Single-cell and deep sequencing of IgG-switched macaque B cells reveal a diverse Ig repertoire following immunization

Journal of Immunology

Volumn 192, Issue 8, 2014, Pages 3637-3644

  Sundling, Christopher ^a   Zhang, Zhenhai ^b,c   Phad, Ganesh E ^a   Sheng, Zizhang ^b   Wang, Yimeng ^d   Mascola, John R ^e   Li, Yuxing ^d   Wyatt, Richard T ^d   Shapiro, Lawrence ^b   Hedestam, Gunilla B Karlsson ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Department of Biochemistry and Molecular Biophysics Columbia University ^*  (United States)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; B-LYMPHOCYTES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV ANTIBODIES; HIV-1; IMMUNIZATION; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOGLOBULINS; IMMUNOLOGIC MEMORY; MACACA MULATTA; MOLECULAR SEQUENCE DATA; SINGLE-CELL ANALYSIS;

EID: 84898652113     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303334     Document Type: Article

References (50)

1. Sela-Culang, I., V. Kunik, and Y. Ofran. 2013. The structural basis of antibodyantigen recognition. Front. Immunol. 4: 302.
2. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129.
3. Tangye, S. G., and D. M. Tarlinton. 2009. Memory B cells: effectors of longlived immune responses. Eur. J. Immunol. 39: 2065-2075.
4. Good, K. L., D. T. Avery, and S. G. Tangye. 2009. Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells. J. Immunol. 182: 890-901.
5. Martin, S. W., and C. C. Goodnow. 2002. Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 3: 182-188.
6. 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.
7. Poulsen, T. R., A. Jensen, J. S. Haurum, and P. S. Andersen. 2011. Limits for antibody affinity maturation and repertoire diversification in hypervaccinated humans. J. Immunol. 187: 4229-4235.
8. Poulsen, T. R., P. J. Meijer, A. Jensen, L. S. Nielsen, and P. S. Andersen. 2007. Kinetic, affinity, and diversity limits of human polyclonal antibody responses against tetanus toxoid. J. Immunol. 179: 3841-3850.
9. 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.
10. Wu, X., Z. Y. Yang, Y. Li, C. M. Hogerkorp, W. R. Schief, M. S. Seaman, T. Zhou, S. D. Schmidt, L. Wu, L. Xu, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
11. Sundling, C., Y. Li, N. Huynh, C. Poulsen, R. Wilson, S. O'Dell, Y. Feng, J. R. Mascola, R. T. Wyatt, and G. B. Karlsson Hedestam. 2012. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci. Transl. Med. 4: 142ra196.
12. Sundling, C., M. N. Forsell, S. O'Dell, Y. Feng, B. Chakrabarti, S. S. Rao, K. Loré, J. R. Mascola, R. T. Wyatt, I. Douagi, and G. B. Karlsson Hedestam. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207: 2003-2017.
13. Yang, X., J. Lee, E. M. Mahony, P. D. Kwong, R. Wyatt, and J. Sodroski. 2002. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76: 4634-4642.
14. Sundling, C., G. Phad, I. Douagi, M. Navis, and G. B. Karlsson Hedestam. 2012. Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J. Immunol. Methods 386: 85-93.
15. Tiller, T., E. Meffre, S. Yurasov, M. Tsuiji, M. C. Nussenzweig, and H. Wardemann. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329: 112-124.
16. 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.
17. Ye, J., N. Ma, T. L. Madden, and J. M. Ostell. 2013. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41(Web Server issue): W34-40.
18. Li, W., and A. Godzik. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
19. Alamyar, E., V. Giudicelli, S. Li, P. Duroux, and M. P. Lefranc. 2012. IMGT/ HighV-QUEST: the IMGT(R) web portal for immunoglobulin (IG) or antibody and T cell receptor (TR) analysis from NGS high throughput and deep sequencing. Immunome Res. 8: 26.
