Selective expansion of HIV-1 envelope glycoprotein-specific B cell subsets recognizing distinct structural elements following immunization

Journal of Immunology

Volumn 183, Issue 5, 2009, Pages 3373-3382

  Dosenovic, Pia ^a,b   Chakrabarti, Bimal ^c   Soldemo, Martina ^a,b   Douagi, Iyadh ^a,b   Forsell, Mattias N E ^a,b,c   Li, Yuxing ^c   Phogat, Adhuna ^c   Paulie, Staffan ^d   Hoxie, James ^e   Wyatt, Richard T ^c   Karlsson Hedestam, Gunilla B ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d Mabtech AB   (Sweden)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; VIRUS GLYCOPROTEIN; EPITOPE; GP140 ENVELOPE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; RECOMBINANT VACCINE; VIRUS ENVELOPE PROTEIN;

ANALYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL EXPANSION; CELL SPECIFICITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROLOGY; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY PRODUCING CELL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BLOOD; BONE MARROW CELL; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE COUNT; METABOLISM; MOLECULAR GENETICS; SECRETION; SPLEEN; VIROLOGY;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIBODY-PRODUCING CELLS; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CELL PROLIFERATION; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES, B-LYMPHOCYTE; HIV ANTIBODIES; IMMUNOLOGIC MEMORY; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; SPLEEN; VACCINES, SYNTHETIC;

EID: 70349249520     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900407     Document Type: Article

References (71)

