A germinal center-independent pathway generates unswitched memory B cells early in the primary response

Journal of Experimental Medicine

Volumn 209, Issue 3, 2012, Pages 597-606

  Taylor, Justin J ^a   Pape, Kathryn A ^a   Jenkins, Marc K ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; CD38 ANTIGEN; CD40 ANTIGEN; GLYCOL SALICYLATE; IMMUNOGLOBULIN M;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; GERMINAL CENTER; IMMUNOSTIMULATION; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

5'-NUCLEOTIDASE; ANIMALS; ANTIGENS, CD38; ANTIGENS, CD40; ANTIGENS, DIFFERENTIATION; B-LYMPHOCYTE SUBSETS; DNA-BINDING PROTEINS; FEMALE; GERMINAL CENTER; IMMUNOLOGIC MEMORY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPOTENT STEM CELLS; PHENOTYPE; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 84860363209     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111696     Document Type: Article

References (31)

1. Anderson, S.M., M.M. Tomayko, A. Ahuja, A.M. Haberman, and M.J. Shlomchik. 2007. New markers for murine memory B cells that define mutated and unmutated subsets. J. Exp. Med. 204:2103-2114. http://dx.doi.org/10.1084/jem.20062571
2. Benson, M.J., R. Elgueta, W. Schpero, M. Molloy, W. Zhang, E. Usherwood, and R.J. Noelle. 2009. Distinction of the memory B cell response to cognate antigen versus bystander inflammatory signals. J. Exp. Med. 206: 2013-2025. http://dx.doi.org/10.1084/jem.20090667
3. Blink, E.J., A. Light, A. Kallies, S.L. Nutt, P.D. Hodgkin, and D.M. Tarlinton. 2005. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J. Exp. Med. 201:545-554. http://dx.doi.org/10.1084/jem.20042060
4. Chan, T.D., D. Gatto, K. Wood, T. Camidge, A. Basten, and R. Brink. 2009. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183:3139-3149. http://dx.doi.org/10.4049/jimmunol.0901690
5. Coffey, F., B. Alabyev, and T. Manser. 2009. Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity. 30:599-609. http://dx.doi.org/10.1016/j.immuni.2009.01.011
6. Dent, A.L., A.L. Shaffer, X. Yu, D. Allman, and L.M. Staudt. 1997. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science. 276:589-592. http://dx.doi.org/10.1126/science.276.5312.589
7. Dogan, I., B. Bertocci, V. Vilmont, F. Delbos, J. Mégret, S. Storck, C.A. Reynaud, and J.C. Weill. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10:1292-1299. http://dx.doi.org/10.1038/ni.1814
8. Erickson, L.D., B.G. Durell, L.A. Vogel, B.P. O'Connor, M. Cascalho, T. Yasui, H. Kikutani, and R.J. Noelle. 2002. Short-circuiting long-lived humoral immunity by the heightened engagement of CD40. J. Clin. Invest. 109:613-620.
9. + B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J. Immunol. 177:3728-3736.
10. Fukuda, T., T. Yoshida, S. Okada, M. Hatano, T. Miki, K. Ishibashi, S. Okabe, H. Koseki, S. Hirosawa, M. Taniguchi, et al. 1997. Disruption of the Bcl6 gene results in an impaired germinal center formation. J. Exp. Med. 186:439-448. http://dx.doi.org/10.1084/jem.186.3.439
11. Garside, P., E. Ingulli, R.R. Merica, J.G. Johnson, R.J. Noelle, and M.K. Jenkins. 1998. Visualization of specific B and T lymphocyte interactions in the lymph node. Science. 281:96-99. http://dx.doi.org/10.1126/science.281.5373.96
12. Han, S., K. Hathcock, B. Zheng, T.B. Kepler, R. Hodes, and G. Kelsoe. 1995. Cellular interaction in germinal centers. Roles of CD40 ligand and B7-2 in established germinal centers. J. Immunol. 155:556-567.
