Plasmablasts During Acute Dengue Infection Represent a Small Subset of a Broader Virus-specific Memory B Cell Pool

EBioMedicine

Volumn 12, Issue , 2016, Pages 178-188

  Appanna, Ramapraba ^a   KG, Srinivasan ^a   Xu, Mei Hui ^a   Toh, Ying Xiu ^a   Velumani, Sumathy ^a   Carbajo, Daniel ^a   Lee, Chia Yin ^a   Zuest, Roland ^a   Balakrishnan, Thavamalar ^a   Xu, Weili ^a   Lee, Bernett ^a   Poidinger, Michael ^a   Zolezzi, Francesca ^a,d   Leo, Yee Sin ^b,c   Thein, Tun Linn ^b   Wang, Cheng I ^a   Fink, Katja ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b TAN TOCK SENG HOSPITAL   (Singapore)

^c Dept Medicine Endocrinol Diabet   (Singapore)

^d GALDERMA R D   (Spain)

Author keywords

Antibodies; Dengue; Memory B cells; Plasmablasts

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN VARIABLE REGION; VIRUS ANTIBODY; VIRUS ANTIGEN;

ADULT; ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE ACTIVATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; DENGUE VIRUS 3; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MEMORY CELL; MOLECULAR CLONING; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PLASMABLAST; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; VIRUS NEUTRALIZATION; WESTERN BLOTTING; ACUTE DISEASE; ANIMAL; B LYMPHOCYTE; CELL LINE; CLONAL EVOLUTION; CROSS REACTION; DENGUE VIRUS; GENETICS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PHENOTYPE; PLASMA CELL; SERODIAGNOSIS; VIROLOGY;

ACUTE DISEASE; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; B-LYMPHOCYTE SUBSETS; CELL LINE; CLONAL EVOLUTION; CROSS REACTIONS; DENGUE; DENGUE VIRUS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; NEUTRALIZATION TESTS; PHENOTYPE; PLASMA CELLS;

EID: 84992573946     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.09.003     Document Type: Article

References (48)

