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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Immunomodulatory proteins in Heligmosomoides polygyrus excretory/secretory products. Andrea M. Kemter Thesis submitted for the degree of Doctor of Philosophy The University of Edinburgh 2016 Abstract Infections with parasitic helminths are counted as neglected tropical diseases; they infect millions of people worldwide, causing high morbidity and economic loss. Many parasites establish long lasting infections in the host by blocking immune recognition, activation and effector pathways. To allow in depth research on their modes of immune evasion, several mouse models for parasitic helminth infections have been established. Heligmosomoides polygyrus for example is a gastrointestinal nematode of rodents exhibiting a wide spectrum of immunomodulatory effects, mediated in part by soluble molecules released by adult worms in vitro, the excretory/secretory products (HES). HES is a potent inhibitor of dendritic cell (DC) activation by Toll-like receptor (TLR) ligands, completely abolishing LPS induced IL-12 production and reducing the upregulation of cell surface activation markers. As of now, neither the modulatory molecule nor its mechanism of action are known. Here, the effect of HES on TLR ligand induced DC maturation was characterized in considerably more detail compared to previous publications. It could be shown to inhibit DC maturation induced by various TLR ligands, on both protein and mRNA levels. These effects were comparable in both C57BL/6 and BALB/c derived cells; in contrast to this HES differentially affected alternative activation of BMDC from these two mouse strains. Although for most of the experiments GM-CSF differentiated BMDC were used, HES also inhibited LPS induced activation of splenic CD11c+ cells as well as the activation of all three populations described in Flt3-L differentiated BMDC - pDCs, CD11b+ cDCs and CD24+ cDCs. Furthermore, it could be shown here that HES also inhibits LPS induced maturation in human monocyte derived DCs. In the search for the component in HES responsible for its inhibition of TLR ligand induced DC maturation, exosome depleted HES rather than exosomes was inhibitory, and the effect was heat labile. This lead to the conclusion that the modulatory molecule has a protein component which is indispensable for its effect; following this reasoning HES was subjected i to fractionation, with subsequent analysis of the fraction protein contents by mass spectrometry. The top nine candidate proteins were expressed recombinantly; however, the recombinants were not able to inhibit LPS induced DC activation. In parallel, experiments to elucidate the mechanism by which HES inhibits TLR ligand induced DC maturation were performed. This led to the conclusion that HES induces changes in the cells that, while not affecting the induction of signalling downstream of TLRs, do impair its maintenance. As a complement to these experiments, the transcriptomes of LPS and LPS+HES treated cells eight hours after LPS stimulation were compared. This revealed that transcripts encoding a number of transcription factors inducing the expression of activation markers after TLR ligation were reduced upon treatment of cells with HES, as were the transcript levels of IRAK2, a kinase necessary for persistent signalling. In addition, HES increased the transcript levels for several factors known to negatively regulate DC maturation, including ATF3. Furthermore, this analysis revealed changes in transcript levels of factors like HIF-1a, indicating an even greater reliance on aerobic glycolysis if cells were treated with HES, in addition to hints at increased ER and oxidative stress. In conclusion, this work narrows down the list of potential DC modulators in HES, gives a first insight into changes in DC metabolism induced by HES and sheds light on the role of a number of signalling pathways with important roles in DC activation as targets of DC inhibition by HES. ii Lay Summary Parasitic helminths infect millions of people worldwide, and can cause severe symptoms; infections of animals are equally problematic, as they cause great economic loss. These worms have developed a number of ways to avoid the immune response of their hosts, including inhibiting the activation of the cells responsible for recognizing infectious agents and activating specific immune reactions. This effect is mediated by factors the parasites produce and secrete. Finding the specific component in these parasite products and how it affects immune cells was the aim here, as it could be exploited for the development of treatment strategies for a number of different conditions. To find the component in question, methods to identify specific proteins were used, and the most promising candidates produced in the laboratory. These top candidates did not reproduce the effect, but a number of further possibilities are yet to be tested. In addition, by analysing changes within the cells that lead to their activation, insights into how the parasite affects these cells could be gained as well. Finally, these effects could not only be seen in mouse, but also in human cells, showing that this research could indeed be useful for drug development. iii Declaration I declare that this thesis has been composed by myself, describes my own work and that the work has not been submitted towards any other degree. The experiments using exosomes and exosome depleted HES have been carried out in collaboration with Gillian Coakley. Selected figures from reviews published by other researchers have been used where appropriate; the authors and source are indicated in each case. Andrea Kemter May 2016 v Acknowledgements And with this, almost four years in Edinburgh come to an end - and I have to say, I will be sad to leave, it has been a great four(ish) years! Many people have contributed to making sure of that: First of all: Rick - thank you so much for being the best supervisor I could have wished for, helping me to get here in the first place and then giving me loads of freedom to develop my project while always being there with advice and guidance, sending me to great conferences (just saying, Hydra!), and giving me the freedom to pursue my sport too, which took quite a few hours out of my week! And finally, thank you so much for all your help in the last year or so, making sure I could finish my PhD without (too much) panic, and making me actually get a Postdoc position long before I would have even started thinking about it. Then the whole rest of the lab - lab-mama Yvonne, who has saved me countless of times; Danielle and Henry, who’ve worked with me on/helped me with quite a few experiments (and gave me cat-time!); Gillian, for letting me play with exosomes, and my office desk and lab-bench neighbour Xuhang, both of you were great conference mates!; as well as Janice, Kara, James, Katie, Lisa, Stephie, Elaine, Chris and David Dresser - all of you taught me so much, be it methods or discussing science, and have made the lab a great place to work in! Also, thanks to Yvonne and Henry for your help proofreading Material and Methods / the candidate protein chapter! In general, the people in Ashworth Labs, I really enjoyed the very collegial atmosphere; special mention here has to go to a few people who helped me immeasurably, like Martin Waterfall, who helped me out so many times when I ran into FACS trouble; Thomas Tan for teaching me a lot about cell signalling; Al Ivens for help with the array and answering bioinformatics questions Henry and I were clueless about; the Allen and Taylor labs especially, sharing labs and offices - and quite a few times reagents - with us, and especially Sharon for many chats and discussions. Andrew MacDonald for inviting me to Manchester to learn/try out the FLDCs and human moDCs, and his lab, especially Alex Phythian-Adams who organized my visit there and taught me how to make FLDCs - I’ve also learned so many new things about flow cytometry! - and Cecilia Forss and James Crooks for the moDCs. And finally: my friends and family. There’s way too much to write it all, so just: THANK YOU! One thing to mention here though: thank you, Johannes, for giving me your UoE PhD thesis LATEX template, it probably saved me hours (or days?) of trying to get the layout right! Meinen Eltern: ich kann gar nicht beschreiben wie dankbar ich bin, euch zu haben - ihr seid immer für mich da wenn ich Unterstützung oder gutes Zureden brauche, erinnert mich, ab und zu auch mal Pausen einzulegen, und seid überhaupt die besten Eltern die ich mir wünschen könnte! Danke! vii Contents Contents Table of Contents ix List of Figures xiii List of Tables xv 1 Introduction1 1.1 Helminths....................................1 1.1.1 Helminths infecting humans and their animal models.......4 1.1.1.1 Heligmosomoides polygyrus ..................6 1.2 Immune responses to helminths........................9 1.3 Dendritic cells.................................. 14 1.3.1 Signalling pathways in DC activation................ 17 1.3.2 Metabolism............................... 23 1.3.3 Mechanisms to control DC activation...............
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