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Lipopolysaccharide Versus Lipoteichoic Acid Leukocyte Profound Differences in Leukocyte-Endothelial Cell Responses to Lipopolysaccharide Versus Lipoteichoic Acid This information is current as Bryan G. Yipp, Graciela Andonegui, Christopher J. Howlett, of September 25, 2021. Stephen M. Robbins, Thomas Hartung, May Ho and Paul Kubes J Immunol 2002; 168:4650-4658; ; doi: 10.4049/jimmunol.168.9.4650 http://www.jimmunol.org/content/168/9/4650 Downloaded from References This article cites 49 articles, 24 of which you can access for free at: http://www.jimmunol.org/content/168/9/4650.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 25, 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 © 2002 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Profound Differences in Leukocyte-Endothelial Cell Responses to Lipopolysaccharide Versus Lipoteichoic Acid1 Bryan G. Yipp,* Graciela Andonegui,† Christopher J. Howlett,‡ Stephen M. Robbins,‡ Thomas Hartung,§ May Ho,* and Paul Kubes2† We have investigated the effects of LPS from Escherichia coli, lipoteichoic acid (LTA), and peptidoglycan (PepG) from Staphy- lococcus aureus, and live S. aureus on leukocyte-endothelial interactions in vivo using intravital microscopy to visualize muscle microvasculature. Systemic vs local administration of LPS induced very different responses. Local administration of LPS into muscle induced significant leukocyte rolling, adhesion, and emigration in postcapillary venules at the site of injection. LPS given systemically dramatically dropped circulating leukocyte counts and increased neutrophils in the lung. However, the drop in circulating leukocytes was not associated with leukocyte sequestration to the site of injection (peritoneum) nor to peripheral microvessels in muscles. Unlike LPS, various preparations of LTA had no systemic and very minor local effect on leukocyte- Downloaded from endothelial interactions, even at high doses and for prolonged duration. LPS, but not LTA, potently activated human endothelium to recruit leukocytes under flow conditions in vitro. Endothelial adhesion molecule expression was also increased extensively with LPS, but not LTA. Interestingly, systemic administration of live S. aureus induced leukocyte-endothelial cell responses similar to LPS. PepG was able to induce leukocyte-endothelial interactions in muscle and peritoneum, but had no effect systemically (no increase in neutrophils in lungs and no decrease in circulating neutrophil counts). These results demonstrate that: 1) LPS has potent, but divergent local and systemic effects on leukocyte-endothelial interactions; 2) S. aureus can induce a systemic response http://www.jimmunol.org/ similar to LPS, but this response is unlikely to be due to LTA, but more likely to be mediated in part by PepG. The Journal of Immunology, 2002, 168: 4650–4658. key feature of inflammation is the sequestration of leu- tol-linked protein, and an associate signal transducer Toll-like re- kocytes from the circulation to the endothelium, result- ceptor 4 (TLR4)3 (10, 11). Therefore, TLR4 is a critical receptor A ing in leukocyte emigration into the surrounding tissue. involved in the LPS detection system (12) that confers responsive- Leukocyte recruitment occurs in a sequential multistep fashion (1, ness to circulating and tissue leukocytes as well as endothelium ␣ 2). Endothelium activated, for example, with LPS or TNF- ex- (13). By contrast, lipoteichoic acid (LTA), the Gram-positive cell by guest on September 25, 2021 presses the adhesion molecules that mediate tethering, rolling, and membrane equivalent to LPS, does not appear to activate TLR4, adhesion. Therefore, a localized response to LPS or infection will but rather functions through a second TLR, namely TLR2, to ac- induce brisk recruitment of leukocytes without undue damage to tivate immune responses. Nevertheless, in macrophages or cell line the surrounding tissue or organs. In contrast, an inappropriate in- equivalents, the in vitro work has suggested very similar mecha- flammatory response such as systemic sepsis will cause leukocytes nisms of action for the two lipoproteins. Both LPS and LTA act by to localize to the lung, where they become physically trapped and binding a TLR (14–18), activating various tyrosine kinases, and are not able to recirculate (3–6). Indeed, a key feature in human translocating the transcription