Increased survival is a selective feature of human circulating antigen-induced plasma cells synthesizing high-affinity antibodies

Blood

Volumn 111, Issue 2, 2008, Pages 741-749

  González García, Inés ^a   Rodríguez Bayona, Beatriz ^a   Mora López, Francisco ^a   Campos Caro, Antonio ^a   Brieva, José A ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FLUORESCEIN ISOTHIOCYANATE; IMMUNOGLOBULIN G ANTIBODY; MESSENGER RNA; PROTEIN; PROTEIN BLIMP 4; STROMAL CELL DERIVED FACTOR 1; TETANUS TOXOID; UNCLASSIFIED DRUG;

ADULT; ANTIBODY PRODUCTION; ANTIGEN BINDING; APOPTOSIS; ARTICLE; BONE MARROW; CELL FATE; CELL HOMING; CELL SURVIVAL; CELL TYPE; CHEMOTAXIS; CONTROLLED STUDY; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NORMAL HUMAN; PLASMA CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

EID: 38349140107     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-08-108118     Document Type: Article

References (52)

1. Jacob J, Kassir R, Kelsoe G. 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. 1991;173:1165-1175.
2. Liu YJ, Zhang J, Lane PJ, Chan EY, MacLennan IC. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur J Immunol. 1991;21:2951-2962.
3. van Rooijen N. Direct intrafollicular differentiation of memory B cells into plasma cells. Immunol Today. 1990;11:154-157.
4. Dilosa RM, Maeda K, Masuda A, Szakal AK, Tew JG. Germinal center B cells and antibody production in the bone marrow. J Immunol. 1991;146:4071-4077.
5. Ho F, Lortan JE, MacLennan IC, Khan M. Distinct short-lived and long-lived antibody-producing cell populations. Eur J Immunol. 1986;16:1297-1301.
6. Smith KG, Hewitson TD, Nossal GJ, Tarlinton DM. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur J Immunol. 1996;26:444-448.
7. Pelletier N, Casamayor-Palleja M, De Luca K, et al. The endoplasmic reticulum is a key component of the plasma cell death pathway. J Immunol. 2006;176:1340-1347.
8. Koch G, Osmond DG, Julius MH, Benner R. The mechanism of thymus-dependent antibody formation in bone marrow. J Immunol. 1981;126:1447-1451.
9. McMillan R, Longmire RL, Yelenosky R, Lang JE, Heath V, Craddock CG. Immunoglobulin synthesis by human lymphoid tissues: normal bone marrow as a major site of IgG production. J Immunol. 1972;109:1386-1394.
10. Slifka MK, Antia R, Whitmire JK, Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity. 1998;8:363-372.
11. Manz RA, Thiel A, Radbruch A. Lifetime of plasma cells in the bone marrow. Nature. 1997;388:133-134.
12. Takahashi Y, Dutta PR, Cerasoli DM, Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl, V: affinity maturation develops in two stages of clonal selection. J Exp Med. 1998;187:885-895.
13. Roldan E, Garcia-Pardo A, Brieva JA. VLA-4-fibronectin interaction is required for the terminal differentiation of human bone marrow cells capable of spontaneous and high rate immunoglobulin secretion. J Exp Med. 1992;175:1739-1747.
14. Minges Wols HA, Underhill GH, Kansas GS, Witte PL. The role of bone marrow-derived stromal cells in the maintenance of plasma cell longevity. J Immunol. 2002;169:4213-4221.
15. Cassese G, Arce S, Hauser AE, et al. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J Immunol. 2003;171:1684-1690.
16. Sze DM, Toellner KM, Garcia de Vinuesa C, Taylor DR, MacLennan IC. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J Exp Med. 2000;192:813-821.
17. Ellyard JI, Avery DT, Phan TG, Hare NJ, Hodgkin PD, Tangye SG. Antigen-selected, immunoglobulin-secreting cells persist in human spleen and bone marrow. Blood. 2004;103:3805-3812.
18. Withers DR, Fiorini C, Fischer RT, Ettinger R, Lipsky PE, Grammer AC. T cell-dependent survival of CD20+ and CD20- plasma cells in human secondary lymphoid tissue. Blood. 2007;109:4856-4864.
19. Mallison SM 3rd, Smith JP, Schenkein HA, Tew JG. Accumulation of plasma cells in inflamed sites: effects of antigen, nonspecific microbial activators, and chronic inflammation. Infect Immun. 1991;59:4019-4025.
20. Benner R, Hijmans W, Haaijman JJ. The bone marrow: the major source of serum immunoglobulins, but still a neglected site of antibody formation. Clin Exp Immunol. 1981;46:1-8.
21. Hargreaves DC, Hyman PL, Lu TT, et al. A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med. 2001;194:45-56.
22. Muehlinghaus G, Cigliano L, Huehn S, et al. Regulation of CXCR3 and CXCR4 expression during terminal differentiation of memory B cells into plasma cells. Blood. 2005;105:3965-3971.
23. Medina F, Segundo C, Campos-Caro A, Gonzalez-Garcia I, Brieva JA. The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood. 2002;99:2154-2161.
24. Odendahl M, Mei H, Hoyer BF, et al. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood. 2005;105:1614-1621.
