IgM(high)CD21(high) lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells

Journal of Immunology

Volumn 162, Issue 12, 1999, Pages 7198-7207

  Oliver, Alyce M ^a   Martin, Flavius ^a   Kearney, John F ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN M; IMMUNOGLOBULIN E RECEPTOR; LIPOPOLYSACCHARIDE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CELL LINE; CONTROLLED STUDY; EFFECTOR CELL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE; ANIMAL; ANTIGEN PRESENTING CELL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL CLONE; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-PRESENTING CELLS; B-LYMPHOCYTE SUBSETS; CLONE CELLS; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, COMPLEMENT 3D; RECEPTORS, IGE; SPLEEN; T-LYMPHOCYTES; UP-REGULATION;

EID: 0033563309     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Rolink, A., and F. Melchers. 1996. B-cell development in the mouse. Immunol. Lett. 54:157.
2. Hardy, R. R., and K. Hayakawa. 1995. B-lineage differentiation stages resolved by multiparameter flow cytometry. Ann. NY Acad. Sci. 764:19.
3. Burrows, P. D., and M. D. Cooper. 1997. B cell development and differentiation. Curr. Opin. Immunol. 9:239.
4. Liu, Y. J., and C. Arpin. 1997. Germinal center development. Immunol. Rev. 156:111.
5. Eugster, H. P., M. Muller, U. Karrer, B. D. Car, B. Schnyder, V. M. Eng, Woerly, H. M. Le, P. F. Di, M. Aguet, et al. 1996. Multiple immune abnormalities in tumor necrosis factor and lymphotoxin-α double-deficient mice. Int. Immunol. 8:23.
6. Kelsoe, G., and B. Zheng. 1993. Sites of B-cell activation in vivo. Curr. Opin. Immunol. 5:418.
7. McHeyzer-Williams, M. G., M. J. McLean, P. A. Lalor, and G. J. Nossal. 1993. Antigen-driven B cell differentiation in vivo. J. Exp. Med. 178:295.
8. Nossal, G. J. 1994. Differentiation of the secondary B-lymphocyte repertoire: the germinal center reaction. Immunol. Rev. 137:173.
9. Zinkernagel, R. M., M. F. Bachmann, T. M. Kundig, S. Oehen, H. Pirchet, and H. Hengartner. 1996. On immunological memory. Annu. Rev. Immunol. 14:333.
10. Cumano, A., and K. Rajewsky. 1986. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5:2459.
11. Rajewsky, K. 1993. B-cell lifespans in the mouse-why to debate what? Immunol. Today 14:40.
12. Oliver, A. M., F. Martin, G. L. Gartland, R. H. Carter, and J. F. Kearney. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27:2366.
13. Stall, A. M., S. M. Wells, and K. P. Lam. 1996. B-1 cells: unique origins and functions. Semin. Immunol. 8:45.
14. Kumararatne, D. S , H. Bazin, and I. C. MacLennan. 1981. Marginal zones: the major B cell compartment of rat spleens. Eur. J. Immunol. 11:858.
15. Gray, D., D. S. Kumararatne, J. Lortan, M. Khan, and I. C. MacLennan. 1984. Relation of intra-splenic migration of marginal zone B cells to antigen localization on follicular dendritic cells. Immunology 52:659.
16. Cyster, J. G., and C. C. Goodnow. 1995. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 2:13.
17. Milstein, C., and M. S. Neuberger. 1996. Maturation of the immune response. Adv. Protein Chem. 49:451.
18. Foote, J., and C. Milstein. 1991. Kinetic maturation of an immune response. Nature 352:530.
19. Smith, K. G., A. Light, G. J. Nossal, and D. M. Tarlinton. 1997. The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 16:2996.
20. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature 381:751.
21. 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.
22. Dunn-Walters, D. K., P. G. Isaacson, and J. Spencer. 1995. Analysis of mutations in immunoglobulin heavy chain variable region genes of microdissected marginal zone (MGZ) B cells suggests that the MGZ of human spleen is a reservoir of memory B cells. J. Exp. Med. 182:559.
23. Hayakawa, K., Y. S. Li, R. Wasserman, S. Sauder, S. Shinton, and R. R. Hardy. 1997. B lymphocyte developmental lineages. Ann. NY Acad. Sci. 815:15.
24. Allman, D. M., S. E. Ferguson, V. M. Lentz, and M. P. Cancro. 1993. Peripheral B cell maturation. II. Heat-stable antigen(hi) splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J. Immunol. 151:4431.
25. Snapper, C. M., H. Yamada, D. Smoot, R. Sneed, A. Lees, and J. J. Mond. 1993. Comparative in vitro analysis of proliferation, Ig secretion, and Ig class switching by murine marginal zone and follicular B cells. J. Immunol. 150:2737.
