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7432.Full.Pdf CD27 Is Acquired by Primed B Cells at the Centroblast Stage and Promotes Germinal Center Formation This information is current as Yanling Xiao, Jenny Hendriks, Petra Langerak, Heinz Jacobs of September 29, 2021. and Jannie Borst J Immunol 2004; 172:7432-7441; ; doi: 10.4049/jimmunol.172.12.7432 http://www.jimmunol.org/content/172/12/7432 Downloaded from References This article cites 43 articles, 23 of which you can access for free at: http://www.jimmunol.org/content/172/12/7432.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 29, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2004 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology CD27 Is Acquired by Primed B Cells at the Centroblast Stage and Promotes Germinal Center Formation1 Yanling Xiao, Jenny Hendriks, Petra Langerak, Heinz Jacobs, and Jannie Borst2 Studies on human B cells have featured CD27 as a marker and mediator of the B cell response. We have studied CD27 expression and function on B cells in the mouse. We find that B cells acquire CD27 at the centroblast stage and lose it progressively upon further differentiation. It is not a marker for somatically mutated B cells and is present at very low frequency on memory B cells. Enrichment of CD27 among centroblasts and the presence of its ligand CD70 on occasional T and B cells in or near germinal centers (GCs) suggested a role for CD27/CD70 interactions in clonal B cell expansion. Accordingly, GC formation in response to influenza virus infection was delayed in CD27 knockout mice. CD27 deficiency did not affect somatic hypermutation or serum levels of virus-specific IgM, IgG, and IgA attained in primary and recall responses. Adoptive transfer of T and B cells into ؊/؊ CD27/CD28 mice revealed that CD27 promotes GC formation and consequent IgG production by two distinct mechanisms. Downloaded from Stimulation of CD27 on B cells by CD28؉ Th cells accelerates GC formation, most likely by promoting centroblast expansion. In addition, CD27 on T cells can partially substitute for CD28 in supporting GC formation. The Journal of Immunology, 2004, 172: 7432–7441. xpression of TNFR family member CD27 is restricted to CD27ϩ B cells as memory B cells. In particular, CD27 was re- ϩ ϩ naive and activated CD4 and CD8 T cells and subsets cently found at low levels on all GC B cells from human tonsils, http://www.jimmunol.org/ E of B and NK cells. Its membrane-bound ligand CD70 is and dramatically up-regulated upon their in vitro differentiation confined to activated lymphocytes and mature dendritic cells (1– into plasma cells (17). In this study, we have analyzed in detail the 4). In vitro studies have established that CD27 promotes expansion expression of CD27 on B cells in the mouse and find it in line with Ϫ/Ϫ of newly activated T cells (1, 5, 6). In CD27 mice, generation a contribution of CD27 to centroblast expansion. ϩ ϩ and maintenance of CD4 and CD8 effector T cells in response In vitro studies on human B cells indicate that CD27 can pro- to antigenic challenge is impaired (7). We have recently resolved mote IgM, IgG, IgA, and IgE secretion (10, 16, 18, 19). Whether that CD27 rescues activated T cells from death, and in this way, CD27/CD70 interactions enhance Ig production by delivering dif- increments the yield of live T cells upon their clonal expansion at ferentiation signals to B cells or by sustaining expansion of dif- the site of priming. In addition, CD27 exerts a prosurvival effect on by guest on September 29, 2021 ϩ ϩ ferentiating cells is unclear. Jacquot et al. (20) found that CD27 did CD4 and CD8 T cells at tissue sites (8). not drive expansion of activated B cells, but promoted the gener- In humans, CD27 is induced by B cell receptor triggering and ation of a plasma cell phenotype and IgG secretion. However, maintained long-term (9, 10). CD27ϩ B cells are predominantly other data argue that CD27 does promote expansion of activated B found in germinal centers (GCs)3 and marginal zones (11, 12). It cells (19, 21). All in vitro studies rely on deliberate stimulation of is considered a marker for memory B cells (13) based on the fol- ϩ ϩ CD27 with CD70 transfectants. Whether CD27 signals are invoked lowing observations: 1) among IgM D B cells in blood and mar- ϩ in vivo will depend on availability of CD70. In both humans and