A division-linked mechanism for the rapid generation of Ig-secreting cells from human memory B cells

Journal of Immunology

Volumn 170, Issue 1, 2003, Pages 261-269

  Tangye, Stuart G ^a   Avery, Danielle T ^a   Hodgkin, Philip D ^a,b,c  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD38 ANTIGEN; CD40 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2; LIGAND; LYMPHOCYTE SURFACE MARKER;

ANTIBODY RESPONSE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL DIVISION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOGLOBULIN PRODUCING CELL; IMMUNOGLOBULIN PRODUCTION; IMMUNOSTIMULATION; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MEMORY CELL; PLASMA CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; STAINING; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

EID: 0037220807     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.1.261     Document Type: Article

References (63)

1. McHeyzer-Williams, M. G., and R. Ahmed. 1999. B cell memory and the longlived plasma cell. Curr. Opin. Immunol. 11:172.
2. Slifka, M. K., and R. Ahmed. 1998. Long-lived plasma cells: A mechanism for maintaining persistent antibody production. Curr. Opin. Immunol. 10:252.
3. Liu, Y. J., and J. Banchereau. 1996. The paths and molecular controls of peripheral B-cell development. Immunologist 4:55.
4. Liu, Y. J., and C. Arpin. 1997. Germinal center development. Immunol. Rev. 156:111.
5. Banchereau, J., and F. Rousset. 1992. Human B lymphocytes: Phenotype, proliferation, and differentiation. Adv. Immunol. 52:125.
6. MacLennan, I. C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117.
7. Liu, Y. J., S. Oldfield, and I. C. MacLennan. 1988. Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18:355.
8. Liu, Y. J., J. Zhang, P. J. Lane, E. Y. Chan, and I. C. MacLennan. 1991. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21:2951.
9. Nossal, G. J. V., and O. Makela. 1962. Autoradiographic studies on the immune response. I. The kinetics of plasma cell proliferation. J. Exp. Med. 115:209.
10. Sze, D. M., K. M. Toellner, C. Garcia 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.
11. Calame, K. L. 2001. Plasma cells: Finding new light at the end of B cell development. Nat. Immunol. 2:1103.
12. - memory B cell compartment. J. Exp. Med. 191:1149.
13. Berek, C., J. M. Jarvis, and C. Milstein. 1987. Activation of memory and virgin B cell clones in hyperimmune animals. Eur. J. Immunol. 17:1121.
14. Manz, R. A., M. Lohning, G. Cassese, A. Thiel, and A. Radbruch. 1998. Survival of long-lived plasma cells is independent of antigen. Int. Immunol. 10:1703.
15. Schittek, B., and K. Rajewsky. 1990. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 346:749.
16. Fearon, D. T., P. Manders, and S. D. Wagner. 2001. Arrested differentiation, the self-renewing memory lymphocyte, and vaccination. Science 293:248.
17. Arpin, C., J. Dechanet, C. Van Kooten, P. Merville, G. Grouard, F. Briere, J. Banchereau, and Y. J. Liu. 1995. Generation of memory B cells and plasma cells in vitro. Science 268:720.
18. Arpin, C., J. Banchereau, and Y. J. Liu. 1997. Memory B cells are biased towards terminal differentiation: A strategy that may prevent repertoire freezing. J. Exp. Med. 186:931.
19. Choe, J., and Y. S. Choi. 1998. IL-10 interrupts memory B cell expansion in the germinal center by inducing differentiation into plasma cells. Eur. J. Immunol 28:508.
20. Terstappen, L. W., S. Johnsen, I. M. Segers-Nolten, and M. R. Loken. 1990. Identification and characterization of plasma cells in normal human bone marrow by high-resolution flow cytometry. Blood 76:1739.
21. + is the common phenotype of myeloma cells. Ann. Hematol. 64:132.
