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TLR-2 Antigen Presentation Pathways Through Regulates CD1 Mycobacterium Tuberculosis

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TLR-2 Antigen Presentation Pathways Through Regulates CD1 Mycobacterium Tuberculosis Mycobacterium tuberculosis Regulates CD1 Antigen Presentation Pathways through TLR-2 This information is current as Carme Roura-Mir, Lisheng Wang, Tan-Yun Cheng, Isamu of October 2, 2021. Matsunaga, Christopher C. Dascher, Stanford L. Peng, Matthew J. Fenton, Carsten Kirschning and D. Branch Moody J Immunol 2005; 175:1758-1766; ; doi: 10.4049/jimmunol.175.3.1758 http://www.jimmunol.org/content/175/3/1758 Downloaded from References This article cites 64 articles, 32 of which you can access for free at: http://www.jimmunol.org/content/175/3/1758.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 October 2, 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 © 2005 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Mycobacterium tuberculosis Regulates CD1 Antigen Presentation Pathways through TLR-21 Carme Roura-Mir,2* Lisheng Wang,2,3* Tan-Yun Cheng,* Isamu Matsunaga,* Christopher C. Dascher,* Stanford L. Peng,4* Matthew J. Fenton,5† Carsten Kirschning,‡ and D. Branch Moody6* Mycobacterium tuberculosis remains a major pathogen of worldwide importance, which releases lipid Ags that are presented to human T cells during the course of tuberculosis infections. Here we report that cellular infection with live M. tuberculosis or exposure to mycobacterial cell wall products converted CD1؊ myeloid precursors into competent APCs that expressed group 1 CD1 proteins (CD1a, CD1b, and CD1c). The appearance of group 1 CD1 proteins at the surface of infected or activated cells occurred via transcriptional regulation, and new CD1 protein synthesis and was accompanied by down-regulation of CD1d transcripts and protein. Isolation of CD1-inducing factors from M. tuberculosis using normal phase chromatography, as well as Downloaded from the use of purified natural and synthetic compounds, showed that this process involved polar lipids that signaled through TLR-2, and we found that TLR-2 was necessary for the up-regulation of CD1 protein expression. Thus, mycobacterial cell wall lipids provide two distinct signals for the activation of lipid-reactive T cells: lipid Ags that activate T cell receptors and lipid adjuvants that activate APCs through TLR-2. These dual activation signals may represent a system for selectively promoting the presen- tation of exogenous foreign lipids by those myeloid APCs, which come into direct contact with pathogens. The Journal of Immunology, 2005, 175: 1758–1766. http://www.jimmunol.org/ he discovery of CD1 Ag presentation pathways provides phosphatidylinositols, sulfatides, and isoglobosides activate CD1- a new perspective on microbial immunity by showing restricted T cells (12–16). Thus, mammalian APCs normally en- T how T cells can recognize lipid Ags from pathogens. CD1 counter and present both foreign and self lipid Ags to T cells, proteins present a variety of pathogen-derived lipids to T cells in raising basic questions about how such responses are regulated. vitro (1–6), and T cells reactive to mycobacterial lipid Ags have A role for CD1-expressing APCs in controlling differential T been isolated from the bloodstream of tuberculosis patients, pro- cell responses to self and foreign Ags has been suggested by stud- viding evidence that CD1 and lipid-reactive T cells normally func- ies showing that dendritic cells (DCs)7 and B cells have highly tion in the host response during infections with Mycobacterium regulated subcellular pathways for internalizing exogenous lipid by guest on October 2, 2021 tuberculosis (7–9). However, CD1-mediated T cell responses are Ags into endosomal compartments for loading onto CD1 proteins. not limited only to foreign pathogens, as endogenous mammalian For example, myeloid dendritic cells use the mannose receptor phosphatidylinositols normally bind to cellular CD1 proteins as (CD206) and Langerhans cells use langerin (CD207) to deliver they traverse the secretory pathway (10, 11), and self gangliosides, exogenous lipid Ags to endosomes (17, 18), where saposin lipid- transfer proteins and a low pH environment promote binding of lipid Ags to CD1 proteins (19–22). Such endosomal loading path- *Division of Rheumatology, Immunology and Allergy, Brigham and Women’s Hos- pital and Harvard Medical School, Boston, MA 02115; †The Pulmonary Center, Bos- ways are necessary for efficient T cell activation by most or all ton University School of Medicine, Boston, MA 02118; and ‡Institute of Medical known bacterial lipid Ags, including mycolic acid, lipoarabino- Microbiology, Immunology and Hygiene, Technical University of Munich, Munich, Germany mannan (LAM), glucose monomycolate (GMM), mannosyl phos- phomycoketides, and didehydroxymycobactins (DDM) (1, 4, 23– Received for publication April 6, 2005. Accepted for publication May 16, 2005. 