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A Novel Pathway for Salmonella B Cell Receptor-Mediated B Cell Receptor-Mediated Internalization of Salmonella: A Novel Pathway for Autonomous B Cell Activation and Antibody Production This information is current as of October 7, 2021. Yuri Souwer, Alexander Griekspoor, Tineke Jorritsma, Jelle de Wit, Hans Janssen, Jacques Neefjes and S. Marieke van Ham J Immunol 2009; 182:7473-7481; ; doi: 10.4049/jimmunol.0802831 Downloaded from http://www.jimmunol.org/content/182/12/7473 Supplementary http://www.jimmunol.org/content/suppl/2009/06/02/182.12.7473.DC1 Material http://www.jimmunol.org/ References This article cites 46 articles, 21 of which you can access for free at: http://www.jimmunol.org/content/182/12/7473.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on October 7, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *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 © 2009 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology B Cell Receptor-Mediated Internalization of Salmonella: A Novel Pathway for Autonomous B Cell Activation and Antibody Production1 Yuri Souwer,2*† Alexander Griekspoor,2† Tineke Jorritsma,* Jelle de Wit,* Hans Janssen,† Jacques Neefjes,3† and S. Marieke van Ham3* The present paradigm is that primary B cells are nonphagocytosing cells. In this study, we demonstrate that human primary B cells are able to internalize bacteria when the bacteria are recognized by the BCR. BCR-mediated internalization of Salmonella typhimurium results in B cell differentiation and secretion of anti-Salmonella Ab by the Salmonella-specific B cells. In addition, BCR-mediated internalization leads to efficient Ag delivery to the MHC class II Ag-loading compartments, even though Salmonella ,remains vital intracellularly in primary B cells. Consequently, BCR-mediated bacterial uptake induces efficient CD4؉ T cell help which boosts Salmonella-specific Ab production. BCR-mediated internalization of Salmonella by B cells is superior over extra- Downloaded from cellular Ag extraction to induce rapid and specific humoral immune responses and efficiently combat infection. The Journal of Immunology, 2009, 182: 7473–7481. efense against pathogens is essential for survival and is compartments (termed MIIC4 for MHC class II-containing com- controlled by the innate and acquired arms of the im- partment) for loading of Ag onto newly synthesized MHC class II D mune system. Ag presentation by B lymphocytes is molecules (3). Besides internalization of Ag, the BCR drives in- http://www.jimmunol.org/ needed to generate high-affinity Abs (1, 2). Development of an tracellular targeting by accelerating the delivery of Ag to MIICs effective humoral immune response is mediated by two actions of (9). Furthermore, BCR signaling ignited by Ag induces acidifica- the BCR: transmembrane signaling through BCR complexes to tion of the MIICs, which favors Ag loading onto newly synthe- induce B cell differentiation and Ag internalization for processing sized MHC class II molecules (10). Together, these cellular adap- tations enable B cells to preferentially present specific Ags that followed by MHC class II-mediated presentation to acquire T cell ϩ help. The proper execution of both actions requires binding of a have been internalized via the BCR to CD4 T cells. Since primary B cells are considered to be not phagocytic, it polyvalent Ag to multiple BCR molecules. Indeed, many B cell is unclear how they acquire Ags from bacteria for Ag presen- Ags are polyvalent as they are bound in multiple copies to the by guest on October 7, 2021 tation. B cells can present particulate Ags in the context of particulate surfaces of microbes or cells (3). MHC class II (11–14) and are able to extract Ag from a non- The role of CD4ϩ T cells in the induction of protective immu- ϩ internalizable surface (15). Studies on MHC-mediated presen- nity against pathogens is well established (4, 5). CD4 T cell tation of BCR-specific Ags are mainly performed with soluble activation requires MHC class II Ag presentation after Ag pro- Ags or with pre-cross-linked anti-BCR Abs. We used Salmo- cessing in the endocytic pathway and subsequent binding of anti- nella typhimurium as a model system to study MHC class II Ag genic peptides to MHC class II molecules, a process controlled by presentation of particulate, polyvalent Ags, and B cell activa- the MHC class II chaperones HLA-DM and HLA-DO (6–8). B tion. Being facultative intracellular pathogens, immunity to Sal- cells use their BCR to concentrate specific Ag to the Ag-loading monella requires adequate humoral and cell-mediated immune responses (16, 17). Salmonella