22. Liu, Y. J., and J. Banchereau. 1997. Regulation of B-cell commitment to plasma cells or to memory B cells. Semin. Immunol. 9:235.
23. Hodgkin, P. D., J. H. Lee, and A. B. Lyons. 1996. B cell differentiation and isotype switching is related to division cycle number. J. Exp. Med. 184:277.
24. Hasbold, J., A. B. Lyons, M. R. Kehry, and P. D. Hodgkin. 1998. Cell division number regulates IgG1 and IgE switching of B cells following stimulation by CD40 ligand and IL-4. Eur. J. Immunol. 28:1040.
25. Gett, A. V., and P. D. Hodgkin. 1998. Cell division regulates the T cell cytokine repertoire, revealing a mechanism underlying immune class regulation. Proc. Natl. Acad. Sci. USA 95:9488.
26. Hasbold, J., J. S. Hong, M. R. Kehry, and P. D. Hodgkin. 1999. Integrating signals from IFN-γ and IL-4 by B cells: positive and negative effects on CD40 ligand-induced proliferation, survival, and division-linked isotype switching to IgG1, IgE, and IgG2a. J. Immunol. 163:4175.
27. Deenick, E. K., J. Hasbold, and P. D. Hodgkin. 1999. Switching to IgG3, IgG2b, and IgA is division linked and independent, revealing a stochastic framework for describing differentiation. J. Immunol. 163:4707.
28. Tangye, S. G., A. Ferguson, D. T. Avery, C. S. Ma, and P. D. Hodgkin. 2002. Isotype switching by human B cells is division-associated and regulated by cytokines. J. Immunol. 169:4298.
29. Bird, J. J., D. R. Brown, A. C. Mullen, N. H. Moskowitz, M. A. Mahowald, J. R. Sider, T. F. Gajewski, C. R. Wang, and S. L. Reiner. 1998. Helper T cell differentiation is controlled by the cell cycle. Immunity 9:229.
30. Gudmundsdottir, H., A. D. Wells, and L. A. Turka. 1999. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: Effector function is linked to proliferative capacity. J. Immunol. 162:5212.
31. Murali-Krishna, K., and R. Ahmed. 2000. Cutting edge: naive T cells masquerading as memory cells. J. Immunol. 165:1733.
32. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: Impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1:311.
33. Kehry, M. R., and B. E. Castle. 1994. Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Semin. Immunol. 6:287.
34. Tangye, S. G., B. C. M. van de Weerdt, D. T. Avery, and P. D. Hodgkin. 2002. CD84 is upregulated on a major population of human memory B cells and recruits the SH2-domain containing proteins SAP and EAT-2. Eur. J. Immunol. 32:1640.
35. Tangye, S. G., Y. J. Liu, G. Aversa, J. H. Phillips, and J. E. de Vries. 1998. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J. Exp. Med. 188:1691.
36. + peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188:1679.
37. Lyons, A. B., and C. R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171:131.
38. Merville, P., J. Dechanet, G. Grouard, I. Durand, and J. Banchereau. 1995. T cell-induced B cell blasts differentiate into plasma cells when cultured on bone marrow stroma with IL-3 and IL-10. Int. Immunol. 7:635.
39. Agematsu, K., H. Nagumo, Y. Oguchi, T. Nakazawa, K. Fukushima, K. Yasui, S. Ito, T. Kobata, C. Morimoto, and A. Komiyama. 1998. Generation of plasma cells from peripheral blood memory B cells: Synergistic effect of interleukin-10 and CD27/CD70 interaction. Blood 91:173.
40. Jacquot, S., T. Kobata, S. Iwata, C. Morimoto, and S. F. Schlossman. 1997. CD154/CD40 and CD70/CD27 interactions have different and sequential functions in T cell-dependent B cell responses: Enhancement of plasma cell differentiation by CD27 signaling. J. Immunol. 159:2652.
41. Jung, J., J. Choe, L. Li, and Y. S. Choi. 2000. Regulation of CD27 expression in the course of germinal center B cell differentiation: the pivotal role of IL-10. Eur. J. Immunol. 30:2437.
