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Lymphocytes in the Peritoneum Home to the Omentum and Are Activated by Resident Dendritic Cells

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Lymphocytes in the Peritoneum Home to the Omentum and Are Activated by Resident Dendritic Cells Lymphocytes in the Peritoneum Home to the Omentum and Are Activated by Resident Dendritic Cells This information is current as Douglas A. Carlow, Michael R. Gold and Hermann J. of September 25, 2021. Ziltener J Immunol 2009; 183:1155-1165; Prepublished online 24 June 2009; doi: 10.4049/jimmunol.0900409 http://www.jimmunol.org/content/183/2/1155 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2009/06/25/jimmunol.090040 Material 9.DC1 http://www.jimmunol.org/ References This article cites 56 articles, 18 of which you can access for free at: http://www.jimmunol.org/content/183/2/1155.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 25, 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 Lymphocytes in the Peritoneum Home to the Omentum and Are Activated by Resident Dendritic Cells1 Douglas A. Carlow,2* Michael R. Gold,† and Hermann J. Ziltener* The omentum is of interest in the context of obesity-related metabolic disease where adipose tissue exhibits inflammatory changes; however, the immunology of the omentum is underexplored. The greater omentum is draped from the stomach and consists predominantly of adipose tissue studded with lymphoreticular aggregations (milky spots) that distinguish it from other visceral adipose tissues. Milky spots are thought to contain and conduct leukocytes in transit from the blood to the peritoneal cavity, particularly during peritonitis. We show here that both B and T lymphocytes counterflow from the peritoneal cavity to the omentum in mice. Residence in the omentum was brief with a t1/2 residence time of 6 h. Omentum access was pertussis toxin- sensitive, dependent on activation of the Rap1 GTPase, and on the integrin LFA-1. B cells and CD44high T cells accessed the low omentum most efficiently, but homing of resting CD44 T cells was also observed. Omental tissue from normal healthy mice was Downloaded from found to contain CD8؊CD11bhighMHC class IIhighCD11chigh dendritic cells that promoted the rapid activation of T cells entering the omentum and cross-presented soluble OVA or OVA acquired from either OVA-expressing Escherichia coli or OVA-pulsed spleen cells. We conclude that the omentum incorporates two key features of immunological sentinel function, actively supported lymphocyte traffic and dendritic cells, that reinforce a conceptual framework for function in stimulating adaptive immunity. These results extend basic understanding of omental and peritoneal cavity immunology and of how proinflammatory events occurring within the peritoneal cavity might affect adipocyte and hepatocyte metabolism. The Journal of Immunology, 2009, http://www.jimmunol.org/ 183: 1155–1165. he greater omentum in the mouse consists of a band of Most leukocytes found within the murine greater omentum intraabdominal adipose tissue running from the distal are concentrated in milky spots, on the periphery of the adipose T spleen to the duodenal lobe of the pancreas. Among the tissue band also known as the omental fat band (OFB). Milky intraabdominal adipose tissues, the greater omentum is unique be- spots are composed of both myeloid and lymphoid cells and are cause it is thought to function in peritoneal surveillance and as an reactive structures that increase in size and number in response to access route for blood leukocytes entering the resting (1, 2) and peritoneal inflammatory stimuli. Milky spots develop a more or- inflamed (3) peritoneal cavity (PC).3 Murine and human greater ganized structure where T and B cells segregate as in secondary by guest on September 25, 2021 omenta share many microanatomical features despite some differ- lymphoid tissues (5, 6). This structural organization originally led ences in gross appearance (4). The greater omentum is a mobile to the proposal that milky spots were themselves secondary lym- structure that moves with gut peristalsis in the small free volume phoid organs (6). However, segregation of B and T cell areas was of peritoneal fluid. This movement is thought to be essential for the not observed in the resting omentum (5, 7). Furthermore, the fail- omentum to access injured or infected peritoneal surfaces where it ure to detect a significant number of dendritic cells (DCs) within adheres and facilitates repair processes. The omentum has also the omentum (5, 7–9) led to the view that the greater omentum is gained clinical prominence in providing healing capacity when an inflammation-induced lymphoid structure, lacking the defining surgically translocated