Independent expansion of epitope-specific plasma cell responses upon HIV-1 envelope glycoprotein immunization

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 44-51

  Forsell, Mattias N E ^a   Soldemo, Martina ^a   Dosenovic, Pia ^a   Wyatt, Richard T ^b   Karlsson, Mikael C I ^a   Karlsson Hedestam, Gunilla B ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; IMMUNOGLOBULIN G; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE ACTIVATION; BINDING COMPETITION; CELL EXPANSION; CELL SPECIFICITY; CONTROLLED STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; IMMUNOGLOBULIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; WILD TYPE;

AIDS VACCINES; ANIMALS; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES, B-LYMPHOCYTE; FEMALE; HIV ENVELOPE PROTEIN GP120; HUMANS; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; PLASMA CELLS; PROTEIN SUBUNITS;

EID: 84879677332     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203087     Document Type: Article

References (57)

1. Jacob, J., R. Kassir, and G. Kelsoe. 1991. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173: 1165-1175.
2. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centres. Nature 354: 389-392. (Pubitemid 21896846)
3. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129. (Pubitemid 121001525)
4. Victora, G. D., and M. C. Nussenzweig. 2012. Germinal centers. Annu. Rev. Immunol. 30: 429-457.
5. Benjamin, D. C., J. A. Berzofsky, I. J. East, F. R. Gurd, C. Hannum, S. J. Leach, E. Margoliash, J. G. Michael, A. Miller, E. M. Prager, et al. 1984. The antigenic structure of proteins: a reappraisal. Annu. Rev. Immunol. 2: 67-101.
6. Dal Porto, J. M., A. M. Haberman, M. J. Shlomchik, and G. Kelsoe. 1998. Antigen drives very low affinity B cells to become plasmacytes and enter germinal centers. J. Immunol. 161: 5373-5381. (Pubitemid 28519098)
7. Paus, D., T. G. Phan, T. D. Chan, S. Gardam, A. Basten, and R. Brink. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203: 1081-1091.
8. Schwickert, T. A., R. L. Lindquist, G. Shakhar, G. Livshits, D. Skokos, M. H. Kosco-Vilbois, M. L. Dustin, and M. C. Nussenzweig. 2007. In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446: 83-87. (Pubitemid 46348044)
9. Shih, T. A., E. Meffre, M. Roederer, and M. C. Nussenzweig. 2002. Role of BCR affinity in T cell dependent antibody responses in vivo. Nat. Immunol. 3: 570-575. (Pubitemid 34662310)
10. 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. (Pubitemid 34309599)
11. Mascola, J. R., and D. C. Montefiori. 2010. The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28: 413-444.
12. Walker, L. M., and D. R. Burton. 2010. Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr. Opin. Immunol. 22: 358-366.
13. Phogat, S., and R. Wyatt. 2007. Rational modifications of HIV-1 envelope glycoproteins for immunogen design. Curr. Pharm. Des. 13: 213-227. (Pubitemid 46085294)
14. Garrity, R. R., G. Rimmelzwaan, A. Minassian, W. P. Tsai, G. Lin, J. J. de Jong, J. Goudsmit, and P. L. Nara. 1997. Refocusing neutralizing antibody response by targeted dampening of an immunodominant epitope. J. Immunol. 159: 279-289. (Pubitemid 127493710)
15. Douek, D. C., P. D. Kwong, and G. J. Nabel. 2006. The rational design of an AIDS vaccine. Cell 124: 677-681. (Pubitemid 43261441)
16. Tobin, G. J., J. D. Trujillo, R. V. Bushnell, G. Lin, A. R. Chaudhuri, J. Long, J. Barrera, L. Pena, M. J. Grubman, and P. L. Nara. 2008. Deceptive imprinting and immune refocusing in vaccine design. Vaccine 26: 6189-6199.
17. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280: 1884-1888. (Pubitemid 28299385)
18. Moore, J. P., and J. Sodroski. 1996. Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein. J. Virol. 70: 1863-1872. (Pubitemid 26062950)
19. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659. (Pubitemid 28289647)
20. Huang, C. C., S. N. Lam, P. Acharya, M. Tang, S. H. Xiang, S. S. Hussan, R. L. Stanfield, J. Robinson, J. Sodroski, I. A. Wilson, et al. 2007. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317: 1930-1934. (Pubitemid 47509439)