42. Liu, Y. J., C. Barthelemy, O. de Bouteiller, C. Arpin, I. Durand, and J. Banchereau. 1995. Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to T cells by rapid up-regulation of B7-1 and B7-2. Immunity 2:239.
43. Krajewski, S., R. D. Gascoyne, J. M. Zapata, M. Krajewska, S. Kitada, M. Chhanabhai, D. Horsman, K. Berean, L. D. Piro, I. Fugier-Vivier, et al. 1997. Immunolocalization of the ICE/Ced-3-family protease, CPP32 (Caspase-3), in non-Hodgkin's lymphomas, chronic lymphocytic leukemias, and reactive lymph nodes. Blood 89:3817.
44. + tonsillar plasma cells are rescued from apoptosis by bone marrow fibroblasts. J. Exp. Med. 183:227.
45. Roldan, E., A. Garcia-Pardo, and J. A. Brieva. 1992. 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. 175:1739.
46. + cells. Cytometry 39:231.
47. Tourigny, M. R., J. Ursini-Siegel, H. Lee, K. M. Toellner, A. F. Cunningham, D. S. Franklin, S. Ely, M. Chen, X. F. Qin, Y. Xiong, I. C. MacLennan, and S. Chen-Kiang. 2002. CDK inhibitor p18(INK4c) is required for the generation of functional plasma cells. Immunity 17:179.
48. Vernino, L., L. M. McAnally, J. Ramberg, and P. E. Lipsky. 1992. Generation of nondividing high rate Ig-secreting plasma cells in cultures of human B cells stimulated with anti-CD3-activated T cells. J. Immunol. 148:404.
49. Jelinek, D. F., and P. E. Lipsky. 1983. The role of B cell proliferation in the generation of immunoglobulin-secreting cells in man. J. Immunol. 130:2597.
50. O'Connor, B. P., M. Cascalho, and R. J. Noelle. 2002. Short-lived and long-lived bone marrow plasma cells are derived from a novel precursor population. J. Exp. Med. 195:737.
51. Smith, K. G., T. D. Hewitson, G. J. Nossal, and D. M. Tarlinton. 1996. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26:444.
52. Manz, R. A., A. Thiel, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388:133.
53. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363.
54. Perkins, E. H., T. Sado, and T. Makinodan. 1969. Recruitment and proliferation of immunocompetent cells during the log phase of the primary antibody response. J. Immunol. 103:668.
55. Wehrli, N., D. F. Legler, D. Finke, K. M. Toellner, P. Loetscher, M. Baggiolini, I. C. MacLennan, and H. Acha-Orbea. 2001. Changing responsiveness to chemokines allows medullary plasmablasts to leave lymph nodes. Eur. J. Immunol. 31:609.
56. Hargreaves, D. C., P. L. Hyman, T. T. Lu, V. N. Ngo, A. Bidgol, G. Suzuki, Y. R. Zou, D. R. Littman, and J. G. Cyster. 2001. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194:45.
57. Dilosa, R. M., K. Maeda, A. Masuda, A. K. Szakal, and J. G. Tew. 1991. Germinal center B cells and antibody production in the bone marrow. J. Immunol. 146:4071.
58. Kawano, M. M., K. Mihara, N. Huang, T. Tsujimoto, and A. Kuramoto. 1995. Differentiation of early plasma cells on bone marrow stromal cells requires interleukin-6 for escaping from apoptosis. Blood 85:487.
59. Maruyama, M., K. P. Lam, and K. Rajewsky. 2000. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407:636.
60. Turner, C. A., Jr., D. H. Mack, and M. M. Davis. 1994. Bhmp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77:297.
61. Reimold, A. M., N. N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E. M. Gravallese, D. Friend, M. J. Grusby, F. Alt, and L. H. Glimcher. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300.
62. Usui, T., Y. Wakatsuki, Y. Matsunaga, S. Kaneko, H. Koseki, T. Kita, and H. Kosek. 1997. Overexpression of B cell-specific activator protein (BSAP/Pax-5) in a late B cell is sufficient to suppress differentiation to an Ig high producer cell with plasma cell phenotype. J. Immunol. 158:3197.
63. Shaffer, A. L., X. Yu, Y. He, J. Boldrick, E. P. Chan, and L. M. Staudt. 2000. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13:199.