26. Waldschmidt, T. J., F. G. Kroese, L. T. Tygrett, D. H. Conrad, and R. G. Lynch. 1991. The expression of B cell surface receptors. III. The murine low-affinity IgE Fc receptor is not expressed on Ly 1 or 'Ly 1-like' B cells. Int. Immunol. 3:305.
27. Kumararatne, D. S., and I. C. MacLennan. 1981. Cells of the marginal zone of the spleen are lymphocytes derived from recirculating precursors. Eur. J. Immunol. 11:865.
28. Kumararatne, D. S., and I. C. MacLennan. 1982. The origin of marginal-zone cells. Adv. Exp. Med. Biol. 149:83.
29. Jennings, C. D., and K. A. Foon. 1997. Recent advances in flow cytometry: application to the diagnosis of hematologic malignancy. Blood 90:2863.
30. Fu, Y. X., G. Huang, M. Matsumoto, H. Molina, and D. D. Chaplin. 1997. Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc. Natl. Acad. Sci. USA 94:5739.
31. Martin, F., X. Chen, and J. F. Kearney. 1997. Development of VH81X transgene-bearing B cells in fetus and adult: sites for expansion and deletion in conventional and CD5/B1 cells. Int. Immunol. 9:493.
32. Martin, F., W. J. Won, and J. F. Kearney. 1998. Generation of the germline peripheral B cell repertoire: VH81X-λ B cells are unable to complete all developmental programs. J. Immunol. 160:3748.
33. Kinoshita, T., J. Takeda, K. Hong, H. Kozono, H. Sakai, and K. Inoue. 1988. Monoclonal antibodies to mouse complement receptor type 1 (CR1). Their use in a distribution study showing that mouse erythrocytes and platelets are CR1-negative. J. Immunol. 140:3066.
34. Kinoshita, T., G. Thyphronitis, G. C. Tsokos, F. D. Finkelman, K. Hong, H. Sakai, and K. Inoue. 1990. Characterization of murine complement receptor type 2 and its immunological cross-reactivity with type 1 receptor. Int. Immunol. 2:651.
35. Oliver, A. M., F. Martin, and J. F. Kearney. 1997. Mouse CD38 is down-regulated on germinal center B cells and mature plasma cells. J. Immunol. 158:1108.
36. Takahashi, K., Y. Kozono, T. J. Waldschmidt, D. Berthiaume, R. J. Quigg, Baron, and V. M. Holers. 1997. Mouse complement receptors type 1 (CR1; CD35) and type 2 (CR2;CD21): expression on normal B cell subpopulations and decreased levels during the development of autoimmunity in MRL/lpr mice. J. Immunol. 159:1557.
37. Chen, X., F. Martin, K. A. Forbush, R. M. Perlmutter, and J. F. Kearney. 1997. Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone. Int. Immunol. 9:27.
38. Hartley, S. B., and C. C. Goodnow. 1994. Censoring of self-reactive B cells with a range of receptor affinities in transgenic mice expressing heavy chains for a lysozyme-specific antibody. Int. Immunol. 6:1417.
39. Chen, J., M. Trounstine, F. W. Alt, F. Young, C. Kurahara, J. F. Loring, and D. Huszar. 1993. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int. Immunol. 5:647.
40. Timens, W., A. Boes, and S. Poppema. 1989. Human marginal zone B cells are not an activated B cell subset: strong expression of CD21 as a putative mediator for rapid B cell activation. Eur. J. Immunol. 19:2163.
41. Waldschmidt, T., K. Snapp, T. Foy, L. Tygrett, and C. Carpenter. 1992. B-cell subsets defined by the Fc epsilon R. Ann. NY Acad. Sci. 651:84.
42. Lenschow, D. J., A. I. Sperling, M. P. Cooke, G. Freeman, L. Rhee, D. C. Decker, G. Gray, L. M. Nadler, C. C. Goodnow, and J. A. Bluestone. 1994. Differential up-regulation of the B7-1 and B7-2 costimulatory molecules after Ig receptor engagement by antigen. J. Immunol. 153:1990.
43. Thompson, C. B. 1995. Distinct roles for the costimulatory ligands B7-1 and B7-2 in T helper cell differentiation? Cell 81:979.
44. Goodnow, C. C. 1992. Transgenic mice and analysis of B-cell tolerance. Annu. Rev. Immunol. 10:489.
45. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, and K. Raphael. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676.
46. Sanderson, R. D., P. Lalor, and M. Bernfield. 1989. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1:27.
47. Arpin, C., J. Dechanet, K. C. Van, 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.
48. Buiting, A. M., R. Z. De, G. Kraal, and R. N. Van. 1996. Humoral immune responses against particulate bacterial antigens are dependent on marginal metallophilic macrophages in the spleen. Scand. J. Immunol. 43:398.