13. Itano, A.A., S.J. McSorley, R.L. Reinhardt, B.D. Ehst, E. Ingulli, A.Y. Rudensky, and M.K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 19:47-57. http://dx.doi.org/10.1016/S1074-7613(03)00175-4
14. 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. 30:2437-2443. http://dx.doi.org/10.1002/1521-4141(2000)30:8<2437::AID-IMMU2437>3.0.CO;2-M
15. Klein, U., R. Küppers, and K. Rajewsky. 1997. Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood. 89: 1288-1298.
16. + 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. 188:1679-1689. http://dx.doi.org/10.1084/jem.188.9.1679
17. MacLennan, I.C.M. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139. http://dx.doi.org/10.1146/annurev.iy.12.040194.001001
18. Manz, R.A., M. Löhning, G. Cassese, A. Thiel, and A. Radbruch. 1998. Survival of long-lived plasma cells is independent of antigen. Int. Immunol. 10:1703-1711. http://dx.doi.org/10.1093/intimm/10.11.1703
19. Maul, R.W., and P.J. Gearhart. 2010. AID and somatic hypermutation. Adv. Immunol. 105:159-191. http://dx.doi.org/10.1016/S0065-2776(10)05006-6
20. McHeyzer-Williams, L.J., and M.G. McHeyzer-Williams. 2005. Antigenspecific memory B cell development. Annu. Rev. Immunol. 23:487-513. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115732
21. Moon, J.J., H.H. Chu, J. Hataye, A.J. Pagán, M. Pepper, J.B. McLachlan, T. Zell, and M.K. Jenkins. 2009. Tracking epitope-specific T cells. Nat. Protoc. 4:565-581. http://dx.doi.org/10.1038/nprot.2009.9
22. Nurieva, R.I., Y. Chung, G.J. Martinez, X.O. Yang, S. Tanaka, T.D. Matskevitch, Y.H. Wang, and C. Dong. 2009. Bcl6 mediates the development of T follicular helper cells. Science. 325:1001-1005. http://dx.doi.org/10.1126/science.1176676
23. Pape, K.A., J.J. Taylor, R.W. Maul, P.J. Gearhart, and M.K. Jenkins. 2011. Different B cell populations mediate early and late memory during an endogenous immune response. Science. 331:1203-1207. http://dx.doi.org/10.1126/science.1201730
24. Schittek, B., and K. Rajewsky. 1992. Natural occurrence and origin of somatically mutated memory B cells in mice. J. Exp. Med. 176:427-438. http://dx.doi.org/10.1084/jem.176.2.427
25. 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. http://dx.doi.org/10.1084/jem.20102477
26. + B cells and the dynamics of memory B cell generation. J. Exp. Med. 206:2659-2669. http://dx.doi.org/10.1084/jem.20091087
27. Shinall, S.M., M. Gonzalez-Fernandez, R.J. Noelle, and T.J. Waldschmidt. 2000. Identification of murine germinal center B cell subsets defined by the expression of surface isotypes and differentiation antigens. J. Immunol. 164:5729-5738.
28. Tarlinton, D.M. 2008. Evolution in miniature: selection, survival and distribution of antigen reactive cells in the germinal centre. Immunol. Cell Biol. 86:133-138. http://dx.doi.org/10.1038/sj.icb.7100148
29. Tomayko, M.M., N.C. Steinel, S.M. Anderson, and M.J. Shlomchik. 2010. Cutting edge: Hierarchy of maturity of murine memory B cell subsets. J. Immunol. 185:7146-7150. http://dx.doi.org/10.4049/jimmunol.1002163
30. Toyama, H., S. Okada, M. Hatano, Y. Takahashi, N. Takeda, H. Ichii, T. Takemori, Y. Kuroda, and T. Tokuhisa. 2002. Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity. 17:329-339. http://dx.doi.org/10.1016/S1074-7613(02)00387-4
31. Vremec, D., M. Zorbas, R. Scollay, D.J. Saunders, C.F. Ardavin, L. Wu, and K. Shortman. 1992. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J. Exp. Med. 176:47-58. http://dx.doi.org/10.1084/jem.176.1.47