21. Zhou, T., L. Xu, B. Dey, A. J. Hessell, D. Van Ryk, S. H. Xiang, X. Yang, M. Y. Zhang, M. B. Zwick, J. Arthos, et al. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737. (Pubitemid 46279718)
22. Calarese, D. A., C. N. Scanlan, M. B. Zwick, S. Deechongkit, Y. Mimura, R. Kunert, P. Zhu, M. R. Wormald, R. L. Stanfield, K. H. Roux, et al. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300: 2065-2071. (Pubitemid 36760127)
23. Wyatt, R., P. D. Kwong, E. Desjardins, R. W. Sweet, J. Robinson, W. A. Hendrickson, and J. G. Sodroski. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393: 705-711. (Pubitemid 28289663)
24. Kwong, P. D., and J. R. Mascola. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37: 412-425.
25. Burton, D. R., P. Poignard, R. L. Stanfield, and I. A. Wilson. 2012. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337: 183-186.
26. Harris, A., M. J. Borgnia, D. Shi, A. Bartesaghi, H. He, R. Pejchal, Y. K. Kang, R. Depetris, A. J. Marozsan, R. W. Sanders, et al. 2011. Trimeric HIV-1 glycoprotein gp140 immunogens and native HIV-1 envelope glycoproteins display the same closed and open quaternary molecular architectures. Proc. Natl. Acad. Sci. USA 108: 11440-11445.
27. Liu, J., A. Bartesaghi, M. J. Borgnia, G. Sapiro, and S. Subramaniam. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
28. Mao, Y., L. Wang, C. Gu, A. Herschhorn, S. H. Xiang, H. Haim, X. Yang, and J. Sodroski. 2012. Subunit organization of the membrane-bound HIV-1 envelope glycoprotein trimer. Nat. Struct. Mol. Biol. 19: 893-899.
29. White, T. A., A. Bartesaghi, M. J. Borgnia, J. R. Meyerson, M. J. de la Cruz, J. W. Bess, R. Nandwani, J. A. Hoxie, J. D. Lifson, J. L. Milne, and S. Subramaniam. 2010. Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog. 6: e1001249.
30. Douagi, I., M. N. Forsell, C. Sundling, S. O'Dell, Y. Feng, P. Dosenovic, Y. Li, R. Seder, K. Loré, J. R. Mascola, et al. 2010. Influence of novel CD4 bindingdefective HIV-1 envelope glycoprotein immunogens on neutralizing antibody and T-cell responses in nonhuman primates. J. Virol. 84: 1683-1695.
31. Forsell, M. N., B. Dey, A. Mörner, K. Svehla, S. O'dell, C. M. Högerkorp, G. Voss, R. Thorstensson, G. M. Shaw, J. R. Mascola, et al. 2008. B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathog. 4: e1000171.
32. Dosenovic, P., B. Chakrabarti, M. Soldemo, I. Douagi, M. N. Forsell, Y. Li, A. Phogat, S. Paulie, J. Hoxie, R. T. Wyatt, and G. B. Karlsson Hedestam. 2009. Selective expansion of HIV-1 envelope glycoprotein-specific B cell subsets recognizing distinct structural elements following immunization. J. Immunol. 183: 3373-3382.
33. Starcich, B. R., B. H. Hahn, G. M. Shaw, P. D. McNeely, S. Modrow, H. Wolf, E. S. Parks, W. P. Parks, S. F. Josephs, R. C. Gallo, et al. 1986. Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 45: 637-648. (Pubitemid 16063128)
34. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422: 307-312. (Pubitemid 36378357)
35. Forsell, M. N., Y. Li, M. Sundbäck, K. Svehla, P. Liljeström, J. R. Mascola, R. Wyatt, and G. B. Karlsson Hedestam. 2005. Biochemical and immunogenic characterization of soluble human immunodeficiency virus type 1 envelope glycoprotein trimers expressed by semliki forest virus. J. Virol. 79: 10902-10914. (Pubitemid 41170632)
36. Selvarajah, S., B. Puffer, R. Pantophlet, M. Law, R. W. Doms, and D. R. Burton. 2005. Comparing antigenicity and immunogenicity of engineered gp120. J. Virol. 79: 12148-12163. (Pubitemid 41346077)
37. Selvarajah, S., B. A. Puffer, F. H. Lee, P. Zhu, Y. Li, R. Wyatt, K. H. Roux, R. W. Doms, and D. R. Burton. 2008. Focused dampening of antibody response to the immunodominant variable loops by engineered soluble gp140. AIDS Res. Hum. Retroviruses 24: 301-314. (Pubitemid 351282104)
