Establishment of a CCL19/CCL21 dual transgenic system for investigating the functions of T cell zone stromal cells
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1 Research Collection Doctoral Thesis Establishment of a CCL19/CCL21 dual transgenic system for investigating the functions of T cell zone stromal cells Author(s): Chai, Qian Publication Date: 2013 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETH No ESTABLISHMENT OF A CCL19 /CCL21 DUAL TRANSGENIC SYSTEM FOR INVESTIGATING THE FUNCTIONS OF T CELL ZONE STROMAL CELLS A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by QIAN CHAI MSc, Uppsala University born on February 14 th, 1984 citizen of P. R. China accepted on the recommendation of Prof. Dr. Salomé Regine Leibundgut-Landmann Prof. Dr. Burkhard Ludewig PD Dr. Volker Thiel 2013
3 Summary SUMMARY Summary In order to achieve the function of protecting the body, efficient interactions between cellular compartments in secondary lymphoid organs (SLOs) are needed to trap antigens and control immune responses. Mesenchymal stromal cells in SLOs play essential roles in the development of lymphoid tissues and the maintenance of the structures. Moreover, research in the recent decades demonstrated the importance of mesenchymal stromal cells for regulation of lymphocyte migration and function. Fibroblast reticular cells (FRCs) are the mesenchymal stromal cells of the T cell zone that build up the conduit system to direct interstitial fluids and regulate T cell migration and survival via producing C-C motif chemokine 19 (CCL19), CCL21, and Interleukin-7 (IL7), respectively. However, little is known about the molecular and functional mechanisms of FRCs during lymphoid tissue development and in the regulation of immune responses. The major aim of this PhD thesis was therefore to generate a novel stromal cell specific transgenic mouse model in order to track stromal cells in vivo and to investigate the functions of mesenchymal stromal cells on immunological and developmental processes in more detail via conditional gene manipulation and transgene tracking in situ. We have generated a bacterial artificial chromosome (BAC)-trangenic mouse model in which the Cre-recombinase is driven by the Ccl19 promoter to target in FRCs. Ccl19- cre transgenic mice have been obtained and crossed to Rosa26-eyfp (R26-eyfp) mice for transgene expression analysis which revealed that the transgene expression in lymph nodes (LNs) was almost exclusively confined to podoplanin (PDPN) + CD31 - FRCs. Likewise, transgene activity in Peyer s patches (PPs) was largely restricted to FRC-like cells. In spleen around 12% of the transgene activity was confined to FRCs. Moreover, Ccl19-cre transgene-producing cells showed activity during inflammatory conditions and 1
4 Summary participated in stromal network restoration after lymphocytic choriomeningitis virus (LCMV) infection. To further understand the role of mesenchymal stromal cells in SLO development and FRC diversification during development, we have assessed the impact of lymphotoxinbeta receptor (LTβR) signaling on Ccl19-cre + cells. Conditional ablation of LTβR resulted in profound changes in the development and organization of SLOs. The structure of spleen was altered and the number of PPs was significantly reduced. However, LTβR blockade in Ccl19-expressing mesenchymal cells did not abrogate LN development but impacted on the maturation of FRCs from myofibroblastic precursors. Moreover, although myofibroblasic FRC precursors were able to generate the T cell zone structure and to maintain the function of the conduit system, LTβR-dependent maturation of FRCs is important to maintain immunocompetence. Taken together, this study has generated and characterized the mesenchymal stromal cell specific mouse model Ccl19-cre. Moreover, further analysis revealed the importance of LN FRCs for LN development and function. Taken together, the Ccl19-cre mouse is well-suited to dissect the role of mesenchymal stromal cell in lymphoid organogenesis and to address the function of mesenchymal stromal cells in the regulation of immune responses. 2