ginal zones, CD27 cells contain somatic Ig gene mutations (12, ϩ mice, CD70 is induced by Ag receptor triggering in T and B cells 14); 2) Ig class switching is more frequent among CD27 than CD27Ϫ B cells (9); 3) upon activation, CD27ϩ B cells secrete Ig (2, 3, 22). In humans, CD70 has been detected on B cells, which more efficiently than CD27Ϫ B cells (15); and 4) cord blood B may represent recent GC immigrants (23). CD70 expression is cells lack CD27, while the percentage of CD27ϩ B cells in blood very transient and plasma membrane levels are often extremely increases with age (16). Although these findings are in line with low, making it difficult to detect (3). In this study, we have used CD27 being a hallmark of primed B cells, they do not classify all confocal laser microscopy to define at what point during the GC reaction CD27/CD70 interactions might play a part. Comparing wild-type and CD27Ϫ/Ϫ mice, we have determined how CD27 contributes to the B cell response to influenza virus. An Division of Immunology, The Netherlands Cancer Institute, Amsterdam, The Neth- erlands effect of CD27 deletion was expected, because anti-viral T cell Received for publication January 5, 2004. Accepted for publication March 26, 2004. responses in draining lymph nodes and the lung are severely im- Ϫ/Ϫ The costs of publication of this article were defrayed in part by the payment of page paired in CD27 mice (7). Apart from determining its impact on charges. This article must therefore be hereby marked advertisement in accordance Ig production, we have studied the role of CD27 in GC formation. with 18 U.S.C. Section 1734 solely to indicate this fact. Present data suggest that CD27 promotes B cell expansion and/or 1 This work was supported by The Netherlands Organization for Scientific Research differentiation into plasma cells. Alternatively or in addition, CD27 and by the Dutch Cancer Society. may promote the B cell response indirectly by facilitating Th cell 2 Address correspondence and reprint requests to Dr. Jannie Borst, Division of Im- munology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, expansion. The costimulatory receptor CD28 and its ligands play The Netherlands. E-mail address: [email protected] a key role in GC formation. Mice lacking CD28 function are 3 Abbreviations used in this paper: GC, germinal center; DLN, draining lymph nodes; greatly defective in Th-dependent IgG responses to hapten-protein FDC, follicular dendritic cells; FSC, forward scatter; HPE, high performance ELISA buffer; OX40L, OX40 ligand; PNA, peanut agglutinin; SA, streptavidin; SHM, so- conjugates, and lack obvious GCs (24–27). To map a contribution matic hypermutation; TR, Texas Red. of CD27 to the GC reaction relative to that of CD28, we generated Copyright © 2004 by The American Association of Immunologists, Inc. 0022-1767/04/$02.00 The Journal of Immunology 7433 mice genetically deficient for both CD27 and CD28, and per- with sera, serially diluted in high performance ELISA buffer (HPE; San- formed adoptive transfer experiments with T and B cells from quin, Amsterdam, The Netherlands) with 1% BSA, followed by biotinyl- CD28Ϫ/Ϫ or CD27Ϫ/Ϫ mice. Collective experiments show that ated goat anti-mouse IgM, -G1, -G2a, -G2b, -G3, or -A mAb (Southern Biotechnology Associates), diluted 1:2,500 in HPE with 1% BSA, and CD27 can support GC formation and Ig production via a major SA-conjugated HRP (Sigma-Aldrich, St. Louis, MO), diluted 1:10,000 in CD28-dependent route that proceeds via CD27 on B cells, and via HPE with 1% BSA. Substrate 3,3Ј,5,5Ј tetramethylbenzidin (Merck, Darm- a minor CD28-independent route that requires CD27 on T cells. stadt, Germany) was added at 0.1 mg/ml (100 ␮l/well), together with 0.06% hydrogen peroxide in 0.1 M sodium acetate (pH 5.5). The reaction was stopped with2MHSO , and OD was read by a Wallac 1420 Materials and Methods 2 4 450 VICTOR2 multilabel counter (PerkinElmer Life Sciences, Boston, MA). Mice Endpoint titers were expressed as reciprocal log3 of the last dilution, which Ϫ Ϫ Ϫ Ϫ Ն Wild-type, CD27 / (7), and CD28 / mice (24) were on a C57BL/6 gave an OD450 of 0.1 OD unit above the OD450 of the negative control background and used for experiments at 6–10 wk of age, in accordance (pooled serum from nonimmunized mice). with national and institutional guidelines.
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