38. Javaherian, K., A. J. Langlois, C. McDanal, K. L. Ross, L. I. Eckler, C. L. Jellis, A. T. Profy, J. R. Rusche, D. P. Bolognesi, S. D. Putney, et al. 1989. Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc. Natl. Acad. Sci. USA 86: 6768-6772. (Pubitemid 19236342)
39. Huang, C. C., M. Tang, M. Y. Zhang, S. Majeed, E. Montabana, R. L. Stanfield, D. S. Dimitrov, B. Korber, J. Sodroski, I. A. Wilson, et al. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028. (Pubitemid 41611916)
40. Wu, L., N. P. Gerard, R. Wyatt, H. Choe, C. Parolin, N. Ruffing, A. Borsetti, A. A. Cardoso, E. Desjardin, W. Newman, et al. 1996. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 384: 179-183. (Pubitemid 26386475)
41. Trkola, A., T. Dragic, J. Arthos, J. M. Binley, W. C. Olson, G. P. Allaway, C. Cheng-Mayer, J. Robinson, P. J. Maddon, and J. P. Moore. 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384: 184-187. (Pubitemid 26386476)
42. Walker, L. M., M. Huber, K. J. Doores, E. Falkowska, R. Pejchal, J. P. Julien, S. K. Wang, A. Ramos, P. Y. Chan-Hui, M. Moyle, et al; Protocol G Principal Investigators. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
43. Grundner, C., M. Pancera, J. M. Kang, M. Koch, J. Sodroski, and R. Wyatt. 2004. Factors limiting the immunogenicity of HIV-1 gp120 envelope glycoproteins. Virology 330: 233-248. (Pubitemid 39451803)
44. Nielsen, M., and O. Lund. 2009. NN-align. An artificial neural network-based alignment algorithm for MHC class II peptide binding prediction. BMC Bioinformatics 10: 296.
45. Nielsen, M., C. Lundegaard, and O. Lund. 2007. Prediction of MHC class II binding affinity using SMM-align, a novel stabilization matrix alignment method. BMC Bioinformatics 8: 238.
46. Moon, J. J., H. H. Chu, M. Pepper, S. J. McSorley, S. C. Jameson, R. M. Kedl, and M. K. Jenkins. 2007. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213. (Pubitemid 47284919)
47. Sze, D. M., K. M. Toellner, C. García de Vinuesa, D. R. Taylor, and I. C. MacLennan. 2000. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J. Exp. Med. 192: 813-821.
48. Schwickert, T. A., G. D. Victora, D. R. Fooksman, A. O. Kamphorst, M. R. Mugnier, A. D. Gitlin, M. L. Dustin, and M. C. Nussenzweig. 2011. A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J. Exp. Med. 208: 1243-1252.
49. Schittek, B., and K. Rajewsky. 1990. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 346: 749-751.
50. Takahashi, Y., H. Ohta, and T. Takemori. 2001. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14: 181-192. (Pubitemid 32206520)
51. Gray, D., P. Dullforce, and S. Jainandunsing. 1994. Memory B cell development but not germinal center formation is impaired by in vivo blockade of CD40-CD40 ligand interaction. J. Exp. Med. 180: 141-155. (Pubitemid 24181063)
52. Collen, D., H. Moreau, L. Stockx, and S. Vanderschueren. 1996. Recombinant staphylokinase variants with altered immunoreactivity. II: Thrombolytic properties and antibody induction. Circulation 94: 207-216. (Pubitemid 26240558)
53. Onda, M., R. Beers, L. Xiang, S. Nagata, Q. C. Wang, and I. Pastan. 2008. An immunotoxin with greatly reduced immunogenicity by identification and removal of B cell epitopes. Proc. Natl. Acad. Sci. USA 105: 11311-11316.
54. Laroche, Y., S. Heymans, S. Capaert, F. De Cock, E. Demarsin, and D. Collen. 2000. Recombinant staphylokinase variants with reduced antigenicity due to elimination of B-lymphocyte epitopes. Blood 96: 1425-1432. (Pubitemid 30658473)
55. Onda, M., R. Beers, L. Xiang, B. Lee, J. E. Weldon, R. J. Kreitman, and I. Pastan. 2011. Recombinant immunotoxin against B-cell malignancies with no immunogenicity in mice by removal of B-cell epitopes. Proc. Natl. Acad. Sci. USA 108: 5742-5747.
56. Nagata, S., and I. Pastan. 2009. Removal of B cell epitopes as a practical approach for reducing the immunogenicity of foreign protein-based therapeutics. Adv. Drug Deliv. Rev. 61: 977-985.
57. Verkoczy, L., G. Kelsoe, M. A. Moody, and B. F. Haynes. 2011. Role of immune mechanisms in induction of HIV-1 broadly neutralizing antibodies. Curr. Opin. Immunol. 23: 383-390. Biomedical Research