25). A general implication of the discovery of endosomal pathways 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 for loading lipid Ags onto CD1 proteins is that APCs can actively with 18 U.S.C. Section 1734 solely to indicate this fact. control which Ags are displayed to T cells by controlling which 1 This work was supported by grants from the Cancer Research Institute, the Amer- lipids are taken up into endosomal compartments (26). ican College of Rheumatology Research and Education Foundation, the Pew Scholars Related to this, there is evidence that myeloid DCs, which are Program in the Biomedical Sciences, the Mizutani Foundation for Glycoscience, and the National Institutes of Health (Grants AR48632 and AI49313). the only peripheral APCs that are known to be capable of express- 2 C.R.-M. and L.W. contributed equally to this study. ing all human CD1 isoforms (CD1a, CD1b, CD1c, CD1d, CD1e), selectively express CD1 proteins and initiate lipid Ag processing 3 Current address: Stem Cell Biology and Regenerative Medicine, Robarts Research Institute, University of Western Ontario, 100 Perth Drive, London, Ontario, Canada pathways in response to certain activating stimuli. For example, N6A 5K8. group 1 CD1 isoforms (CD1a, CD1b, CD1c) are not detectably 4 Current address: Washington University School of Medicine, Campus Box 8045, expressed on the surface of blood-derived monocytes, but these CSRB 6617, 660 South Euclid Avenue, St. Louis, MO 63110. three CD1 proteins can be induced in vitro by high concentrations 5 Current address: Division of Pulmonary and Critical Care Medicine, University of Maryland School of Medicine, 685 West Baltimore Street, MSTF-800, Baltimore, MD 21201. 7 Abbreviations used in this paper: DC, dendritic cell; LAM, lipoarabinomannan; 6 Address correspondence and reprint requests to Dr. D. Branch Moody, Division of GMM, glucose monomycolate; DDM, didehydroxymycobactins; RT-PCR, real-time Rheumatology, Immunology and Allergy, Brigham and Women’s Hospital and Har- PCR; CHO, Chinese hamster ovary; M. tb-GFP, M. tuberculosis expressing GFP; vard Medical School, Smith Building Room 514, 1 Jimmy Fund Way, Boston, MA CWS, cell wall skeleton; PIM, phosphatidylinositol mannoside; araLAM, LAM with 02115. E-mail address: [email protected] arabinosylated termini. Copyright © 2005 by The American Association of Immunologists, Inc. 0022-1767/05/$02.00 The Journal of Immunology 1759 of the cytokines that promote the early phases of differentiation to mix reagent kit in the ABI PRISM 7700 System (Applied Biosystems). DCs, GM-CSF, and IL-4 (1, 27). Related to this, studies of MHC CD1 mRNA levels were determined by the comparative Ct method relative class II-mediated Ag processing have shown that the transition of to the expression of the housekeeping gene GAPDH. Primers are: CD1a (5Ј-TGTTAGCTGTTCTCCCAGGTGA-3Ј forward, 5Ј-AGGATGC- myeloid precursors into immature DCs in response to GM-CSF GATCCAGATGACAT-3Ј reverse), CD1b (5Ј-CCATTTCAACTGT- and IL-4 is associated with increasing rates of macropinocytosis TAGCTGTTCTCTT-3Ј forward, 5Ј-GAAAGGAGGTCGGCCCC-3Ј re- and related mechanisms of bulk flow Ag uptake (28). This raises verse), CD1c (5Ј-TGGTGACAATGCAGACGCA-3Ј forward, 5Ј-GGTTG the possibility that monocytes in the peripheral blood generally ACAAATGAGAAGATCTGGA-3Ј reverse), and CD1d (5Ј-AGCGCTG AAGTCCCGCA-3Ј forward, 5Ј-TATTGGCGAAGGACGAGATCTG-3Ј lack the ability to present lipids on group 1 CD1 proteins, until reverse). The fluorogenic probes are: CD1a (5Ј-FAM-AGACGGGCTCA they traffic to local sites of inflammation or infection, where as yet AGGAGCCTCTCTCCTTAMRA-3Ј), CD1b 5Ј-FAM-CCTGGTGGTAA undefined stimuli lead to CD1 expression. CAGTGAACATGCCTTCC-TAMRA-3Ј), CD1c (5Ј-FAM-CCCAGGAA In these studies, we considered the possibility that microbial CACGTCTCCTTCCATGTCTAMRA-3Ј), and CD1d (5Ј-FAM-AGGCTT Ј pathogens might modulate CD1 expression and Ag-presenting TTCCCCCTCCGCTGCCTAMRA-3
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