20. Rogosch, T., S. Kerzel, K. H. Hoi, Z. Zhang, R. F. Maier, G. C. Ippolito, and M. Zemlin. 2012. Immunoglobulin analysis tool: a novel tool for the analysis of human and mouse heavy and light chain transcripts. Front. Immunol. 3: 176.
21. Arnaout, R., W. Lee, P. Cahill, T. Honan, T. Sparrow, M. Weiand, C. Nusbaum, K. Rajewsky, and S. B. Koralov. 2011. High-resolution description of antibody heavy-chain repertoires in humans. PLoS ONE 6: e22365.
22. Morgan, C., M. Marthas, C. Miller, A. Duerr, C. Cheng-Mayer, R. Desrosiers, J. Flores, N. Haigwood, S. L. Hu, R. P. Johnson, et al. 2008. The use of nonhuman primate models in HIV vaccine development. PLoS Med. 5: e173.
23. Shedlock, D. J., G. Silvestri, and D. B. Weiner. 2009. Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat. Rev. Immunol. 9: 717-728.
24. Staprans, S. I., M. B. Feinberg, J. W. Shiver, and D. R. Casimiro. 2010. Role of nonhuman primates in the evaluation of candidate AIDS vaccines: an industry perspective. Curr. Opin. HIV AIDS 5: 377-385.
25. Gibbs, R. A., J. Rogers, M. G. Katze, R. Bumgarner, G. M. Weinstock, E. R. Mardis, K. A. Remington, R. L. Strausberg, J. C. Venter, R. K. Wilson, et al Rhesus Macaque Genome Sequencing and Analysis Consortium. 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222-234.
26. Larimore, K., M. W. McCormick, H. S. Robins, and P. D. Greenberg. 2012. Shaping of human germline IgH repertoires revealed by deep sequencing. J. Immunol. 189: 3221-3230.
27. 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.
28. Zhou, T., J. Zhu, X. Wu, S. Moquin, B. Zhang, P. Acharya, I. S. Georgiev, H. R. Altae-Tran, G. Y. Chuang, M. G. Joyce, et al NISC Comparative Sequencing Program. 2013. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39: 245-258.
29. Zhu, J., S. O'Dell, G. Ofek, M. Pancera, X. Wu, B. Zhang, Z. Zhang, J. C. Mullikin, M. Simek, D. R. Burton, et al NISC Comparative Sequencing Program. 2012. Somatic populations of PGT135-137 HIV-1-neutralizing antibodies identified by 454 pyrosequencing and bioinformatics. Front. Microbiol. 3: 315.
30. Zhu, J., G. Ofek, Y. Yang, B. Zhang, M. K. Louder, G. Lu, K. McKee, M. Pancera, J. Skinner, Z. Zhang, et al NISC Comparative Sequencing Program. 2013. Mining the antibodyome for HIV-1-neutralizing antibodies with nextgeneration sequencing and phylogenetic pairing of heavy/light chains. Proc. Natl. Acad. Sci. USA 110: 6470-6475.
31. Zhu, J., X. Wu, B. Zhang, K. McKee, S. O'Dell, C. Soto, T. Zhou, J. P. Casazza, J. C. Mullikin, P. D. Kwong, et al NISC Comparative Sequencing Program. 2013. De novo identification of VRC01 class HIV-1-neutralizing antibodies by next-generation sequencing of B-cell transcripts. Proc. Natl. Acad. Sci. USA 110: E4088-E4097.
32. Vollmers, C., R. V. Sit, J. A. Weinstein, C. L. Dekker, and S. R. Quake. 2013. Genetic measurement of memory B-cell recall using antibody repertoire sequencing. Proc. Natl. Acad. Sci. USA 110: 13463-13468.
33. Briney, B. S., J. R. Willis, and J. E. Crowe, Jr. 2012. Human peripheral blood antibodies with long HCDR3s are established primarily at original recombination using a limited subset of germline genes. PLoS ONE 7: e36750.
34. Briney, B. S., J. R. Willis, M. D. Hicar, J. W. Thomas, II, and J. E. Crowe, Jr. 2012. Frequency and genetic characterization of V(DD)J recombinants in the human peripheral blood antibody repertoire. Immunology 137: 56-64.
35. Briney, B. S., J. R. Willis, B. A. McKinney, and J. E. Crowe, Jr. 2012. Highthroughput antibody sequencing reveals genetic evidence of global regulation of the naïve and memory repertoires that extends across individuals. Genes Immun. 13: 469-473.