1. Karlsson Hedestam, G. B., R. A. Fouchier, S. Phogat, D. R. Burton, J. Sodroski, and R. T. Wyatt. 2008. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6: 143-155.
2. Cheng-Mayer, C., J. Homsy, L. A. Evans, and J. A. Levy. 1988. Identification of human immunodeficiency virus subtypes with distinct patterns of sensitivity to serum neutralization. Proc. Natl. Acad. Sci. USA 85: 2815-2819.
3. Profy, A. T., P. A. Salinas, L. I. Eckler, N. M. Dunlop, P. L. Nara, and S. D. Putney. 1990. Epitopes recognized by the neutralizing antibodies of an HIV-1-infected individual. J. Immunol. 144: 4641-4647. (Pubitemid 20224096)
4. Steimer, K. S., C. J. Scandella, P. V. Skiles, and N. L. Haigwood. 1991. Neutralization of divergent HIV-1 isolates by conformation-dependent human antibodies to Gp120. Science 254: 105-108.
5. Kang, C. Y., P. Nara, S. Chamat, V. Caralli, T. Ryskamp, N. Haigwood, R. Newman, and H. Kohler. 1991. Evidence for non-V3-specific neutralizing antibodies that interfere with gp120/CD4 binding in human immunodeficiency virus 1-infected humans. Proc. Natl. Acad. Sci. USA 88: 6171-6175.
6. Moore, J. P., and D. D. Ho. 1993. Antibodies to discontinuous or conformationally sensitive epitopes on the gp120 glycoprotein of human immunodeficiency virus type 1 are highly prevalent in sera of infected humans. J. Virol. 67: 863-875.
7. Sather, D. N., J. Armann, L. K. Ching, A. Mavrantoni, G. Sellhorn, Z. Caldwell, X. Yu, B. Wood, S. Self, S. Kalams, and L. Stamatatos. 2009. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83: 757-769.
8. + T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J. Virol. 79: 13239-13249.
9. Frost, S. D., T. Wrin, D. M. Smith, S. L. Kosakovsky Pond, Y. Liu, E. Paxinos, C. Chappey, J. Galovich, J. Beauchaine, C. J. Petropoulos, et al. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. USA 102: 18514-18519.
10. Karlsson, A. C., A. K. Iversen, J. M. Chapman, T. de Oliviera, G. Spotts, A. J. McMichael, M. P. Davenport, F. M. Hecht, and D. F. Nixon. 2007. Sequential broadening of CTL responses in early HIV-1 infection is associated with viral escape. PLoS ONE 2: e225.
11. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100: 4144-4149.
12. 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.
13. 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.
14. McKeating, J. A., C. Shotton, J. Cordell, S. Graham, P. Balfe, N. Sullivan, M. Charles, M. Page, A. Bolmstedt, S. Olofsson, et al. 1993. Characterization of neutralizing monoclonal antibodies to linear and conformation-dependent epitopes within the first and second variable domains of human immunodeficiency virus type 1 gp120. J. Virol. 67: 4932-4944.
15. Moore, J. P., Q. J. Sattentau, H. Yoshiyama, M. Thali, M. Charles, N. Sullivan, S. W. Poon, M. S. Fung, F. Traincard, M. Pinkus, et al. 1993. Probing the structure of the V2 domain of human immunodeficiency virus type 1 surface glycoprotein gp120 with a panel of eight monoclonal antibodies: human immune response to the V1 and V2 domains. J. Virol. 67: 6136-6151.
16. Nara, P. L., W. G. Robey, L. O. Arthur, D. M. Asher, A. V. Wolff, C. J. Gibbs, Jr., D. C. Gajdusek, and P. J. Fischinger. 1987. Persistent infection of chimpanzees with human immunodeficiency virus: serological responses and properties of reisolated viruses. J. Virol. 61: 3173-3180. (Pubitemid 17131495)
17. Nara, P. L., L. Smit, N. Dunlop, W. Hatch, M. Merges, D. Waters, J. Kelliher, R. C. Gallo, P. J. Fischinger, and J. Goudsmit. 1990. Emergence of viruses resistant to neutralization by V3-specific antibodies in experimental human immunodeficiency virus type 1 IIIB infection of chimpanzees. J. Virol. 64: 3779-3791.
18. Von Gegerfelt, A., J. Albert, L. Morfeldt-Manson, K. Broliden, and E. M. Fenyo. 1991. Isolate-specific neutralizing antibodies in patients with progressive HIV-1-related disease. Virology 185: 162-168.
19. Albert, J., B. Abrahamsson, K. Nagy, E. Aurelius, H. Gaines, G. Nystrom, and E. M. Fenyo. 1990. Rapid development of isolate-specific neutralizing antibodies after primary HIV-1 infection and consequent emergence of virus variants which resist neutralization by autologous sera. AIDS 4: 107-112.
20. Spear, G. T., D. M. Takefman, S. Sharpe, M. Ghassemi, and S. Zolla-Pazner. 1994. Antibodies to the HIV-1 V3 loop in serum from infected persons contribute a major proportion of immune effector functions including complement activation, antibody binding, and neutralization. Virology 204: 609-615.
21. Zwart, G., N. K. Back, C. Ramautarsing, M. Valk, L. van der Hoek, and J. Goudsmit. 1994. Frequent and early HIV-1MN neutralizing capacity in sera from Dutch HIV-1 seroconverters is related to antibody reactivity to peptides from the gp120 V3 domain. AIDS Res. Hum. Retroviruses 10: 245-251. (Pubitemid 24116780)
