Toll-like receptors: Studies on cellular activation and involvement in rheumatoid arthritis
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- Erika Lehmann
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1 DISS. ETH NO Toll-like receptors: Studies on cellular activation and involvement in rheumatoid arthritis A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of'doctor ofnatural Seiences presented by Reinhart Seibl Dip\. Biology, University ofzürich born November 2, 1968 Austrian citizen accepted on the recommendation of Prof. Dr. Jeffrey A. Hubbell, examiner Prof. Dr. Steffen Gay, co-examiner Dr. med. Roger P. Lauener, co-examiner Dr. Heike Hall-Bozic, co-examiner Zürich, 2003
2 Summary In the past years, the innate immune system has been researched with increasing interest. Receptors such as members of the family oftoll-like receptors (TLRs) recognize conserved molecules ofmicroorganisms and trigger the induction of many cellular activation pathways. The activation of an innate immune response results in the first response to invading pathogens, Furthermore, the innate immune system is also essential for the induction of the adaptive immune system. More recently, it has been found that TLRs recognize not only foreign but alsohost-derived molecules. Rheumatoid arthritis (RA) is considered to be an auto immune disease, but so far, no ultimate cause could be identified, In this thesis, a potential involvement oftoll-like receptors in the pathogenesis ofrheumatoid arthritis was investigated. Additionally, more basic issues ofearly cellular responses in the innate immune system after the stimulation with ligands of TLRs were studied. In the first part, cellular activation upon ligand recognition by TLR2 was investigated. An increased production of the antimicrobial peptide ß-defensin 2 upon TLR2-mediated cell activation could be demonstrated. This innate immune response was reinforced by CDI4- and MHC dass Il-molecules. In the second part, the role oftlrs in rheumatoid arthritis was assessed. In vitro studies revealed an upregulation oftlr2 mrna expression in synovial fibroblasts under conditions present in rheumatoid synovium, where increased levels of cytokines such as interleukin-iß, or tumor necrosis factor-u are found. Moreover, known ligands oftlrs increased the expression of TLR2 mrna in these cells. Sections of synovial tissue were analyzed for the appearance of TLR2 mrna and showed enhanced localization oftlr2 in the rheumatoid synovium, particularly at sites of synovial invasion into cartilage or bone. Subsequent experirnents supported these findings by demonstrating that Ra-typical features, such as activation of nuclear factor kappa B (NF-KB), as weil as the expression of proinflammatory cytokines, matrix-metalloproteinases, and chemokines were upregulated in RA synovial fibroblasts upon exposure toligands oftlr2. III
3 IV
4 Zusammenfassung In den vergangenen Jahren nahm das Interesse an der Erforschung des angeborenen Immunsystems (innate immune system) stark zu. Rezeptoren aus der Familie der Toll-like Rezeptoren (TLRs) erkennen konservierte Moleküle von Mikroorganismen und aktivieren dabei eine breite Palette von Zellaktivierungsmechanismen. Die Aktivierung des angeborenen Immunsystems ist die erste Antwort auf eindringende Pathogene. Ausserdem spielt das angeborene Immunsystem eine wichtige Rolle bei der Aktivierung des erworbenen Immunsystems (adaptive immune system). Kürzlich wurde festgestellt, dass TLRs neben fremden auch wirtseigene Moleküle erkennen können. Rheumatoide Arthritis (RA) gilt als Autoimmunkrankheit, wobei die auslösenden Ursachen noch nicht identifiziert werden konnten. In dieser Arbeit steht der mögliche Einfluss von Toll-like Rezeptoren in der Pathogenese der rheumatoiden Arthritis im Mittelpunkt. Ausserdem wurden auch grundlegendere Aspekte der frühen zellulären Reaktionen des angeborenen Immunsystem durch die Bindung der Toll-Iike Rezeptoren an ihre Liganden untersucht. Im ersten Teil dieser Arbeit wurden Zellaktivierungsmechanismen, die durch die Bindung von Tolllike Rezeptor 2 (TLR2) an seine Liganden ausgelöst werden, untersucht. Dabei konnte gezeigt werden, dass die Produktion des antimikrobiellen Peptids ß-Defensin 2 durch TLR2-vermittelte Zellaktivierung gesteigert wird. Diese Aktivierung des angeborenen Immunsystems wurde durch CDI4- und MHC Klasse-Il-Moleküle verstärkt. Im zweiten Teil dieser Arbeit wurde die Rolle von Toll-like Rezeptoren in der rheumatoiden Arthritis untersucht. Durch in vitro Studien konnte gezeigt werden, dass die Boten-RNA (mrna) für TLR2 in synovialen Fibroblasten unter Bedingungen, wie sie in rheumatoiden Gelenken angetroffen werden, zum Beispiel bei hohen Konzentrationen der Zytokine Interleukin-Iß (IL-Iß) oder Tumor-necrosis Faktor a (TNF-a), in erhöhtem Masse exprimiert wird. Auch durch Liganden von Toll-like Rezeptoren wurde die Produktion von TLR2 mrna induziert. Histologische Schnitte von rheumatoidem Synovialgewebe zeigten eine erhöhte Expression von TLR2 mrna, insbesondere an Orten synovialer Invasion v
5 In den Knorpel oder Knochen. Weitere Untersuchungen bestätigten diese Beobachtungen, indem gezeigt werden konnte, dass die Zugabe von Liganden für den TLR2 in isolierten synovialen Fibroblasten zu einer Aktivierung des Transkriptionsfaktors Nuc1ear Factor kappa B (NF-KB), aber auch zu einer erhöhten Produktion von entzündungsfördernden Zytokinen, Matrix-Metalloproteinasen und Chemokinen führte. Für weiterführende Studien über den Einfluss des TLR2 in RA wurde ein lösliches rekombinantes Fusionsprotein in einem Baculovirus-Expressionssystem hergestellt, das aus der extrazellulären Domäne von TLR2 und der coiled-coil Domäne des murinen Matrilins-l besteht (TLR2-matrilin). Mit Festphasen-Bindungsstudien konnte gezeigt werden, dass dieses Protein in der Lage ist, Liganden des TLR2 zu binden. Zudem konnte nachgewiesen werden, dass Tl.Rz-matrilin in vitro eine durch TLR2 vermittelte Zellaktivierung, im Gegensatz zu einer Aktivierung über TLR4 durch Lipopolysaccharide, fast vollständig inhibiert wurde. Damit stellt dieses Fusionsprotein ein wichtiges Instrument für die Untersuchung der Rolle von TLR2 in vivo, wie beispielsweise bei der rheumatoiden Arthritis, und für die Identifizierung weiterer möglicher Liganden von TLR2 in vitro dar. VI
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