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Inflammation in Type 2 Diabetes and the Neuroendocrine Role of IL-18

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Inflammation in Type 2 Diabetes and the Neuroendocrine Role of IL-18 Inflammation in type 2 diabetes and the neuroendocrine role of IL-18 Chris Booker A thesis submitted for the degree of PhD at the University of Otago, Dunedin, New Zealand Date: May 2012 Abstract: Cardiovascular disease is one of the leading causes of morbidity and mortality in type 2 diabetes, and yet, recent randomised controlled trials investigating the effect of different regimens of blood glucose control failed to show any benefit of more intensive control on rates of cardiovascular mortality, and minimal benefit on levels of morbidity. This thesis examines the theoretical understanding of type 2 diabetes, including the historical process which led to the above trials being conducted. A review of the historical and modern evidence surrounding the role of chronic inflammation suggests that this may be a common pathogenic alteration in obesity, diabetes and cardiovascular disease which may contribute to the development of cardiovascular disease in persons with type 2 diabetes, and even the pathogenesis of type 2 diabetes itself. This thesis therefore investigates the role of inflammation in type 2 diabetes, by a two-pronged approach: one investigates the effects of a dietary intervention on levels of chronic inflammation in participants with type 2 diabetes in the Lifestyle Over and Above Drugs in Diabetes (LOADD) randomised controlled trial. In this trial, chronic inflammation is assessed by a range of inflammatory markers and adipokines including leptin, neopterin, tumor necrosis factor α and its soluble receptors, the interleukins 1, 6, 10, and 18, and interleukin 1 receptor antagonist. The dietary intervention group exhibited a significant reduction in circulating levels of interleukin-18 (IL-18) and neopterin relative to a 'care as usual' control group; reductions which further analyses suggest were unrelated to concomitant changes in adiposity or glycaemia. In the second branch of the thesis, the neuroendocrine effects of IL-18 are further investigated in rodents, as previous evidence has linked this cytokine with effects on appetite, body weight, and blood glucose control. Clear evidence of central production of IL-18 in the medial habenula is presented, with transport along fibres in the fasciculus retroflexus terminating in the interpeduncular nucleus (IPN). However, no evidence for a corresponding IPN focus of expression of the genes encoding the IL-18 receptor was found. In light of this discrepancy, further investigations were conducted to assess other potential receptors for central IL-18 action; bioinformatics approaches suggest that the interleukin-1 receptor accessory protein like (IL1RAPL) receptors may form alternative central receptors for IL-18, and immunohistochemistry experiments localize IL1RAPL1 in the interpeduncular nucleus. A model is thus proposed whereby habenula IL- 18 expression may influence appetite via actions on IL1RAPL1 in the IPN. The thesis concludes with a discussion of the hypothesis of inflammation as a cause of diabetes and cardiovascular disease, and the potential for an improved understanding of the pathological processes involved in type 2 diabetes to produce greater improvements in clinical outcomes than has been attained thus far. i Acknowledgements: It is difficult to know where to start when it comes to writing an acknowledgements section, as not only have so many assisted during the process of completing this thesis itself and the research contained therein, but also all the others who have provided guidance, mentoring and just simply bouncing-of-ideas in the years beforehand while working as a young scientist, have all in some way or other contributed to the current thesis in your hands now. As little science can be done without money these days, I should perhaps first thank the funders, especially the National Heart Foundation of New Zealand who provided me with a postgraduate scholarship without which, quite simply, this thesis never would have been completed. In many ways it's quite a strange experience to have an organisation you've never previously been involved with contribute a sizeable financial sum to allow you to pursue a higher education and spend your days in research and contemplation, and I am extremely grateful for having had the opportunity to do so. The Southern Trust, Lotteries New Zealand, and Health Research Council of New Zealand have all contributed to the funding of the LOADD study at various stages, and the Maurice and Phyllis Paykel Trust provided pilot funding to pursue our ideas around investigating the neuroendocrine role of IL-18, which led to further funding from the Health Research Council, and these funders jointly contributed to