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Exploring the Effects of Endemic East African Co-Infections on HIV Susceptibility in the Female Genital Tract

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Exploring the Effects of Endemic East African Co-Infections on HIV Susceptibility in the Female Genital Tract Exploring the Effects of Endemic East African Co-infections on HIV Susceptibility in the Female Genital Tract by Sergey Yegorov A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Immunology University of Toronto © Copyright by Sergey Yegorov 2018 Abstract Exploring the Effects of Endemic East African Co-infections on HIV susceptibility in the Female Genital Tract Sergey Yegorov Doctor of Philosophy Department of Immunology University of Toronto 2018 RATIONALE: Human immunodeficiency virus (HIV) remains a leading cause of global morbidity with the highest burden in Sub-Saharan Africa (SSA). For reasons that are incompletely understood, the likelihood of HIV transmission is several fold higher in SSA than in higher income countries, and most of these infections are acquired by women. Residents of SSA are also exposed to a variety of endemic infections that could elevate HIV susceptibility through effects on mucosal and systemic immunology. In the East African Lake Victoria region high HIV transmission geographically overlaps with endemic malaria and Schistosoma mansoni infections. Therefore in this thesis I aimed to explore the impact of these infections on HIV susceptibility in the female genital tract. MAIN FINDINGS: The prevalence of malaria in adult women from Entebbe, Uganda was much lower than expected, but this low prevalence was masked by high rates of over-diagnosis in public health facilities. The prevalence of S. mansoni infection approached 50% and was associated with systemic immune alterations and several socio-behavioral HIV risk factors, emphasizing the importance of controlling these confounders in mucosal studies. A longitudinal clinical trial of S. mansoni treatment effects [ClinicalTrials.gov ID: NCT02878564] demonstrated a substantial anthelminthic treatment-induced reduction of HIV entry into both genital and blood CD4 T cells for two ii months after standard therapy, despite transient mucosal and systemic immune activation. Furthermore, schistosomiasis treatment was associated with the induction of Type I Interferon pathways, providing a possible mechanism for the reduced HIV entry seen in the trial. CONCLUSIONS: Collectively, the findings presented in this thesis i) highlight the importance of understanding the epidemiology of endemic infections and associated socio-behavioral factors that could confound studies of mucosal HIV susceptibility, and ii) suggest that S. mansoni treatment may lead to new HIV prevention strategies in SSA. iii Acknowledgements It is with immense gratitude that I acknowledge all of the study participants, my mentors, colleagues, study team members and friends. This thesis would not have been possible without the participation, support, mentorship and encouragement of so many of you. While it is impossible to acknowledge here everyone, I will try to thank some of the most important people that helped this dissertation become a reality. First and foremost, I thank my PhD supervisor and mentor, Dr. Rupert Kaul, for believing in me and providing me with the opportunity to work on the most unusual and exciting research projects. If I were given a choice to start my PhD studies all over again, I would not hesitate to choose the Kaul lab again. I am truly thankful to my PhD committee members, Dr. Kevin Kain, Dr. Scott Gray-Owen and Dr. Andrea Boggild, for sharing their immense expertise and knowledge and guiding me through the long and winding PhD path. I deeply thank the past and present members of the Kaul lab for their endless support and friendship. I am especially grateful to Jessica Prodger for introducing me to doing research in Uganda. I sincerely thank Vineet Joag for sharing the secrets of successfull laboratory experimentation and for mind-challenging scientific discussions. I extend my gratitude to Ronald Galiwango, who was always there to encourage me and discuss everything- from failure to success. I am thankful to Catia Perciani for her mentorship and everlasting enthusiasm for science. I am deeply indepted to Sanja Huibner, who has been a constant source of support for me and who made it possible for many of the experiments described in this thesis to go smoothly. I say a big thank you to Kamnoosh Shahabi, Rodney Rousseau, Connie J. Kim, Brett Shannon, Avid Mohammadi, Yoojin Choi, Elizabeth Lau, Segen Kidane, Fat Malazogu, Rabea Nadeem, Sareh Bagherichimeh and Sarah Grech for all your wisdom, help and advice. I would like to acknowledge all my colleagues in the HIV Research group at UofT, especially the members of Dr. Mario Ostrowski's lab- Jun Liu, Nur Rahman, Vitaliy Matveev, Shariq Mujib, Jordan Schwartz, Parshin Edraki, Amber Wang, Mohammed Saleh- for all your help, collaboration and friendship. I thank the faculty and students in the Department of Immunology for insightful dialogues and bright ideas. Special thanks iv to Professor Michelle Letarte, who has been a great mentor to me and has now become a family friend. I greatly appreciate my colleagues and study team members in Uganda, where I spent almost a year working on our research projects. I am grateful to Dr. Noah Kiwanuka and Dr. Bernard Bagaya for their partnership. I would like to extend my gratitude to the members of UVRI-IAVI- Paul Kato, Brian Kabuubi, Enoch Muyanja, Aloysious Ssemaganda, Andrew Mubiru, Dr Juliet Mpendo, Violet Mirembe, Monica Balyeku, Racheal Wanyana and Annet Nanvubya- for their diligence and willingness to help with our studies. I am deeply thankful to the staff of the UVRI clinic, and especially George Miiro, Obenyu Peninah Akiteng and David Drajole, without whose participation our studies would have been impossible to realize. I thank the staff of Entebbe Hospital- Sr. Winfred, Shardiah Namusisi, Sr. Josephine, Sr. Kalule, Sr. Stella and Rose Openda. I am also sincerely thankful to the Entebbe community and Calvary Chapel for helping our community outreach. Thank you to Professor Alison Elliot and Dr. Stephen Cose for allowing me to participate in your lab meetings and to learn from your vast knowledge of immunology and infectious disease. Finally, I profoundly thank my family. Thanks to my mum, aunts and cousins for being patient and encouraging of my studies, even when that meant being far apart from me. To Sara- for endless motivation, for being with me on both good and bad days, for helping me succeed in Africa...for everything… and for Aleksey! Thank you. v Table of Contents Acknowledgements ......................................................................................................... iv List of Figures ................................................................................................................. ix List of Tables ................................................................................................................... x List of Abbreviations ........................................................................................................ xi List of Publications ........................................................................................................ xiv Chapter I: Introduction .................................................................................................... 1 1. HIV biology and evolution ........................................................................................ 1 1.1 Brief history ................................................................................................................. 1 1.2 HIV nomenclature and global distribution .................................................................... 2 1.3 HIV structure and life cycle ......................................................................................... 3 2. HIV disease and transmission ................................................................................. 4 2.1 HIV clinical course: brief overview ............................................................................... 4 2.2 HIV acquisition routes: a focus on women .................................................................. 5 2.3 Initial steps of HIV infection in the Female genital tract ............................................... 5 2.4 HIV target cells and markers of susceptibility .............................................................. 7 2.4.1 T cell subtypes ........................................................................................................ 7 2.4.2 Activation markers: CD38 and HLA-DR................................................................... 8 2.4.3 Activation markers: CD69 ....................................................................................... 8 2.4.4 Integrins and the Common mucosal immunologic system ....................................... 9 2.4.5 Antiviral defense mechanisms ............................................................................... 11 2.4.5.1 IFN-I signaling: a potent antiviral defense mechanism .................................................11 2.4.6 Inflammation and HIV susceptibility ....................................................................... 14 2.4.7 Cytokines and HIV susceptibility ........................................................................... 15 3. Endemic co-infections and HIV susceptibility..........................................................16 3.1 Malaria ...................................................................................................................... 17 3.1.1 Impact of malaria on HIV susceptibility: epidemiological evidence .......................
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