5 Zusammenfassung ZUSAMMENFASSUNG Zusammenfassung Effiziente Interaktionen zwischen den zellulären Komponenten in sekundären lymphatischen Organen (SLOs) sind notwendig um Antigene einzufangen und Immunantworten zu kontrollieren und somit den Schutz des Körpers zu gewährleisten. Mesenchymale Stromazellen in SLOs spielen eine essentielle Rolle in der Entwicklung von lymphatischem Gewebe und der Aufrechterhaltung dessen Strukturen. Außerdem zeigte die Forschung der letzten Jahrzehnte die Wichtigkeit mesenchymaler Stromazellen die Regulierung der Migration von Lymphozyten und deren Funktion betreffend. Fibroblastische Retikulumzellen (FRCs) sind die mesenchymalen Stromazellen der T-Zell-Zone aus denen das Gefäßsystem zur Leitung interstitieller Flüssigkeiten besteht und die sowohl die T-Zell-Migration als auch das Überleben von T-Zellen durch die Produktion von CCL19, CCL21 und IL7 regulieren. Allerdings ist bisher wenig über die molekularen und funktionalen Mechanismen von FRCs während der Entwicklung lymphatischer Organe und deren Rolle in der Regulierung von Immunantworten bekannt. Das Hauptziel dieser Doktorarbeit war deshalb ein neues stromazellspezifisches transgenes Mausmodell zu erschaffen, welches das Aufspüren von Stromazellen in vivo und die Erforschung der Funktionen mesenchymaler Stromazellen während immunologischer und Entwicklungsprozessen anhand von konditionaler Genmanipulation und Transgenverfolgung in situ näher im Detail erlaubt. Während dieser Doktorarbeit gelang es anhand eines bakteriellen künstlichen Chromosoms (BAC) ein Mausmodell zu erschaffen welches es mithilfe einer durch den Ccl19- Promotor gesteuerten Cre-Rekombinase ermöglicht FRCs aufzuspüren. Ccl19-cre transgene Mäuse wurden erfolgreich kreiert und zur Analyse der Transgenexpression mit R26-eyfp Mäusen gekreuzt. Dies zeigte, dass sich die Expression des Transgens in 3
6 Zusammenfassung Lymphknoten (LNs) fast ausschließlich auf Podoplanin (PDPN) + CD31 - FRCs beschränkte. Gleichzeitig war die Transgenaktivität in Peyer-Plaques (PPs) größtenteils auf FRC-ähnliche Zellen beschränkt. In der Milz machten FRCs ungefähr 12% der Transgenaktivität aus. Zudem zeigten Ccl19-cre transgenproduzierende Zellen während Entzündungen Aktivität und spielten eine Rolle in der Wiederherstellung des Stromanetzwerkes nach Infektionen mit dem lymphozytischen Choriomeningitis-Virus (LCMV). Um die Rolle mesenchymaler Stromazellen in der Entwicklung von SLOs und die Veränderungen von FRCs während der Entwicklung besser zu verstehen, wurden des Weiteren die Auswirkungen der Signalübertragung des Lymphotoxin-β Rezeptors (LTβR) auf Ccl19-cre + Zellen erforscht. Konditionale Ablation von LTβR resultierte in schwerwiegenden Änderungen in der Entwicklung und Organisation von SLOs. Außerdem war eine veränderte Struktur der Milz feststellbar und die Anzahl der PPs war signifikant reduziert. Trotzdem verhinderte eine Blockade von LTβR in Ccl19-exprimierenden mesenchymalen Zellen nicht die Entwicklung von LNs, wenn auch die Reifung von myofibroblastischen Vorgängern zu FRCs beeinflusst war. Zudem zeigte sich, dass die LTβR-abhängige Reifung von FRCs wichtig für die Erhaltung der Immunkompetenz ist, obwohl myofibroblastische FRC-Vorgänger in der Lage waren die T-Zell-Zonenstruktur zu schaffen und die Funktionen des Lymphgefäßsystems aufrecht zu erhalten. Zusammenfassend erzeugte und charakterisierte diese Arbeit das für mesenchymale Stromazellen spezifische Mausmodell Ccl19-cre. Außerdem enthüllten weitere Untersuchungen die Wichtigkeit von FRCs in LNs im Bereich der Entwicklung und Funktion von LNs. Es zeigte sich, dass die Ccl19-cre Maus gut geeignet dafür ist die Rolle mesenchymaler Stromazellen in der Entstehung lymphatischer Organe zu untersuchen und um weitere Erkenntnisse über die Funktion von mesenchymalen Stromazellen in der Regulierung von Immunantworten zu gewinnen. 4
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