36. DeKosky, B. J., G. C. Ippolito, R. P. Deschner, J. J. Lavinder, Y. Wine, B. M. Rawlings, N. Varadarajan, C. Giesecke, T. Dörner, S. F. Andrews, et al. 2013. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat. Biotechnol. 31: 166-169.
37. Wu, Y. C., D. Kipling, and D. K. Dunn-Walters. 2012. Age-related changes in human peripheral blood IGH repertoire following vaccination. Front. Immunol. 3: 193.
38. Wu, Y. C., D. Kipling, H. S. Leong, V. Martin, A. A. Ademokun, and D. K. Dunn-Walters. 2010. High-throughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 116: 1070-1078.
39. Mathonet, P., and C. G. Ullman. 2013. The application of next generation sequencing to the understanding of antibody repertoires. Front. Immunol. 4: 265.
40. Margolin, D. H., K. A. Reimann, J. Sodroski, G. B. Karlsson, K. Tenner-Racz, P. Racz, and N. L. Letvin. 1997. Immunoglobulin V(H) usage during primary infection of rhesus monkeys with chimeric simian-human immunodeficiency viruses. J. Virol. 71: 8582-8591.
41. Andris, J. S., A. B. Miller, S. R. Abraham, S. Cunningham, F. Roubinet, A. Blancher, and J. D. Capra. 1997. Variable region gene segment utilization in rhesus monkey hybridomas producing human red blood cell-specific antibodies: predominance of the VH4 family but not VH4-21 (V4-34). Mol. Immunol. 34: 237-253.
42. Bible, J. M., W. Howard, H. Robbins, and D. K. Dunn-Walters. 2003. IGHV1, IGHV5 and IGHV7 subgroup genes in the rhesus macaque. Immunogenetics 54: 867-873.
43. Margolin, D. H., E. H. Saunders, B. Bronfin, N. de Rosa, M. K. Axthelm, O. G. Goloubeva, S. Eapen, R. S. Gelman, and N. L. Letvin. 2006. Germinal center function in the spleen during simian HIV infection in rhesus monkeys. J. Immunol. 177: 1108-1119.
44. Klein, F., R. Diskin, J. F. Scheid, C. Gaebler, H. Mouquet, I. S. Georgiev, M. Pancera, T. Zhou, R. B. Incesu, B. Z. Fu, et al. 2013. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153: 126-138.
45. Breden, F., C. Lepik, N. S. Longo, M. Montero, P. E. Lipsky, and J. K. Scott. 2011. Comparison of antibody repertoires produced by HIV-1 infection, other chronic and acute infections, and systemic autoimmune disease. PLoS ONE 6: e16857.
46. Jiang, N., J. He, J. A. Weinstein, L. Penland, S. Sasaki, X. S. He, C. L. Dekker, N. Y. Zheng, M. Huang, M. Sullivan, P. C. Wilson, H. B. Greenberg, M. M. Davis, D. S. Fisher, and S. R. Quake. 2013. Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med. 5: 171ra119.
47. Scheid, J. F., H. Mouquet, N. Feldhahn, B. D. Walker, F. Pereyra, E. Cutrell, M. S. Seaman, J. R. Mascola, R. T.Wyatt, H.Wardemann, and M. C. Nussenzweig. 2009. A method for identification of HIV gp140 binding memory B cells in human blood. J. Immunol. Methods 343: 65-67.
48. Huang, C. C., M. Venturi, S. Majeed, M. J. Moore, S. Phogat, M. Y. Zhang, D. S. Dimitrov, W. A. Hendrickson, J. Robinson, J. Sodroski, et al. 2004. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc. Natl. Acad. Sci. USA 101: 2706-2711.
49. Li, L., X. H. Wang, S. Banerjee, B. Volsky, C. Williams, D. Virland, A. Nadas, M. S. Seaman, X. Chen, P. Spearman, et al. 2012. Different pattern of immunoglobulin gene usage by HIV-1 compared to non-HIV-1 antibodies derived from the same infected subject. PLoS ONE 7: e39534.
50. Xiao, M., P. Prabakaran, W. Chen, B. Kessing, and D. S. Dimitrov. 2013. Deep sequencing and Circos analyses of antibody libraries reveal antigendriven selection of Ig VH genes during HIV-1 infection. Exp. Mol. Pathol. 95: 357-363.