the completion of the work included here. I obviously owe many thanks to my supervisors Jim and Dave. Jim, it's been a long time since I first started working at the Edgar National Centre for Diabetes Research shortly after its formation and had but a vague idea that there was a 'type 1' and 'type 2' diabetes, but your mentoring and inspiration along the way has been invaluable, and I certainly wouldn't have got so far as to contemplate a thesis on diabetes without it. It's a rare experience to work with someone with such a wealth of experience and perspective, and I'm sure your talk of things such as seeing fibre come in and out of nutrition 'fashion' has rubbed off in some way in my appreciation of the historical diabetes literature and thinking of longer-term timescales of research. To Dave, after discussing the problems of obesity and diabetes over many an ale-based beverage I remember coming to you with a paper from Nature Medicine and some vague ideas of trying to figure out what IL-18 was doing in the brain. Maybe you should have said 'aim for something a little less ambitious son!', but I'm glad that instead you were on board with giving it a go and were willing to put your name out there as PI on a project which could well have failed (and did seem like it was for a while). With a bit of ii hindsight maybe I can say that like any good discovery science project, it led us down completely different lines of thought than when we started, and yet despite ending up outside the lab's comfort zone with completely different receptors and brain regions than we'd usually investigate, you've stayed supportive throughout. Many thanks. To all the team involved in the LOADD study: Kirsten, Minako, Sue, Alex, Ashley, Sheila, Margaret, and many others, thanks for all your input and help, you've all certainly made my job the easy one in this project. Thank you Sheila for your additional help in the statistical analysis and interpretation, and I'd especially like to thank Ashley, Holly and Michelle, from the Lipid Laboratory for help with all the LOADD study assays, as well as Drs Sarah Young and Clare Fitzpatrick for their assistance in planning and conducting the multiplex analyses. Many thanks as well to the wider ENCDOR team for their support. There are so many to thank from the 'Grattan lab' that I can't name you all, but special thanks to Ilona, Sharon, Jet and Rachael Augustine who took the time to teach me various hands-on lab procedures during the course of this PhD. To all the wider members of the lab and CNE group, many thanks for providing a great 'science geek' working environment and comraderie in general. I'd also like to thank the members of my PhD committee, who took the time to read over various reports and updates, and provide feedback during our annual meetings: Marilyn, Kirsten, Sheila, Jim, Dave and, for a spell, Dr Alex Tups. Y por último, gracias a mi amor Paulina por soportar mi ausencia durante las noches y fines de semana mientras que estaba ocupado haciendo las investigaciones y escribiendo este pequeño libro. Tal vez es más duro la vida de la pareja de un científico, que la del dicho científico. Entonces espero que valdría la pena para ti también, aunque no puedo garantizar que en el futuro cuando me preguntes en que pienso, que igual no voy a responder 'trabajo'. Gracias por tu apoyo. iii Table of contents: Page Preliminaries Abstract……………………………………………………………………………….. i Acknowledgements…………………………………………………………………... ii Table of contents……………………………………………………………………... iv List of tables…………………………………………………………………………... viii List of figures…………………………………………………………………………. x List of biological and chemical abbreviations………………………………………. xiv List of trial and organisation acronyms……………………………………………... xvi Interleukin-1 family nomenclature…………………………………………………. xvii References for list of figures and interleukin-1 family nomenclature table.......... xviii Section 1: Introduction Chapter 1: Introduction.………………………………………………………………………….. 3 1.1 Diabetes: the glucose disease.………………………………………………………... 4 1.2 The (attempted) prevention of diabetes complications by glucose lowering therapy………………………………………………………………………………... 6 1.3 End of the glucose apotheosis?................................................................................... 11 1.4 The pathogenesis of diabetes and its complications revisited……………………… 12 1.5 Lifestyle effects on inflammatory markers………………………………………….. 27 1.6 Inflammation and diabetes: a key role of NF-κB…………………………………… 37 1.7 A role for IL-18 in metabolic disease………………………………………………... 39 1.8 Patterns and dynamics of cytokine release………………………………………….. 43 Section 2: Inflammatory marker and adipokines in the Lifestyle Over and Above Drugs in Diabetes (LOADD) Study Chapter 2: Overview and methods of the LOADD study 2.1 The LOADD study: rationale………………………………………………………… 47 2.2 Inflammatory markers
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