25. Moser K, Tokoyoda K, Radbruch A, MacLennan I, Manz RA. Stromal niches, plasma cell differentiation and survival. Curr Opin Immunol. 2006;18:265-270.
26. Ingold K, Zumsteg A, Tardivel A, et al. Identification of proteoglycans as the APRIL-specific binding partners. J Exp Med. 2005;201:1375-1383.
27. Kallies A, Hasbold J, Tarlinton DM, et al. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J Exp Med. 2004;200:967-977.
28. Blink EJ, Light A, Kallies A, Nutt SL, Hodgkin PD, Tarlinton DM. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J Exp Med. 2005;201:545-554.
29. Stevens RH, Macy E, Morrow C, Saxon A. Characterization of a circulating subpopulation of spontaneous antitetanus toxoid antibody producing B cells following in vivo booster immunization. J Immunol. 1979;122:2498-2504.
30. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002;298:2199-2202.
31. Gonzalez-Garcia I, Ocana E, Jimenez-Gomez G, Campos-Caro A, Brieva JA. Immunization-induced perturbation of human blood plasma cell pool: progressive maturation, IL-6 responsiveness, and high PRDI-BF1/BLIMP1 expression are critical distinctions between antigen-specific and nonspecific plasma cells. J Immunol. 2006;176:4042-4050.
32. Kodo H, Gale RP, Saxon A. Antibody synthesis by bone marrow cells in vitro following primary and booster tetanus toxoid immunization in humans. J Clin Invest. 1984;73:1377-1384.
33. Saxon A, Mitsuyasu R, Stevens R, Champlin RE, Kimata H, Gale RP. Designed transfer of specific immune responses with bone marrow transplantation. J Clin Invest. 1986;78:959-967.
34. Smith KG, Light A, Nossal GJ, Tarlinton DM. The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 1997;16:2996-3006.
35. Makoff AJ, Oxer MD, Romanos MA, Fairweather NF, Ballantine S. Expression of tetanus toxin fragment C in E. coli: high level expression by removing rare codons. Nucleic Acids Res. 1989;17:10191-10202.
36. Leyendeckers H, Odendahl M, Lohndorf A, et al. Correlation analysis between frequencies of circulating antigen-specific IgG-bearing memory B cells and serum titers of antigen-specific IgG. Eur J Immunol. 1999;29:1406-1417.
37. Chatelier RC, Ashcroft RG, Lloyd CJ, et al. Binding of fluoresceinated epidermal growth factor to A431 cell sub-populations studied using a modelin-dependent analysis of flow cytometric fluorescence data. EMBO J. 1986;5:1181-1186.
38. Rundquist I. Equilibrium binding of DAPI and 7-aminoactinomycin D to chromatin of cultured cells. Cytometry. 1993;14:610-617.
39. Gordon IL. Scatchard analysis of fluorescent concanavalin A binding to lymphocytes. Cytometry. 1995;20:238-244.
40. Brieva JA, Stevens RH. Human in vivo antigen-induced lymphoblastoid B cells are capable of cyclical antibody production in vitro. J Immunol. 1984;133:147-153.
41. Lefranc, Marie-Paule. The International Immunogenetics Information System IgVH database. Available at: http://imgt.cines.fr/. Accessed January 2007. .
42. National Institutes of Health. GenBank. http://www.ncbi.nlm.nih.gov/ genbank/. Accessed September 7, 2007.
43. Jaimes MC, Rojas OL, Kunkel EJ, et al. Maturation and trafficking markers on rotavirus-specific B cells during acute infection and convalescence in children. J Virol. 2004;78:10967-10976.
44. Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity. 2003;19:607-620.
45. Turner CA Jr, Mack DH, Davis MM. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin- secreting cells. Cell. 1994;77:297-306.
46. Chang B, Casali P. The CDR1 sequences of a major proportion of human germline Ig VH genes are inherently susceptible to amino acid replacement. Immunol Today. 1994;15:367-373.
47. Pellat-Deceunynck C, Bataille R. Normal and malignant human plasma cells: proliferation, differentiation, and expansions in relation to CD45 expression. Blood Cells Mol Dis. 2004;32:293-301.
48. Piskurich JF, Lin KI, Lin Y, Wang Y, Ting JP, Calame K. BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat Immunol. 2000;1:526-532.
49. Morrow CD, Macy EM, Stevens RH. Analysis of human anti-diphtheria antibodies by isoelectric focusing: evidence for restricted clonal heterogeneity of anti-fragment A antibodies. Infect Immun. 1981;31:1132-1137.
50. Dal Porto JM, Haberman AM, Shlomchik MJ, Kelsoe G. Antigen drives very low affinity B cells to become plasmacytes and enter germinal centers. J Immunol. 1998;161:5373-5381.
51. Paus D, Phan TG, Chan TD, 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. 2006;203:1081-1091.
52. Merville P, Dechanet J, Desmouliere A, et al. Bcl-2+ tonsillar plasma cells are rescued from apoptosis by bone marrow fibroblasts. J Exp Med. 1996;183:227-236.