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Fimbriae Porphyromonas Gingivalis TLR2 Transmodulates Monocyte Adhesion and Transmigration via Rac1- and PI3K-Mediated Inside-Out Signaling in Response to Porphyromonas gingivalis This information is current as Fimbriae of September 25, 2021. Evlambia Harokopakis, Mohamad H. Albzreh, Michael H. Martin and George Hajishengallis J Immunol 2006; 176:7645-7656; ; doi: 10.4049/jimmunol.176.12.7645 Downloaded from http://www.jimmunol.org/content/176/12/7645 References This article cites 58 articles, 32 of which you can access for free at: http://www.jimmunol.org/ http://www.jimmunol.org/content/176/12/7645.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists by guest on September 25, 2021 • 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 © 2006 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology TLR2 Transmodulates Monocyte Adhesion and Transmigration via Rac1- and PI3K-Mediated Inside-Out Signaling in Response to Porphyromonas gingivalis Fimbriae Evlambia Harokopakis,* Mohamad H. Albzreh,‡ Michael H. Martin,*† and George Hajishengallis2*† We present evidence for a novel TLR2 function in transmodulating the adhesive activities of human monocytes in response to the fimbriae of Porphyromonas gingivalis, a pathogen implicated in chronic periodontitis and atherosclerosis. Monocyte recruitment into the subendothelium is a crucial step in atherosclerosis, and we investigated the role of P. gingivalis fimbriae in stimulating monocyte adhesion to endothelial cells and transendothelial migration. Fimbriae induced CD11b/CD18-dependent adhesion of human monocytes or mouse macrophages to endothelial receptor ICAM-1; these activities were inhibited by TLR2 blockade or Downloaded from deficiency or by pharmacological inhibitors of PI3K. Moreover, this inducible adhesive activity was sensitive to the action of Clostridium difficile toxin B, but was not affected by Clostridium botulinum C3 exoenzyme, pertussis toxin, or cholera toxin. Accordingly, we subsequently showed through the use of dominant negative signaling mutants of small GTPases, that Rac1 mediates the ability of fimbria-stimulated monocytes to bind ICAM-1. A dominant negative mutant of Rac1 also inhibited the lipid kinase activity of PI3K suggesting that Rac1 acts upstream of PI3K in this proadhesive pathway. Furthermore, fimbriae stimulated monocyte adhesion to HUVEC and transmigration across HUVEC monolayers; both activities required TLR2 and Rac1 signaling http://www.jimmunol.org/ and were dependent upon ICAM-1 and the high-affinity state of CD11b/CD18. P. gingivalis-stimulated monocytes displayed enhanced transendothelial migration compared with monocytes stimulated with nonfimbriated isogenic mutants. Thus, P. gingi- valis fimbriae activate a novel proadhesive pathway in human monocytes, involving TLR2, Rac1, PI3K, and CD11b/CD18, which may constitute a mechanistic basis linking P. gingivalis to inflammatory atherosclerotic processes. The Journal of Immunology, 2006, 176: 7645–7656. ␤ he 2 integrin heterodimer CD11b/CD18 (Mac-1, CR3) is (1, 10). Inside-out signaling pathways for CD11b/CD18 activation a multifunctional receptor with significant and diverse can be induced upon stimulation of other surface receptors, such as by guest on September 25, 2021 T roles in immunity and inflammation (1, 2). The functional chemotactic receptors (1, 10) or TLRs (11, 12). versatility of this integrin is attributed, at least partly, to its ability The potential of CD11b/CD18 for vascular cell interactions by to recognize multiple and structurally unrelated molecules, includ- binding to ICAM-1 or to endothelial-associated matrix proteins, ing its endothelial counter-receptor ICAM-1, fibrinogen, iC3b, such as fibrinogen, may contribute to cardiovascular inflammation Factor X, and platelet glycoprotein Ib␣ (3–6). Abundantly ex- (5, 13). In this context, the adhesion of bloodborne leukocytes to pressed by neutrophils and monocytes, CD11b/CD18 plays a role the arterial endothelium, followed by their migration into the sub- in their migration to sites of extravascular inflammation (3, 7–9). endothelial area is a hallmark of early atherogenesis (14). The The interactions of CD11b/CD18 with fibrinogen and ICAM-1 transmigratory process is mediated by interacting sets of cell ad- mediate adhesion of neutrophils or monocytes to sites of fibrino- hesion molecules, including the CD11b/CD18-ICAM-1 