis of the neutralization breadth of the anti-V3 antibody F425-B4e8 and re-assessment of its epitope fine specificity by scanning mutagenesis. Virology 2007, 364:441-453.
24. Patel M.B., Hoffman N.G., Swanstrom R. Subtype-specific conformational differences within the V3 region of subtype B and subtype C human immunodeficiency virus type 1 Env proteins. J. Virol. 2008, 82:903-916.
25. Peeters M., Vincent R., Perret J.L., Lasky M., Patrel D., Liegeois F., Courgnaud V., Seng R., Matton T., Molinier S., Delaporte E. Evidence for differences in MT2 cell tropism according to genetic subtypes of HIV-1: syncytium-inducing variants seem rare among subtype C HIV-1 viruses. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 1999, 20:115-121.
26. Rerks-Ngarm S., Pitisuttithum P., Nitayaphan S., Kaewkungwal J., Chiu J., Paris R., Premsri N., Namwat C., de Souza M., Adams E., Benenson M., Gurunathan S., Tartaglia J., McNeil J.G., Francis D.P., Stablein D., Birx D.L., Chunsuttiwat S., Khamboonruang C., Thongcharoen P., Robb M.L., Michael N.L., Kunasol P., Kim J.H. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 2009, 361:2209-2220.
27. Scheid J.F., Mouquet H., Feldhahn N., Seaman M.S., Velinzon K., Pietzsch J., Ott R.G., Anthony R.M., Zebroski H., Hurley A., Phogat A., Chakrabarti B., Li Y., Connors M., Pereyra F., Walker B.D., Wardemann H., Ho D., Wyatt R.T., Mascola J.R., Ravetch J.V., Nussenzweig M.C. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 2009, 458:636-640.
28. Scheid J.F., Mouquet H., Ueberheide B., Diskin R., Klein F., Olivera T.Y., Pietzsch J., Fenyo D., Abadir A., Velinzon K., Hurley A., Myung S., Boulad F., Poignard P., Burton D., Pereyra F., Ho D.D., Walker B.D., Seaman M.S., Bjorkman P.J., Chait B.T., Nussenzweig M.C. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 2011, 333:1633-1637.
29. 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. 2010, 84:1439-1452.
30. Teng N.N., Lam K.S., Calvo Riera F., Kaplan H.S. Construction and testing of mouse-human heteromyelomas for human monoclonal antibody production. Proc. Natl. Acad. Sci. USA 1983, 80:7308-7312.
31. Tiller T., Tsuiji M., Yurasov S., Velinzon K., Nussenzweig M.C., Wardemann H. Autoreactivity in human IgG+ memory B cells. Immunity 2007, 26:205-213.
32. Totrov M., Jiang X., Kong X.P., Cohen S., Krachmarov C., Salomon A., Williams C., Seaman M.S., Cardozo T., Gorny M.K., Wang S., Lu S., Pinter A., Zolla-Pazner S. Structure-guided design and immunological characterization of immunogens presenting the HIV-1 gp120 V3 loop on a CTB scaffold. Virology 2010, 405:513-523.
33. Traggiai E., Becker S., Subbarao K., Kolesnikova L., Uematsu Y., Gismondo M.R., Murphy B.R., Rappuoli R., Lanzavecchia A. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 2004, 10:871-875.
34. Walker L.M., Huber M., Doores K.J., Falkowska E., Pejchal R., Julien J.P., Wang S.K., Ramos A., Chan-Hui P.Y., Moyle M., Mitcham J.L., Hammond P.W., Olsen O.A., Phung P., Fling S., Wong C.H., Phogat S., Wrin T., Simek M.D., Principal Investigators P.G., Koff W.C., Wilson I.A., Burton D.R., Poignard P. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 2011, 477:466-470.
35. Walker L.M., Phogat S.K., Chan-Hui P.Y., Wagner D., Phung P., Goss J.L., Wrin T., Simek M.D., Fling S., Mitcham J.L., Lehrman J.K., Priddy F.H., Olsen O.A., Frey S.M., Hammond P.W., Miiro G., Serwanga J., Pozniak A., McPhee D., Manigart O., Mwananyanda L., Karita E., Inwoley A., Jaoko W., Dehovitz J., Bekker L.G., Pitisuttithum P., Paris R., Allen S., Kaminsky S., Zamb T., Moyle M., Koff W.C., Poignard P., Burton D.R. Broad and potent neutralizing antibodies from an african donor reveal a new HIV-1 vaccine target. Science 2009, 326:285-289.
36. Watkins J.D., Siddappa N.B., Lakhashe S.K., Humbert M., Sholukh A., Hemashettar G., Wong Y.L., Yoon J.K., Wang W., Novembre F.J., Villinger F., Ibegbu C., Patel K., Corti D., Agatic G., Vanzetta F., Bianchi S., Heeney J.L., Sallusto F., Lanzavecchia A., Ruprecht R.M. An anti-HIV-1 V3 loop antibody fully protects cross-clade and elicits T-cell immunity in macaques mucosally challenged with an R5 clade C SHIV. PloS One 2011, 6:e18207.
37. 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 2010, 329:856-861.
38. Zolla-Pazner S., Kong X., Jiang X., Cardozo T., Nadas A., Cohen S., Totrov M., Seaman M.S., Wang S., Lu S. Cross-clade HIV-1 neutralizing antibodies induced with V3-scaffold protein immunogens following priming with gp120 DNA. J. Virol. 2011, 85:9887-9898.