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Roles of Regulatory T Cells in Endometriosis-Associated Infertility

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Roles of Regulatory T Cells in Endometriosis-Associated Infertility COPYRIGHT AND USE OF THIS THESIS This thesis must be used in accordance with the provisions of the Copyright Act 1968. Reproduction of material protected by copyright may be an infringement of copyright and copyright owners may be entitled to take legal action against persons who infringe their copyright. Section 51 (2) of the Copyright Act permits an authorized officer of a university library or archives to provide a copy (by communication or otherwise) of an unpublished thesis kept in the library or archives, to a person who satisfies the authorized officer that he or she requires the reproduction for the purposes of research or study. The Copyright Act grants the creator of a work a number of moral rights, specifically the right of attribution, the right against false attribution and the right of integrity. You may infringe the author’s moral rights if you: - fail to acknowledge the author of this thesis if you quote sections from the work - attribute this thesis to another author - subject this thesis to derogatory treatment which may prejudice the author’s reputation For further information contact the University’s Director of Copyright Services sydney.edu.au/copyright Roles of regulatory T cells in endometriosis-associated infertility by Azmat Riaz SID: 420021533 A thesis submitted to the Sydney Medical School in fulfilment of the requirement for the degree of Master of Philosophy in Medicine September 2014 Queen Elizabeth II Research Institute for Mothers and Infants Department of Obstetrics, Gynaecology and Neonatology Sydney Medical School The University of Sydney, NSW, 2006 Australia i Declaration I hereby declare that the contents of this thesis consist of original work carried out by the author unless otherwise stated and duly acknowledged. To the best of my knowledge no part of this thesis has been submitted in whole or part for the award of any other degree of the university or other institution. Azmat Riaz September 2014 ii Acknowledgements First of all, I would like to express my deepest appreciation for my primary supervisor, Dr Alison Hey Cunningham. Without her guidance and help, this thesis would not have been possible within the limited time frame. I would also like to acknowledge, with much appreciation, the crucial role of Dr Marina Berbic for her guidance. Special thanks to Dr Emily Miller, Dr Cecilia Ng, Dr Michael Cooper, Dr Neil Campbell, Dr Nesrin Varol and Dr Anthony Warren for helping me in sample collection, Dr Frank Manconi for his technical assistance, Fiona Kupresanin and Dr Philip Fromm at RPAH for analyzing the samples by flow cytometry, Dr Lyndal Anderson for dating the endometrial samples and Dr Georgina Luscombe and Muhammad Afzal for statistical analysis. I would also like to thank all the students and staff at Queen Elizabeth II Research Institute for Mothers and Infants for their company and encouragement. I appreciate the advice and comments given by Professor Ian Fraser and Dr Robert Markham which helped me improve my presentation skills. I also want to thank my colleagues Cecilia Wong, Manika Saxena and Yachna Mehta who have supported me throughout the study period. I will be grateful forever for your love. Finally, I would like to say a big thanks to my family and husband for their encouragement and prayers. iii Abstract Background Endometriosis is an oestrogen-dependent benign condition which is characterised by the presence of endometrial-like glands and stroma outside the uterus. Women with endometriosis usually present with pelvic pain and/or infertility. Endometriosis is a leading cause of infertility. Endometriosis is commonly thought to result from implantation of viable shed endometrial fragments in the peritoneal cavity after retrograde menstruation through the fallopian tubes; and genetic and endometrial factors, coelomic metaplasia and dissemination of menstrual debris through blood and lymphatic vessels may also contribute to its pathogenesis. In endometriosis, immune cells may be unable to effectively target the shed menstrual debris and allow their implantation. Regulatory T cells (Tregs) are a group of immuno-suppressive lymphocytes that control other immune cells. In early pregnancy, Tregs suppress maternal immune responses to fetal antigens and prevent fetal rejection. Previous studies have demonstrated that Tregs are disturbed in women with endometriosis. Numbers of Tregs may be inadequate in unexplained infertility and sub-clinical pregnancy loss, yet their precise roles in endometriosis and associated infertility are unclear. Aims This project aimed to investigate the proportions and numbers of blood and endometrial Tregs in women with endometriosis and associated infertility. iv Methods Fertile and infertile women with and without endometriosis were recruited. Flow cytometry (n = 50) and immunohistochemistry (n = 88) were performed to analyse circulating and endometrial immune cell proportions and numbers, particularly Tregs, throughout the menstrual cycle. Results The overall results showed that numbers of Tregs and other lymphocytes differed in women with endometriosis, infertility and endometriosis-associated infertility in the menstrual cycle compared to controls. Endometrial Treg proportions were significantly increased during the proliferative phase in fertile compared to infertile women. Proportions of blood and endometrial live lymphocyte populations were increased during the proliferative phase in endometriosis, infertility and endometriosis-associated infertility. Conclusions This project provides new evidence for alterations in blood and endometrial Tregs and other lymphocyte populations in women with endometriosis, infertility and endometriosis- associated infertility. The immune system is tightly regulated during the normal menstrual cycle and variations in these cyclical patterns at systemic and endometrial levels may contribute to reproductive pathologies such as endometriosis and infertility. There is an indication of increased survival of lymphocytes in blood and the endometrium in endometriosis and infertility before the window of implantation. Increased survival of lymphocytes around the peri-implantation period, possibly secondary to altered Treg count in infertile women, may contribute to an inflammatory endometrial environment and to endometriosis and infertility. v TABLE OF CONTENTS DECLARATION................................................................................................................ I ACKNOWLEDGEMENTS ............................................................................................. II ABSTRACT ..................................................................................................................... III TABLE OF CONTENTS ................................................................................................. V LIST OF FIGURES .......................................................................................................... X LIST OF TABLES ......................................................................................................... XII LIST OF ABBREVIATIONS ..................................................................................... XIV CHAPTER 1 ENDOMETRIOSIS .................................................................................... 1 1.1 Introduction .................................................................................................................. 1 1.2 Uterus and menstrual cycle ......................................................................................... 1 1.3 Endometriotic lesions................................................................................................... 4 1.3.1 Peritoneal endometriosis....................................................................................... 5 1.3.2 Ovarian endometriosis .......................................................................................... 5 1.3.3 Deep infiltrating..................................................................................................... 6 1.4 Pathophysiology ........................................................................................................... 7 1.4.1 Genetic factors ....................................................................................................... 7 1.4.2 Theories of pathogenesis ....................................................................................... 7 1.4.2.1 Coelomic metaplasia ....................................................................................... 7 1.4.2.2 Implantation .................................................................................................... 8 1.4.2.3 An endometrial disease .................................................................................. 8 1.4.2.4 An immune disease. ...................................................................................... 12 1.5 Immunological changes ............................................................................................. 12 1.5.1 Immune cells ........................................................................................................ 13 1.5.2 Immune cell dysregulation in endometriosis .................................................... 14 1.5.3 Cytokines and growth factors ............................................................................ 17 1.6 Clinical aspects ........................................................................................................... 20 1.6.1 Symptoms ............................................................................................................
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