49. Seiler, P., P. Aichele, B. Odermatt, H. Hengartner, R. M. Zinkernagel, and R. A. Schwendener. 1997. Crucial role of marginal zone macrophages and marginal zone metallophils in the clearance of lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 27:2626.
50. Kraal, G. 1992. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132:31.
51. Oldfield, S., J. E. Lortan, M. A. Hyatt, and I. C. MacLennan. 1988. Marginal zone B cells and the localisation of antigen on follicular dendritic cells. Adv. Exp. Med. Biol. 237:99.
52. Humphrey, J. H., D. Grennan, and V. Sundaram. 1984. The origin of follicular dendritic cells in the mouse and the mechanism of trapping of immune complexes on them. Eur. J. Immunol. 14:859.
53. Fang, Y., C. Xu, Y. X. Fu, V. M. Holers, and H. Molina. 1998. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J. Immunol. 160:5273.
54. Kosco-Vilbois, M. H., D. Gray, D. Scheidegger, and M. Julius. 1993. Follicular dendritic cells help resting B cells to become effective antigen-presenting cells: induction of B7/BB1 and upregulation of major histocompatibility complex class II molecules. J. Exp. Med. 178:2055.
55. Linton, P. J., D. Lo, L. Lai, G. J. Thorbecke, and N. R. Klinman. 1992. Among naive precursor cell subpopulations only progenitors of memory B cells originate germinal centers. Eur. J. Immunol. 22:1293.
56. Linton, P. L., D. J. Decker, and N. R. Klinman. 1989. Primary antibody-forming cells and secondary B cells are generated from separate precursor cell subpopulations. Cell 59:1049.
57. Liu, Y. J., C. Barthelemy, B. O. de, 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.
58. MacLennan, I. C., and Y. J. Liu, 1991. Marginal zone B cells respond both to polysaccharide antigens and protein antigens. Res. Immunol. 142:346.
59. Hathcock, K. S., G. Laszlo, C. Pucillo, P. Linsley, and R. J. Hodes. 1994. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 180:631.
60. Hathcock, K. S., and R. J. Hodes. 1996. Role of the CD28-B7 costimulatory pathways in T cell-dependent B cell responses. Adv. Immunol. 62:131.
61. Kozono, Y., R. Abe, H. Kozono, R. G. Kelly, T. Azuma, and V. M. Holers. 1998. Cross-linking CD21/CD35 or CD19 increases both B7-1 and B7-2 expression on murine splenic B cells. J. Immunnl. 160:1565.
62. + T cells. J. Exp. Med. 188:651.
63. Dunn-Walters, D. K., L. Boursier, J. Spencer, and P. G. Isaacson. 1998. Analysis of immunoglobulin genes in splenic marginal zone lymphoma suggests ongoing mutation. Hum. Pathol. 29:585.
64. Inaoki, M., S. Sato, B. C. Weintraub, C. C. Goodnow, and T. F. Tedder. 1997. CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J. Exp. Med. 186:1923.
65. Ahearn, J. M., M. B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R. G. Howard, T. L. Rothstein, and M. C. Carroll. 1996. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 4:251.
66. Arnold, L. W., C. A. Pennell, S. K. McCray, and S. H. Clarke. 1994. Development of B-1 cells: segregation of phosphatidyl choline-specific B cells to the B-1 population occurs after immunoglobulin gene expression. J. Exp. Med. 179:1585.
67. Murakami, M., K. Nakajima, K. Yamazaki, T. Muraguchi, T. Serikawa, and T. Honjo. 1997. Effects of breeding environments on generation and activation of autoreactive B-1 cells in anti-red blood cell autoantibody transgenic mice. J. Exp. Med. 185:791.
68. Roark, J. H., S. H. Park, J. Jayawardena, U. Kavita, M. Shannon, and A. Bendelac. 1998. CD1. 1 expression by mouse antigen-presenting cells and marginal zone B cells. J. Immunol. 160:3121.
69. Brossay, L., D. Jullien, S. Cardell, B. C. Sydora, N. Burdin, R. L. Modlin, and M. Kronenberg. 1997. Mouse CD1 is mainly expressed on hemopoietic-derived cells. J. Immunol. 159:1216.
70. Snapper, C. M., F. R. Rosas, L. Jin, C. Wortham, M. R. Kehry, and J. J. Mond. 1995. Bacterial lipoproteins may substitute for cytokines in the humoral immune response to T cell-independent type II antigens. J. Immunol. 155:5582.
71. Ernst, W. A., J. Maher, S. Cho, K. R. Niazi, D. Chatterjee, D. B. Moody, G. S. Besra, Y. Watanabe, P. E. Jensen, S. A. Porcelli, et al. 1998. Molecular interaction of CD1b with lipoglycan antigens. Immunity 8:331.