pair, gen deposition and the endothelium, respectively (3, 9). These ad- which has been experimentally implicated in atherosclerosis and hesive interactions are tightly regulated. Although the default con- other inflammatory conditions (13, 15–17). It is thought that in- formation of CD11b/CD18 in resting cells is of low affinity, a rapid fectious agents contribute to vascular inflammation and certain and transient shift to a high-affinity binding state (referred to as bacterial pathogens such as Chlamydia pneumoniae, Helicobacter CD11b/CD18 activation) can be triggered by inside-out signaling pylori, and Porphyromonas gingivalis have been implicated as ac- cessory factors in the development or acceleration of atheroscle- rosis (14, 18, 19). In this regard, infection-driven chronic inflam- † *Center for Oral Health and Systemic Disease, Department of Periodontics/End- matory diseases, including periodontitis, are associated with odondics and Department of Microbiology/Immunology, University of Louisville Health Sciences Center, Louisville, KY 40292; and ‡Center of Excellence in Oral and increased risk for cardiovascular disease (20–22). Craniofacial Biology, Louisiana State University Health Sciences Center, New Or- P. gingivalis is a Gram-negative oral bacterium that is strongly leans, LA 70119 associated with chronic periodontitis (23). This pathogen may dis- Received for publication January 26, 2006. Accepted for publication April 6, 2006. seminate from periodontal lesions into the systemic circulation and 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 P. gingivalis-specific DNA has been detected in human athero- with 18 U.S.C. Section 1734 solely to indicate this fact. sclerotic plaques (24). Studies in animal models of periodontitis or 1 This work was supported by U.S. Public Health Service Grant DE015254 from the atherosclerosis have established the P. gingivalis fimbriae (fila- National Institutes of Health. mentous appendages on the cell surface) as a major virulence fac- 2 Address correspondence and reprint requests to Dr. George Hajishengallis, Center tor of this pathogen (25, 26). Although both wild-type P. gingivalis for Oral Health and Systemic Disease, University of Louisville Health Sciences Cen- ter, 501 South Preston Street, Room 206, Louisville, KY 40292. E-mail address: and an isogenic non-fimbriated mutant are detected in the blood [email protected] and aortic arch tissue of orally infected hyperlipidemic mice, only Copyright © 2006 by The American Association of Immunologists, Inc. 0022-1767/06/$02.00 7646 TRANSENDOTHELIAL MIGRATION DEPENDENCE ON TLR2, Rac1, PI3K the presence of wild-type P. gingivalis is associated with periodon- mosphere in PromoCell Endothelial Cell Growth medium (2% FCS, 0.1 tal disease and increased atherosclerotic plaque formation (26). ng/ml epidermal growth factor, 1.0 ng/ml basic fibroblast growth factor, ␮ In this study, we have identified a plausible inflammatory mech- 1.0 g/ml hydrocortisone, 0.4% endothelial cell growth supplement/hep- arin, 50 ␮g/ml gentamicin, 50 ng/ml amphotericin B), according to the anism whereby P. gingivalis fimbriae may contribute to the ath- supplier’s recommendations. Thioglycolate-elicited macrophages were iso- erosclerotic process. Based on earlier findings that P. gingivalis lated from the peritoneal cavity of mice deficient in CD14, TLR2, TLR4, fimbriae bind CD14 and stimulate TLR2/PI3K-mediated inside- both TLR2 and TLR4, or from wild-type control mice, as previously de- out signaling for CD11b/CD18 activation (11, 27), we now show scribed (27, 32). The mice deficient in CD14, TLR2, or TLR4 were of C57BL/6 genetic background, whereas mice harboring homozygous TLR2 that activation of this pathway leads to increased monocyte adhe- and TLR4 mutations were 9-fold backcrossed toward the C3H genetic sion to fibrinogen, ICAM-1, and endothelial cells. This inducible background (kindly donated by Dr. C. Kirschning, Technical University of proadhesive pathway is distinct from other CD11b/CD18 activa- Munich, Munich, Germany). Mouse macrophages were cultured in com- tion pathways stimulated by FMLP or PMA, as shown by differ- plete RPMI as described. The use of animals was reviewed and approved ential toxin sensitivity. On the basis of toxin sensitivity data and by the Institutional Animal Care and Use Committee. Human or mouse cell 3 viability was monitored using
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