factor NF-␬B (19), resulting in the septic shock from Gram-negative or Gram-positive bacteria is in- production and release of numerous proinflammatory mediators, appropriate leukocyte recruitment predominantly in lung with a including TNF-␣, IL-6, IL-1␤, IL-12, and NO (20–24). However, tendency for impaired lung function (7). two very recent in vitro studies reported some significant differ- Gram-negative septic shock is believed to result from the effects ences in mediator release in response to TLR2 vs TLR4 activation of LPS (8, 9). Recent evidence has established a model for LPS (25, 26). Although in vivo studies have suggested that both LPS recognition that involves both CD14, a glycosylphosphatidylinosi- and LTA can induce the same end result, namely shock (8, 27, 28), at least for leukocyte-endothelial cell interactions LPS and LTA may elicit very different responses. For example, TLR4, the re- Immunology Research Group, *Departments of Microbiology and Infectious Disease, †Physiology and Biophysics, and ‡Biochemistry and Molecular Biology, Faculty of ceptor for LPS, was abundant on endothelium, whereas TLR2, the Medicine, University of Calgary, Alberta, Canada; and §Biochemical Pharmacology, receptor for LTA, could not be detected (13). Since the endothe- University of Konstanz, Konstanz, Germany lium affects leukocyte trafficking by expressing adhesion mole- Received for publication October 22, 2001. Accepted for publication February 26, 2002. cules in lungs as well as peripheral microvasculature, LPS vs LTA responses may be quite different. 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 We have investigated leukocyte recruitment in response to local with 18 U.S.C. Section 1734 solely to indicate this fact. and systemic LPS or LTA by directly visualizing leukocyte be- 1 This work was supported by a group grant from the Canadian Institutes of Health havior in vivo, further characterizing the direct effects of each Research and the Alberta Heritage Foundation for Medical Research (AHFMR). P.K. and S.M.R. are Canada Research chairs and P.K. is an AHFMR scientist. M.H. and S.M.R. are AHFMR senior scholars. G.A. is an AHFMR postdoctoral fellow. C.J.H. and B.G.Y. are supported by AHFMR studentships. 2 Address correspondence and reprint requests to Dr. Paul Kubes, Health Sciences 3 Abbreviations used in this paper: TLR, Toll-like receptor; HDMEC, human dermal Center, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 4N1. E-mail ad- microvascular endothelial cell; LTA, lipoteichoic acid; MAPK, mitogen-activated dress: [email protected] protein kinase; MPO, myeloperoxidase; PepG, peptidoglycan. Copyright © 2002 by The American Association of Immunologists 0022-1767/02/$02.00 The Journal of Immunology 4651 lipoprotein on various microvascular beds. Our findings demon- phil) infiltration into the lung (3, 30). The samples were stored at Ϫ20°C strate that LTA and LPS induce profoundly different responses in for no more than 1 wk before the MPO assay was performed. MPO activity terms of leukocyte recruitment. Whereas LPS elicited profound was determined using an assay described previously (31), but with the volumes of each reagent modified for use in 96-well microtiter plates. leukocyte recruitment, LTA had no noticeable effects in vivo or in Change in absorbance at 450 nm over a 90-s period was determined using a human endothelial-leukocyte assay in vitro. Our results provide a kinetic microplate reader (Molecular Devices, Sunnyvale, CA). direct evidence that the in vitro macrophage activity of LTA is not predictive of its physiological effects upon leukocyte-endothelial Circulating and peritoneal neutrophil counts cell interactions. At the end of each experiment, whole blood was collected via cardiac puncture. Total leukocyte counts were performed, using a Bright-line he- Materials and Methods mocytometer (Hausser Scientific, Horsham, PA). Mice were sacrificed, and Reagents the peritoneal cavity was washed with 10 ml HBSS. The cells were sedi- mented by centrifugation at 260 ϫ g for 5 min. The pellet was resuspended All reagents for tissue culture, unless specified, were purchased from Life in DMEM containing 5% FCS. The total number of cells in the lavage fluid Technologies (Gaithersburg, MD). LTA from Staphylococcus aureus (Sig- was counted using a hemocytometer. ma-Aldrich, Oakville, Ontario, Canada) was
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