Rapid isolation of dengue-neutralizing antibodies from single cell-sorted human antigen-specific memory B-cell cultures

mAbs

Volumn 8, Issue 1, 2016, Pages 129-140

  Cox, Kara S ^a,b   Tang, Aimin ^a,b   Chen, Zhifeng ^a,b   Horton, Melanie S ^a,b   Yan, Hao ^a,b   Wang, Xin Min ^a,b   Dubey, Sheri A ^a,b   Distefano, Daniel J ^a,b   Ettenger, Andrew ^c   Fong, Rachel H ^c   Doranz, Benjamin J ^c   Casimiro, Danilo R ^a,b   Vora, Kalpit A ^a,b  

^a Department of Infectious Diseases and Vaccines West Point ^*  (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c Integral Molecular Inc   (United States)

Author keywords

Antigen specific; Cell sorting; Dengue virus; Memory B cell; Vaccine

Indexed keywords

CD40 LIGAND; DENGUE VACCINE; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; RECOMBINANT ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRUS ANTIBODY;

ANIMAL CELL; ANTIBODY ISOLATION; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; B CELL CULTURE; CELL SPECIFICITY; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYBRIDOMA CELL LINE; IMMUNE RESPONSE; MEMORY CELL; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; VACCINATION; VERO CELL LINE; VIRUS NEUTRALIZATION; WESTERN BLOTTING; B LYMPHOCYTE; CELL CULTURE TECHNIQUE; CYTOLOGY; DENGUE VIRUS; FEMALE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MALE;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CELL CULTURE TECHNIQUES; DENGUE VIRUS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC MEMORY; MALE; VIRAL ENVELOPE PROTEINS;

EID: 84964474595     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2015.1109757     Document Type: Article

References (40)

1. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002; 298:2199-202; PMID:12481138; http://dx.doi.org/10.1126/science.1076071
2. Plotkin SA. Correlates of protection induced by vaccination. Clin Vaccine Immunol 2010; 17:1055-65; PMID:20463105; http://dx.doi.org/10.1128/CVI.00131-10
3. Amanna IJ, Carlson NE, Slifka MK. Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med 2007; 357:1903-15; PMID:17989383; http://dx.doi.org/10.1056/NEJMoa066092
4. Blanchard Rohner G, Snape MD, Kelly DF, John T, Morant A, Yu LM, Borkowski A, Ceddia F, Borrow R, Siegrist CA, et al. The magnitude of the antibody and memory B cell responses during priming with a proteinpolysaccharide conjugate vaccine in human infants is associated with the persistence of antibody and the intensity of booster response. J Immunol 2008; 180:2165-73; http://dx.doi.org/10.4049/jimmunol.180.4.2165
5. Scherer EM, Smith RA, Simonich CA, Niyonzima N, Carter JJ, Galloway DA. Characteristics of memory B cells elicited by a highly efficacious HPV vaccine in subjects with no pre-existing immunity. PLoS Pathogens 2014; 10:e1004461; PMID:25330199; http://dx.doi. org/10.1371/journal.ppat.1004461
6. Leyendeckers H, Odendahl M, Lohndorf A, Irsch J, Spangfort M, Miltenyi S, Hunzelmann N, Assenmacher M, Radbruch A, Schmitz J. Correlation analysis between frequencies of circulating antigenspecific IgG-bearing memory B cells and serum titers of antigen-specific IgG. Eur J Immunol 1999; 29:1406-17; PMID:10229109; http://dx.doi.org/10.1002/(SICI)1521-4141(199904)29:04%3c1406: AID-IMMU1406%3e3.0.CO;2-P
7. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, Larsen C, Zheng NY, Mays I, Garman L, Helms C, et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 2008; 453:667-71; PMID:18449194; http://dx.doi.org/10.1038/nature06890
8. Smith SA, Zhou Y, Olivarez NP, Broadwater AH, de Silva AM, Crowe JE, Jr. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J Virol 2012; 86:2665-75; PMID:22171265; http://dx. doi.org/10.1128/JVI.06335-11
9. Smith SA, de Alwis AR, Kose N, Jadi RS, de Silva AM, Crowe JE, Jr. Isolation of dengue virus-specific memory B cells with live virus antigen from human subjects following natural infection reveals the presence of diverse novel functional groups of antibody clones. J Virol 2014; 88:12233-41; PMID:25100837; http://dx.doi.org/10.1128/JVI.00247-14
10. Huang J, Doria-Rose NA, Longo NS, Laub L, Lin CL, Turk E, Kang BH, Migueles SA, Bailer RT, Mascola JR, et al. Isolation of human monoclonal antibodies from peripheral blood B cells. Nat Proto 2013; 8:1907-15; PMID:24030440; http://dx.doi.org/10.1038/nprot.2013.117
11. Roehrig JT. Antigenic structure of flavivirus proteins. Adv Virus Res 2003; 59:141-75; PMID:14696329; http://dx.doi.org/10.1016/S0065-3527(03)59005-4
12. Coller BA, Clements DE, Bett AJ, Sagar SL, Ter Meulen JH. The development of recombinant subunit envelope-based vaccines to protect against dengue virus induced disease. Vaccine 2011; 29:7267-75; PMID:21777637; http://dx.doi.org/10.1016/j. vaccine.2011.07.021
13. Amanna IJ, Slifka MK. Quantitation of rare memory B cell populations by two independent and complementary approaches. J Immunol Methods 2006; 317:175-85; PMID:17055526; http://dx.doi.org/10.1016/j. jim.2006.09.005
14. Agematsu K, Nagumo H, Yang FC, Nakazawa T, Fukushima K, Ito S, Sugita K, Mori T, Kobata T, Morimoto C, et al. B cell subpopulations separated by CD27 and crucial collaboration of CD27+ B cells and helper T cells in immunoglobulin production. Eur J Immunol 1997; 27:2073-9; PMID:9295047; http://dx.doi.org/10.1002/eji.1830270835
15. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998; 188:1679-89; PMID:9802980; http://dx.doi.org/10.1084/jem.188.9.1679
16. Vita R, Overton JA, Greenbaum JA, Ponomarenko J, Clark JD, Cantrell JR, Wheeler DK, Gabbard JL, Hix D, Sette A, et al. The immune epitope database (IEDB) 3.0. Nucl Acids Res 2015; 43:D405-12; PMID:25300482; http://dx.doi.org/10.1093/nar/gku938
17. Christian EA, Kahle KM, Mattia K, Puffer BA, Pfaff JM, Miller A, Paes C, Davidson E, Doranz BJ. Atomiclevel functional model of dengue virus Envelope protein infectivity. Proc Natl Acad Sci U S A 2013; 110:18662-7; PMID:24158478; http://dx.doi.org/10.1073/pnas.1310962110
18. Cockburn JJ, Navarro Sanchez ME, Goncalvez AP, Zaitseva E, Stura EA, Kikuti CM, Duquerroy S, Dussart P, Chernomordik LV, Lai CJ, et al. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. EMBO J 2012; 31:767-79; PMID:22139356; http://dx.doi.org/10.1038/emboj.2011.439
19. Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, Williams KL, Johnson S, Rico-Hesse R, Harris E, Pierson TC, et al. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 2010; 84:9227-39; PMID:20592088; http://dx.doi.org/10.1128/JVI.01087-10
20. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 2002; 108:717-25; PMID:11893341; http://dx.doi.org/10.1016/S0092-8674(02)00660-8