1. 1 Bhatt, S., Gething, P.W., Brady, O.J., et al. The global distribution and burden of dengue. Nature 496:7446 (2013), 504–507.
2. 2 de Alwis, R., Smith, S.A., Olivarez, N.P., et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl. Acad. Sci. U. S. A. 109:19 (2012), 7439–7444.
3. 3 Lai, C.Y., Williams, K.L., Wu, Y.C., et al. Analysis of cross-reactive antibodies recognizing the fusion loop of envelope protein and correlation with neutralizing antibody titers in Nicaraguan dengue cases. PLoS Negl. Trop. Dis., 7(9), 2013, e2451.
4. 4 Lin, H.E., Tsai, W.Y., Liu, I.J., et al. Analysis of epitopes on dengue virus envelope protein recognized by monoclonal antibodies and polyclonal human sera by a high throughput assay. PLoS Negl. Trop. Dis., 6(1), 2012, e1447.
5. 5 Halstead, S.B., Rojanasuphot, S., Sangkawibha, N., Original antigenic sin in dengue. Am.J.Trop. Med. Hyg. 32:1 (1983), 154–156.
6. 6 Midgley, C.M., Bajwa-Joseph, M., Vasanawathana, S., et al. An in-depth analysis of original antigenic sin in dengue virus infection. J. Virol. 85:1 (2010), 410–421.
7. 7 Wrammert, J., Onlamoon, N., Akondy, R.S., et al. Rapid and massive virus-specific plasmablast responses during acute dengue virus infection in humans. J. Virol. 86:6 (2012), 2911–2918.
8. 8 Xu, M., Hadinoto, V., Appanna, R., et al. Plasmablasts generated during repeated dengue infection are virus glycoprotein-specific and bind to multiple virus serotypes. J. Immunol. 189:12 (2012), 5877–5885.
9. 9 Balakrishnan, T., Bela-Ong, D.B., Toh, Y.X., et al. Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection. PLoS One, 6(12), 2011, e29430.
10. 10 Toh, Y.X., Gan, V., Balakrishnan, T., et al. Dengue serotype cross-reactive, anti-e protein antibodies confound specific immune memory for 1 year after infection. Front. Immunol., 5, 2014, 388.
11. 11 Beltramello, M., Williams, K.L., Simmons, C.P., et al. The human immune response to dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8:3 (2010), 271–283.
12. 12 de Alwis, R., Beltramello, M., Messer, W.B., et al. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl. Trop. Dis., 5(6), 2011, e1188.
13. 13 Schieffelin, J.S., Costin, J.M., Nicholson, C.O., et al. Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol. J., 7, 2010, 28.
14. 14 Dejnirattisai, W., Jumnainsong, A., Onsirisakul, N., et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328:5979 (2010), 745–748.
15. 15 Dogan, I., Bertocci, B., Vilmont, V., et al. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10:12 (2009), 1292–1299.
16. 16 Pape, K.A., Taylor, J.J., Maul, R.W., Gearhart, P.J., Jenkins, M.K., Different B cell populations mediate early and late memory during an endogenous immune response. Science 331:6021 (2011), 1203–1207.
17. 17 Paus, D., Phan, T.G., Chan, T.D., Gardam, S., Basten, A., Brink, R., Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203:4 (2006), 1081–1091.
18. 18 Chan, T.D., Gatto, D., Wood, K., Camidge, T., Basten, A., Brink, R., Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183:5 (2009), 3139–3149.
19. 19 Fink, K., Manjarrez-Orduno, N., Schildknecht, A., et al. B cell activation state-governed formation of germinal centers following viral infection. J. Immunol. 179:9 (2007), 5877–5885.
20. 20 Zellweger, R.M., Hangartner, L., Weber, J., Zinkernagel, R.M., Hengartner, H., Parameters governing exhaustion of rare T cell-independent neutralizing IgM-producing B cells after LCMV infection. Eur. J. Immunol. 36:12 (2006), 3175–3185.
21. 21 Hangartner, L., Zinkernagel, R.M., Hengartner, H., Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6:3 (2006), 231–243.
22. 22 Nakaya, H.I., Wrammert, J., Lee, E.K., et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12:8 (2011), 786–795.
23. 23 Pauli, N.T., Kim, H.K., Falugi, F., et al. Staphylococcus aureus Infection induces protein A-mediated immune evasion in humans. J. Exp. Med. 211:12 (2014), 2331–2339.
24. 24 Querec, T.D., Akondy, R.S., Lee, E.K., et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10:1 (2009), 116–125.
25. 25 Reddy, S.T., Ge, X., Miklos, A.E., et al. Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells. Nat. Biotechnol. 28:9 (2010), 965–969.
26. 26 Smith, K., Garman, L., Wrammert, J., et al. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat. Protoc. 4:3 (2009), 372–384.
27. 27 Lavinder, J.J., Wine, Y., Giesecke, C., et al. Identification and characterization of the constituent human serum antibodies elicited by vaccination. Proc. Natl. Acad. Sci. U. S. A. 111:6 (2014), 2259–2264.
28. 28 Berkowska, M.A., Driessen, G.J., Bikos, V., et al. Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways. Blood 118:8 (2011), 2150–2158.
29. 29 Zaitseva, E., Yang, S.T., Melikov, K., Pourmal, S., Chernomordik, L.V., Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog., 6(10), 2010, e1001131.
30. 30 Durocher, Y., Perret, S., Kamen, A., High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res., 30(2), 2002, E9.
31. 31 Lefranc, M.P., Giudicelli, V., Ginestoux, C., et al. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 27:1 (1999), 209–212.
32. 32 Wang, C., Sanders, C.M., Yang, Q., et al. High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl. Acad. Sci. U. S. A. 107:4 (2010), 1518–1523.
33. 33 Bolotin, D.A., Poslavsky, S., Mitrophanov, I., et al. MiXCR: software for comprehensive adaptive immunity profiling. Nat. Methods 12:5 (2015), 380–381.
34. 34 Hershberg, U., Luning Prak, E.T., The analysis of clonal expansions in normal and autoimmune B cell repertoires. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 370(1676), 2015.
35. 35 Yousfi Monod, M., Giudicelli, V., Chaume, D., Lefranc, M.P., IMGT/JunctionAnalysis: the first tool for the analysis of the immunoglobulin and T cell receptor complex V-J and V-D-J JUNCTIONs. Bioinformatics 20:Suppl 1 (2004), i379–i385.
36. 36 Wrammert, J., Koutsonanos, D., Li, G.M., et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208:1 (2011), 181–193.
37. 37 Tan, Y.C., Blum, L.K., Kongpachith, S., et al. High-throughput sequencing of natively paired antibody chains provides evidence for original antigenic sin shaping the antibody response to influenza vaccination. Clin. Immunol. 151:1 (2014), 55–65.
38. 38 Jiang, N., He, J., Weinstein, J.A., et al. Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med., 5(171), 2013, 171ra19.
39. 39 Smith, S.A., de Alwis, A.R., Kose, N., Jadi, R.S., de Silva, A.M., JE, C. 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.
40. 40 Dejnirattisai, W., Wongwiwat, W., Supasa, S., et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 16:2 (2015), 170–177.
41. 41 Fibriansah, G., Tan, J.L., Smith, S.A., et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun., 6, 2015, 6341.
42. 42 Teoh, E.P., Kukkaro, P., Teo, E.W., et al. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med., 4(139), 2012, 139ra83.
43. 43 Wu, Y.C., Kipling, D., Leong, H.S., Martin, V., Ademokun, A.A., Dunn-Walters, D.K., High-throughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 116:7 (2010), 1070–1078.
44. 44 Warsame, A.A., Aasheim, H.C., Nustad, K., et al. Splenic marginal zone lymphoma with VH1-02 gene rearrangement expresses poly- and self-reactive antibodies with similar reactivity. Blood 118:12 (2011), 3331–3339.
45. 45 Cappione, A. 3rd, Anolik, J.H., Pugh-Bernard, A., et al. Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J. Clin. Invest. 115:11 (2005), 3205–3216.
46. 46 Potter, K.N., Hobby, P., Klijn, S., Stevenson, F.K., Sutton, B.J., Evidence for involvement of a hydrophobic patch in framework region 1 of human V4-34-encoded Igs in recognition of the red blood cell I antigen. J. Immunol. 169:7 (2002), 3777–3782.
47. 47 Fibriansah, G., Tan, J.L., Smith, S.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. 6:3 (2014), 358–371.
48. 48 Yoshida, T., Mei, H., Dorner, T., et al. Memory B and memory plasma cells. Immunol. Rev. 237:1 (2010), 117–139.