The p38δ PKD signaling pathway regulates neutrophil migration and neutrophil-mediated inflammation
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- Walter Hofmann
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1 DISS. ETH NO._19236 The p38δ PKD signaling pathway regulates neutrophil migration and neutrophil-mediated inflammation A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH For the degree of Doctor of Sciences presented by Arne Ittner Diplom-Biologe, ETH Zurich, Zurich, Switzerland born 03.Jan.1980 citizen of Germany accepted on the recommendation of Prof. Romeo Ricci, supervisor Prof. Wilhelm Krek, co-supervisor
2 Dissertationsschrift A.Ittner 9 3. Summary (in English) Inflammation is a physiologic response to trauma and infection and initiates host defense and efficient reparative processes. Early during inflammation, leukocytes are recruited from the blood circulation to the site of infection or trauma. Amongst the first white blood cells to arrive are neutrophils, which contribute to host defense using their antimicrobial arsenal, but thus can also inflict collateral damage to surrounding tissues. Inflammatory acute lung injury (ALI) that frequently culminates in the life-threatening acute respiratory distress syndrome (ARDS) has been linked to uncontrolled neutrophil invasion and activity. However, the mechanisms that control recruitment of neutrophils during ALI and ARDS remain unclear. Recruitment of neutrophils is regulated by complex signaling events. Key components in these signaling networks are phosphorylation events mediated by kinases. p38 mitogenactivated protein (MAP) kinases are central regulators of myeloid cell responses to inflammatory stimuli. Although the p38 MAP kinase family member p38δ shows distinct expression in neutrophils, a specific role for this kinase in neutrophils is unknown. Therefore, the goal of my project was to elucidate the role of p38δ in neutrophil function in vivo and in vitro and to define its molecular mechanisms of action in this cell type. The results presented here demonstrate that the p38 MAP kinase p38δ and its target Protein Kinase D1 (PKD1) conversely regulate neutrophil recruitment through a cellautonomous mechanism that determines severity of acute lung injury. Global and myeloid-restricted deletion of MAP kinase p38δ attenuates neutrophil recruitment to inflamed lungs resulting in markedly reduced ALI in mice. Intravital microscopy reveals that neutrophils in p38δ null mice show apparent defects in extravasation. In contrast,
3 Dissertationsschrift A.Ittner 10 myeloid-restricted deletion of PKD1, that is phosphorylated and negatively regulated by p38δ, enhances neutrophil recruitment and exacerbates ALI in both presence and absence of p38δ. Moreover, neutrophils lacking p38δ or PKD1 show obverse effects in migration along a chemoattractant gradient in vitro. Conclusively, the data identify a fundamental interplay of p38δ and PKD1 in neutrophils that modulates inflammation and in particular pathogenesis of ALI.
4 Dissertationsschrift A.Ittner Summary (in German) Entzündung ist eine physiologische Antwort auf Verletzung und Infektion und leitet Immunabwehr und effiziente reparative Prozesse ein. Frühzeitig während der Entzündung werden Leukozyten aus der Blutbahn an die Stelle der Veletzung oder Infektion rekrutiert. Unter den ersten weissen Blutzellen, die dort ankommen, sind Neutrophile. Diese tragen zur Immunabwehr bei mittels ihres antimikrobiellen Arsenals, aber können damit auch das umliegende Gewebe schädigen. Die entzündliche Akute Lungenentzündung (ALI), welche häufig im lebensbedrohenden Akuten Respiratorischen Distress Syndrom (ARDS) kulminiert, hängt mit unkontrollierter Neutrophil- Rekrutierung zusammen. Die Mechanismen, die die Neutrophil-Rekrutierung während ALI und ARDS kontrollieren, sind jedoch unklar. Neutrophil-Rekrutierung wird durch komplexe Signal-Ereignisse reguliert. Schlüsselkomponenten sind hierbei Phosphorylierungen durch Kinasen. Die p38 mitogen-aktivierten protein (MAP) kinasen sind zentrale Regulatoren von myeloiden Zellantworten auf Entzündungs-Stimuli. The p38 MAP kinase family member p38δ shows distinct expression in neutrophils. Obwohl die p38 MAP kinase p38δ eine individuelle Expression in Neutrophilen zeigt, ist eine spezifische Rolle dieser Kinase in Neutrophilen nicht bekannt. Deshalb war das Ziel meines Projektes eine Rolle für p38δ in Neutrophil-Funktionen in vivo und in vitro aufzuzeigen und die molekularen Mechanismen von p38δ in diesem Zelltyp zu definieren Die hier vorgestellten Resultate zeigen auf, dass p38δ und sein Target Protein Kinase D1 (PKD1) die Neutrophil-Rekrutierung gegensätzliche regulieren durch einen Zell- Autonomen Mechanismus, welcher die Schwere der akuten Lungenentzündung bestimmt. Global and myeloid-restricted deletion of MAP kinase p38δ attenuates neutrophil recruitment to inflamed lungs resulting in markedly reduced ALI in mice. Globale und
5 Dissertationsschrift A.Ittner 12 myeloid-restringierte Deletion von MAP kinase p38δ attenuiert die Neutrophil- Rekrutierung in Lungen, was zu markant reduzierter ALI in Mäusen führt. Intravital- Mikroskopie zeigt, dass Neutrophile in p38δ-knockout Mäusen apparente Defekte in der Extravasation haben. Im Gegensatz, führt myeloid-restringierte Deletion von PKD1, das von p38δ phosphoryliert und inhibiert wird, zu erhöhter Neutrophil-Rekrutierung und erschwerter ALI sowohl in Gegenwart wie unter Deletion von p38δ. Zudem zeigen Neutrophile ohne p38δ oder PKD1 gegensätzliche Effekte in der Migration entlang Chemoattraktans-Gradienten in vitro. Zusammenfassend zeigen die Daten ein fundamentals Zusammenspiel von p38δ und PKD1 in Neutrophilen auf, das die Entzündung und besonders die Pathogenese von ALI moduliert.
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