invades host macrophages, but also many other cells and establishes an intracellular niche in- side discrete vacuoles, known as Salmonella-containing vacu- *Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, oles or SCVs (18). This feature of Salmonella is considered Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; crucial for their survival and pathogenicity (19, 20). † and Division of Tumor Biology, The Netherlands Cancer Institute, Amsterdam, The In this report, we show that B cells are highly efficient phago- Netherlands cytes of inert particles, like beads, when these particles are Received for publication August 27, 2008. Accepted for publication April 3, 2009. recognized by the BCR. B cells are thus ligand-selective phago- The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance cytic cells. BCR-mediated internalization of Salmonella gener- with 18 U.S.C. Section 1734 solely to indicate this fact. ates autonomous B cell activation and rapid anti-Salmonella Ab 1 This work was supported by grants from the Dutch Cancer Society (Koningin Wil- secretion. Immediate intimate contact and fusion occurs be- helmina Fonds) (Grant NKI 2001-2415), the Landsteiner Foundation for Blood Research tween MIICs and SCVs. Consequently, Ag presentation and (Grant 0533), and The Netherlands Organization for Scientific Research (De Nederlandse ϩ Organisatie voor Wetenschappelijk Onderzoek). proliferation of Salmonella-specific CD4 T cells is induced. 2 Y.S. and A.G. contributed equally to this work. 3 Address correspondence and reprint requests to Dr. Jacques Neefjes, Division of 4 Abbreviations used in this paper: MIIC, MHC class II-containing compartment; Tumor Biology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX, Am- SCV, Salmonella-containing vacuole; EM, electron microscopy; DAPI, 4Ј,6- sterdam, The Netherlands and Dr. S. Marieke van Ham, Department of Immunopa- diamidino-2-phenylindole; LB, Luria-Bertani; SPI, Salmonella pathogenicity island; thology, Sanquin Research and Landsteiner Laboratory, Academic Medical Center, DC, dendritic cell. University of Amsterdam, Plesmanlaan 125, 1066 CX, Amsterdam, The Netherlands. E-mail addresses: [email protected] and [email protected] Copyright © 2009 by The American Association of Immunologists, Inc. 0022-1767/09/$2.00 www.jimmunol.org/cgi/doi/10.4049/jimmunol.0802831 7474 BCR-MEDIATED BACTERIAL UPTAKE Although BCR-mediated internalization suffices to drive Ab The maximum proliferation capacity of T lymphocytes (varying between production, T cell help further improves the response. The ob- 35 and 60 ϫ 103 cpm) was established by stimulation with anti-CD3 servation that B cells can proliferate and differentiate autono- (CLB.T3/4.E; Sanquin) and anti-CD28 (CLB.CD28/1; Sanquin), which were both used at 1 ␮g/ml. After 5 and 12 days, 150 ␮l of supernatant was mously after Salmonella uptake is important in light of the re- ϩ collected for Ab measurement and fresh medium was added. To study the maining Ab responses to pathogens when CD4 T cell help kinetics of Ag presentation, B cells incubated with Salmonella were irra- fails, as is the case in HIV patients. diated with 60 Gy at indicated time points before incubation with T cells. For B/T cell proliferation assays, after 5 days of culturing, [3H]thymidine (GE Healthcare) was added at a final concentration of 1 ␮Ci/ml (37 kBq/ Materials and Methods ml) for 16 h. Cells were harvested on glass fiber filters (Wallac) and ra- Abs, beads, and fluorophores dioactivity was measured with a 1205 Betaplate liquid scintillation counter (Wallac). For blocking experiments, B cells were preincubated with 5 Goat anti-mouse IgG-conjugated Dynabeads M-450 (Dynal Biotech) were ␮g/ml anti-HLA-DR (L243) for 30 min before T cells were added. For the coated with mAb anti-human IgM (MH15; Sanquin). The anti-human IgM Ab ϩ Ag-specificity assay, CD4 T cells were CFSE labeled and cocultured with (MH15) was mixed with mAb anti-S. typhimurium LPS (1E6; Biodesign In- B cells that had taken up Salmonella. The dividing T cells were sorted after ternational) and rat anti-mouse IgG1 (RM161.1; Sanquin) to generate BCR- 6 days and cultured with 10 IU/ml IL-2 (Chiron) for 6 more days. PBMCs LPS tetrameric Ab complexes. The mAb anti-human HLA-DR (L243) (21) were labeled with CFSE and incubated with tetanus toxoid (7,5 ␮g/ml; was used to block MHC class II-TCR interaction in T cell proliferation assays. Statens Serum Institut, Copenhagen, Denmark) for 11 days, with 10 IU/ml For immunoelectron microscopy (EM), mAb anti-human CD63 (435; San- ϩ IL-2 added on day 6, and proliferating CD4 T cells were sorted.
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