21. Zhang X, Ge P, Yu X, Brannan JM, Bi G, Zhang Q, Schein S, Zhou ZH. Cryo-EM structure of the mature dengue virus at 3.5-A resolution. Nat Struct Mol Biol 2013; 20:105-10; PMID:23241927; http://dx.doi.org/10.1038/nsmb.2463
22. Messer WB, de Alwis R, Yount BL, Royal SR, Huynh JP, Smith SA, Crowe JE, Jr., Doranz BJ, Kahle KM, Pfaff JM, et al. Dengue virus envelope protein domain I/II hinge determines long-lived serotype-specific dengue immunity. Proc Natl Acad Sci U S A 2014; 111:1939-44; PMID:24385585; http://dx.doi.org/10.1073/pnas.1317350111
23. Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X, Rouvinski A, Jumnainsong A, Edwards C, Quyen NT, Duangchinda T, et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 2015; 16:170-7; PMID:25501631; http://dx.doi.org/10.1038/ni.3058
24. Fibriansah G, Ibarra KD, Ng TS, Smith SA, Tan JL, Lim XN, Ooi JS, Kostyuchenko VA, Wang J, de Silva AM, et al. DENGUE VIRUS. Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers. Science 2015; 349:88-91; PMID:26138979; http://dx.doi.org/10.1126/science. aaa8651
25. Wahala WM, Kraus AA, Haymore LB, Accavitti-Loper MA, de Silva AM. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 2009; 392:103-13; PMID:19631955; http://dx.doi.org/10.1016/j. virol.2009.06.037
26. Costin JM, Zaitseva E, Kahle KM, Nicholson CO, Rowe DK, Graham AS, Bazzone LE, Hogancamp G, Figueroa Sierra M, Fong RH, et al. Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. J Virol 2013; 87:52-66; PMID:23077306; http://dx.doi.org/10.1128/JVI.02273-12
27. Fibriansah G, Tan JL, Smith SA, de Alwis AR, Ng TS, Kostyuchenko VA, Ibarra KD, Wang J, Harris E, de Silva A, et al. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol Med 2014; 6:358-71; PMID:24421336
28. Wodak SJ, Malevanets A, MacKinnon SS. The Landscape of Intertwined Associations in Homooligomeric Proteins. Biophys J 2015; 109:1087-100; PMID:26340815; http://dx.doi.org/10.1016/j.bpj.2015.08.010
29. Robert Putnak J, Coller BA, Voss G, Vaughn DW, Clements D, Peters I, Bignami G, Houng HS, Chen RC, Barvir DA, et al. An evaluation of dengue type-2 inactivated, recombinant subunit, and live-attenuated vaccine candidates in the rhesus macaque model. Vaccine 2005; 23:4442-52; PMID:16005749; http://dx. doi.org/10.1016/j.vaccine.2005.03.042
30. Clements DE, Coller BA, Lieberman MM, Ogata S, Wang G, Harada KE, Putnak JR, Ivy JM, McDonell M, Bignami GS, et al. Development of a recombinant tetravalent dengue virus vaccine: immunogenicity and efficacy studies in mice and monkeys. Vaccine 2010; 28:2705-15; PMID:20097152; http://dx.doi.org/10.1016/j.vaccine.2010.01.022
31. Rojas OL, Narvaez CF, Greenberg HB, Angel J, Franco MA. Characterization of rotavirus specific B cells and their relation with serological memory. Virology 2008; 380:234-42; PMID:18789807; http://dx.doi.org/10.1016/j.virol.2008.08.004
32. Scheid JF, Mouquet H, Feldhahn N, Walker BD, Pereyra F, Cutrell E, Seaman MS, Mascola JR, Wyatt RT, Wardemann H, et al. A method for identification of HIV gp140 binding memory B cells in human blood. J Immunol Methods 2009; 343:65-7; PMID:19100741; http://dx.doi.org/10.1016/j.jim.2008.11.012
33. Bryant VL, Ma CS, Avery DT, Li Y, Good KL, Corcoran LM, de Waal Malefyt R, Tangye SG. Cytokinemediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells. J Immunol 2007; 179:8180-90; http://dx.doi.org/10.4049/jimmunol.179.12.8180
34. Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS, Spolski R, Leonard WJ, Lipsky PE. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005; 175:7867-79; http://dx.doi.org/10.4049/jimmunol.175.12.7867
35. Kwakkenbos MJ, Diehl SA, Yasuda E, Bakker AQ, van Geelen CM, Lukens MV, van Bleek GM, Widjojoatmodjo MN, Bogers WM, Mei H, et al. Generation of stable monoclonal antibody-producing B cell receptorpositive human memory B cells by genetic programming. Nat Med 2010; 16:123-8; PMID:20023635; http://dx.doi.org/10.1038/nm.2071
36. Crotty S, Aubert RD, Glidewell J, Ahmed R. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 2004; 286:111-22; PMID:15087226; http://dx.doi. org/10.1016/j.jim.2003.12.015
37. Smith K, Garman L, Wrammert J, Zheng NY, Capra JD, Ahmed R, Wilson PC. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat Proto 2009; 4:372-84; PMID:19247287; http://dx.doi.org/10.1038/nprot.2009.3
38. Collarini EJ, Lee FE, Foord O, Park M, Sperinde G, Wu H, Harriman WD, Carroll SF, Ellsworth SL, Anderson LJ, et al. Potent high-affinity antibodies for treatment and prophylaxis of respiratory syncytial virus derived from B cells of infected patients. J Immunol 2009; 183:6338-45; http://dx.doi.org/10.4049/jimmunol.0901373
39. Davidson E, Doranz BJ. A high-throughput shotgun mutagenesis approach to mapping B-cell antibody epitopes. Immunology 2014; 143:13-20; PMID:24854488; http://dx.doi.org/10.1111/imm.12323
40. Modis Y, Ogata S, Clements D, Harrison SC. A ligandbinding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci U S A 2003; 100:6986-91; PMID:12759475; http://dx.doi.org/10.1073/pnas.0832193100