22. Moore, J. P., and D. D. Ho. 1995. HIV-1 neutralization: the consequences of viral adaptation to growth on transformed T cells. AIDS 9(Suppl. A): S117-S136.
23. Burton, D. R., R. C. Desrosiers, R. W. Doms, W. C. Koff, P. D. Kwong, J. P. Moore, G. J. Nabel, J. Sodroski, I. A. Wilson, and R. T. Wyatt. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5: 233-236.
24. Nara, P. L., and R. Garrity. 1998. Deceptive imprinting: a cosmopolitan strategy for complicating vaccination. Vaccine 16: 1780-1787.
25. 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.
26. Albrecht, H. 2003. Making sense of AIDSVAX. AIDS Clin. Care 15: 42.
27. Binley, J. M., R. W. Sanders, B. Clas, N. Schuelke, A. Master, Y. Guo, F. Kajumo, D. J. Anselma, P. J. Maddon, W. C. Olson, and J. P. Moore. 2000. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J. Virol. 74: 627-643.
28. Kim, M., Z. S. Qiao, D. C. Montefiori, B. F. Haynes, E. L. Reinherz, and H. X. Liao. 2005. Comparison of HIV type 1 ADA gp120 monomers versus gp140 trimers as immunogens for the induction of neutralizing antibodies. AIDS Res. Hum. Retroviruses 21: 58-67.
29. Sanders, R. W., M. Vesanen, N. Schuelke, A. Master, L. Schiffner, R. Kalyanaraman, M. Paluch, B. Berkhout, P. J. Maddon, W. C. Olson, et al. 2002. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 76: 8875-8889.
30. Srivastava, I. K., L. Stamatatos, E. Kan, M. Vajdy, Y. Lian, S. Hilt, L. Martin, C. Vita, P. Zhu, K. H. Roux, et al. 2003. Purification, characterization, and immunogenicity of a soluble trimeric envelope protein containing a partial deletion of the V2 loop derived from SF162, an R5-tropic human immunodeficiency virus type 1 isolate. J. Virol. 77: 11244-11259.
31. Yang, X., M. Farzan, R. Wyatt, and J. Sodroski. 2000. Characterization of stable, soluble trimers containing complete ectodomains of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 74: 5716-5725.
32. 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.
33. Forsell, M. N., Y. Li, M. Sundback, K. Svehla, P. Liljestrom, J. R. Mascola, R. Wyatt, and G. B. 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.
34. Li, Y., K. Svehla, N. L. Mathy, G. Voss, J. R. Mascola, and R. Wyatt. 2006. Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants. J. Virol. 80: 1414-1426.
35. Yang, X., R. Wyatt, and J. Sodroski. 2001. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J. Virol. 75: 1165-1171.
36. Bower, J. F., X. Yang, J. Sodroski, and T. M. Ross. 2004. Elicitation of neutralizing antibodies with DNA vaccines expressing soluble stabilized human immunodeficiency virus type 1 envelope glycoprotein trimers conjugated to C3d. J. Virol. 78: 4710-4719.
37. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79: 10108-10125.
38. Mascola, J. R., P. D'Souza, P. Gilbert, B. H. Hahn, N. L. Haigwood, L. Morris, C. J. Petropoulos, V. R. Polonis, M. Sarzotti, and D. C. Montefiori. 2005. Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J. Virol. 79: 10103-10107.
39. Doria-Rose, N. A., R. M. Klein, M. M. Manion, S. O'Dell, A. Phogat, B. Chakrabarti, C. W. Hallahan, S. A. Migueles, J. Wrammert, R. Ahmed, et al. 2009. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J. Virol. 83: 188-199.
40. Scheid, J., H. Mouquet, N. Feldhahn, B. Walker, F. Pereyra, E. Cutrell, M. Seaman, J. Mascola, R. Wyatt, H. Wardemann, and M. C. Nussenzweig. 2008. A method for identification of HIV gp140 binding memory B cells in human blood. J. Immunol. Methods 343: 65-67.
41. Pancera, M., J. Lebowitz, A. Schon, P. Zhu, E. Freire, P. D. Kwong, K. H. Roux, J. Sodroski, and R. Wyatt. 2005. Soluble mimetics of human immunodeficiency virus type 1 viral spikes produced by replacement of the native trimerization domain with a heterologous trimerization motif: characterization and ligand binding analysis. J. Virol. 79: 9954-9969.
42. Dey, B., K. Svehla, L. Xu, D. Wycuff, T. Zhou, G. Voss, A. Phogat, B. Chakrabarti, Y. Li, G. M. Shaw, et al. 2009. Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog. 5: e1000445.
43. Forsell, M. N., B. Dey, A. Morner, K. Svehla, S. O'Dell, C. M. Hogerkorp, 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.
44. Schulke, N., M. S. Vesanen, R. W. Sanders, P. Zhu, M. Lu, D. J. Anselma, A. R. Villa, P. W. Parren, J. M. Binley, K. H. Roux, et al. 2002. Oligomeric and conformational properties of a proteolytically mature, disulfide-stabilized human immunodeficiency virus type 1 gp140 envelope glycoprotein. J. Virol. 76: 7760-7776.
45. Dey, B., M. Pancera, K. Svehla, Y. Shu, S. H. Xiang, J. Vainshtein, Y. Li, J. Sodroski, P. D. Kwong, J. R. Mascola, and R. Wyatt. 2007. Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J. Virol. 81: 5579-5593.