to wounds. Surprisingly, the immunology characteristics of secondary lymphoid tissues including resident of the omentum is not well understood. professional APCs, permanence in basic structure, and segregation of B and T cell regions in the absence of antigenic stimulation or inflammation. Although there is precedent for omental absorption of protein *The Biomedical Research Centre and the Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada; and and particulates from the PC, lymphatic drainage via this route is †The Department of Microbiology and Immunology and the Infection, Inflammation, considered to be minor relative to exit via diaphragmatic and vis- and Immunity (I3) Research Group, Life Sciences Institute, University of British Columbia, Vancouver, British Columbia, Canada ceral lymphatics (10). Leukocytes may exit the PC upon resolution of an inflammatory response (11, 12) and, in response to innate Received for publication February 4, 2009. Accepted for publication May 21, 2009. immune activators, B-1 B cells migrate from the peritoneum to the 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 spleen via several routes including the omentum (13). Recently, with 18 U.S.C. Section 1734 solely to indicate this fact. splenic B-2 B cells introduced into the PC were shown to access 1 Funding for this work was provided through research grant MOP-77552 to H.J.Z. the omentum, but the molecular mechanisms involved were not from the Canadian Institutes for Health Research (CIHR). identified (2). 2 Address correspondence and reprint requests to Dr. Douglas A. Carlow, The Bio- We report that when splenic or lymph node-derived T and B medical Research Centre, 2222 Health Sciences Mall, University of British Columbia, Vancouver, B.C. V6T 1Z3, Canada. E-mail address: [email protected] cells were introduced into the PC, they both accumulate rapidly 3 Abbreviations used in this paper: PC, peritoneal cavity; CTO, CellTracker Orange; and prominently in the OFB. These observations stimulated ques- DC, dendritic cell; MHC-II, MHC class II; OFB, omental fat band; Rap-GAPII, Rap- tions about the functional significance of such lymphocyte traffic, specific GTPase-activating protein II. in particular for T cells. We therefore investigated the mechanisms Copyright © 2009 by The American Association of Immunologists, Inc. 0022-1767/09/$2.00 underlying lymphocyte entry into the OFB, the distribution and www.jimmunol.org/cgi/doi/10.4049/jimmunol.0900409 1156 PERITONEAL LYMPHOCYTE HOMING TO OMENTAL DCs dynamics of lymphocytes within the OFB, and the nature and func- night culture confirmed that OFB walkout preparations were not contam- tionality of APCs within the OFB. inated with peripheral blood DCs or free peritoneal DCs. Tracking dye labeling in vitro and in vivo Materials and Methods CFSE, CellTracker Orange CMTMR, and CellTracker Orange CMRA Mice tracking dyes (Molecular Probes/Invitrogen) were used according to the 4 Mice aged 7–16 wk were used for analyses. C57BL/6/J (B6), BALB/c, manufacturer’s instructions and as described in Extended Methods. CBA/J, H-Y (14), OT-I (15), and OT-II (16) TCR transgenic mice were Pertussis toxin treatment bred at the specific pathogen-free animal facility at the Biomedical Re- search Centre (University of British Columbia). Procedures employed in Cells were incubated for2hat37°C in the presence or absence of 100 this study were approved by the Animal Care Committee at the University ng/ml pertussis toxin in culture medium, washed, labeled with tracking of British Columbia. dyes, and injected. Media and buffers Rap-GAPII-expressing WEHI-231 cells Standard media was RPMI 1640 supplemented with 8% FCS, 5 ϫ 10Ϫ5 M Preliminary experiments established that WEHI-231 cells (American Type ϫ 2-ME, 100 U/ml penicillin, 100 U/ml streptomycin (StemCell Technolo- Culture Collection CRL 1702), a (BALB/c New Zealand Black)F1 mu- gies), and 2 mM glutamine (Sigma-Aldrich). HBSS lacking Mg2ϩ and rine cell line thought to represent immature B cells, accumulated efficiently Ca2ϩ (Hanks’ (Ϫ)) and HBSS containing Mg2ϩ and Ca2ϩ (Hanks (ϩ)) in the omentum after i.p. injection. WEHI-231 cells expressing Rap-spe- were used as indicated. DMEM supplemented with 10 mM HEPES, 0.5% cific GTPase-activating protein II (Rap-GAPII) or the empty pMSCVpuro BSA (Sigma-Aldrich, catalog no. A7906), and 5 ϫ 10Ϫ5 M 2-ME (DBH vector (BD Clontech) were generated and characterized by McLeod et al. Media) was used for Ab blocking experiments. (21). Ten million cells of the control vector, or Rap-GAP, transfected WEHI-231 cells were labeled with distinct tracking dyes, coinjected i.p., Downloaded from Antibodies and compared for in vivo homing efficiency to the OFB 2 h later.
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