46. Edinger, A. L., M. Ahuja, T. Sung, K. C. Baxter, B. Haggarty, R. W. Doms, and J. A. Hoxie. 2000. Characterization and epitope mapping of neutralizing monoclonal antibodies produced by immunization with oligomeric simian immunodeficiency virus envelope protein. J. Virol. 74: 7922-7935.
47. Crotty, S., R. D. Aubert, J. Glidewell, and R. Ahmed. 2004. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods 286: 111-122.
48. Czerkinsky, C. C., L. A. Nilsson, H. Nygren, O. Ouchterlony, and A. Tarkowski. 1983. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J. Immunol. Methods 65: 109-121. (Pubitemid 14203438)
49. Sedgwick, J. D., and P. G. Holt. 1983. A solid-phase immunoenzymatic technique for the enumeration of specific antibody-secreting cells. J. Immunol. Methods 57: 301-309. (Pubitemid 13116746)
50. Slifka, M. K., and R. Ahmed. 1996. Limiting dilution analysis of virus-specific memory B cells by an ELISPOT assay. J. Immunol. Methods 199: 37-46.
51. Wrammert, J., K. Smith, J. Miller, W. A. Langley, K. Kokko, C. Larsen, N. Y. Zheng, I. Mays, L. Garman, C. Helms, et al. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453: 667-671.
52. Morner, A., I. Douagi, M. N. Forsell, C. Sundling, P. Dosenovic, S. O'Dell, B. Dey, P. D. Kwong, G. Voss, R. Thorstensson, et al. 2009. Human immunodeficiency virus type 1 env trimer immunization of macaques and impact of priming with viral vector or stabilized core protein. J. Virol. 83: 540-551.
53. 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.
54. Wyatt, R., M. Thali, S. Tilley, A. Pinter, M. Posner, D. Ho, J. Robinson, and J. Sodroski. 1992. Relationship of the human immunodeficiency virus type 1 gp120 third variable loop to a component of the CD4 binding site in the fourth conserved region. J. Virol. 66: 6997-7004.
55. 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.
56. 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.
57. Binley, J. M., H. J. Ditzel, C. F. Barbas III, N. Sullivan, J. Sodroski, P. W. Parren, and D. R. Burton. 1996. Human antibody responses to HIV type 1 glycoprotein 41 cloned in phage display libraries suggest three major epitopes are recognized and give evidence for conserved antibody motifs in antigen binding. AIDS Res. Hum. Retroviruses 12: 911-924.
58. Tomaras, G. D., N. L. Yates, P. Liu, L. Qin, G. G. Fouda, L. L. Chavez, A. C. Decamp, R. J. Parks, V. C. Ashley, J. T. Lucas, et al. 2008. Initial B cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82: 12449-12463.
59. Binley, J. M., E. A. Lybarger, E. T. Crooks, M. S. Seaman, E. Gray, K. L. Davis, J. M. Decker, D. Wycuff, L. Harris, N. Hawkins, et al. 2008. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82: 11651-11668.
60. Dhillon, A. K., H. Donners, R. Pantophlet, W. E. Johnson, J. M. Decker, G. M. Shaw, F. H. Lee, D. D. Richman, R. W. Doms, G. Vanham, and D. R. Burton. 2007. Dissecting the neutralizing antibody specificities of broadly neutralizing sera from human immunodeficiency virus type 1-infected donors. J. Virol. 81: 6548-6562.
61. Li, Y., K. Svehla, M. K. Louder, D. Wycuff, S. Phogat, M. Tang, S. A. Migueles, X. Wu, A. Phogat, G. M. Shaw, et al. 2009. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J. Virol. 83: 1045-1059.
62. Moore, P. L., E. S. Gray, I. A. Choge, N. Ranchobe, K. Mlisana, S. S. Abdool Karim, C. Williamson, and L. Morris. 2008. The c3-v4 region is a major target of autologous neutralizing antibodies in human immunodeficiency virus type 1 subtype C infection. J. Virol. 82: 1860-1869.
63. Gorny, M. K., X. H. Wang, C. Williams, B. Volsky, K. Revesz, B. Witover, S. Burda, M. Urbanski, P. Nyambi, C. Krachmarov, et al. 2009. 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. 46: 917-926.
64. 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.
65. Ahuja, A., S. M. Anderson, A. Khalil, and M. J. Shlomchik. 2008. Maintenance of the plasma cell pool is independent of memory B cells. Proc. Natl. Acad. Sci. USA 105: 4802-4807.
66. Amanna, I. J., N. E. Carlson, and M. K. Slifka. 2007. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 357: 1903-1915.
67. DiLillo, D. J., Y. Hamaguchi, Y. Ueda, K. Yang, J. Uchida, K. M. Haas, G. Kelsoe, and T. F. Tedder. 2008. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180: 361-371.
68. Gatto, D., S. W. Martin, J. Bessa, E. Pellicioli, P. Saudan, H. J. Hinton, and M. F. Bachmann. 2007. Regulation of memory antibody levels: the role of persisting antigen versus plasma cell life span. J. Immunol. 178: 67-76.
69. Ochsenbein, A. F., D. D. Pinschewer, S. Sierro, E. Horvath, H. Hengartner, and R. M. Zinkernagel. 2000. Protective long-term antibody memory by antigen-driven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 97: 13263-13268.
70. Schittek, B., and K. Rajewsky. 1990. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 346: 749-751. (Pubitemid 120005987)
71. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372.