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Transcriptional and Genomic Analyses Reveal an Analogous Mechanism for a Piperidinyl

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Transcriptional and genomic analyses reveal an analogous mechanism for a Piperidinyl- Benzimidazolone analogue in Babesia divergens compared to other apicomplexans. by Ingrid Rossouw Submitted in partial fulfilment of the requirements for the degree Philosophiae Doctor In the faculty of Natural and Agricultural Science Department Genetics University of Pretoria Pretoria 2015 Supervisor: Prof. Christine Maritz-Olivier Co-supervisor: Prof. Lyn-Marie Birkholtz 1 Declaration I, Ingrid Rossouw, hereby declare that this dissertation submitted for the degree Philosophiae Doctor at the University of Pretoria, is my own work and has not previously been submitted for a degree at this, or any other university. Ingrid Rossouw Date 2 Plagiarism Declaration Full name: Ingrid Rossouw Student number: 24075681 Title of work: Transcriptional and genomic analyses reveal an analogous mechanism for a Piperidinyl-Benzimidazolone analogue in Babesia divergens compared to other apicomplexans. Declaration: 1. I understand what plagiarism entails and am aware of the University’s policy in this regard. 2. I declare that this thesis (eg. essay, report, project, assignment, dissertation, thesis etc.) is my own, original work. Where someone else’s work has been used (whether from a printed source, the internet or any other source) due acknowledgement was given and reference was made according to the departmental requirements. 3. I did not make use of another student’s previous work and submit it was my own. 4. I did not allow and will not allow anyone to copy my work with the intention of presenting it as his or her own work. 3 Dedication I would like to dedicate this work to the memory of my loving mother. “Be strong and courageous. Do not be terrified; do not be discouraged, for the Lord your God will be with you wherever you go” Joshua 1:9 4 Acknowledgements I wish to thank the following people and organizations without which my research would not have been possible: Prof. Christine Maritz-Olivier my project supervisor for accepting me into her research group, her time, input and guidance. Prof. Lyn-Marie Birkholtz, my co-supervisor for her time, helpful advice, input and acceptance into her lab. I greatly appreciate the use of all her equipment and facilities. Mr. Nicky Olivier at the AGCT for his excellent bioinformatics assistance and advice. My entire research group past and present. The entire malaria research group, in particular Ms. Janette Reader, Dr. Dina Coertzen, Dr. Jandeli Niemand and Dr. Bianca Verlinden. Mr. Willie van Zyl for his patience, advice, computer skills and friendship. Dr. Annel Smit at the flow cytometry unit for her time, input and helpful advice. 5 Dr. Stephane Delbecq, Prof. Eric Marechal and Prof. Laurent Brehelin for providing the Babesia cultures, drug compound and bioinformatic skills, respectively. My dear friends Annette-Christi, Sabine, Bianca, Lorelle, Rudi, Samantha, Luise, Heinrich, Annel and Letitia for their friendship, motivation, lengthy discussions, problem solving abilities, prayers, love and laughter. Funding bodies including the National Research Foundation (NRF), Institutional Research Theme (IRT) (Genomics), Embassy of France in South Africa (Campus France) and the University of Pretoria. To my family, words fail to describe how much I appreciate your prayers, love, support and encouragement over the course of my tertiary studies and in particular the pinnacle - my PhD. Dad, your friendship, faith and insatiable thirst for knowledge motivated me on a daily basis to put things into perspective and to persevere. I wish to thank my siblings, Nicola, Deon and Lize for their unconditional love, for opening their homes and hearts and allowing me to always be myself. My extended family and support system, Nina, Andre, Hennie, Veronica as well as the joys in my life - all the kids, I appreciate your love and support. Lastly to my Lord and Saviour for granting me the opportunity to live my dream, for knowing me better than I know myself and for His unfailing love. 6 Summary Human babesiosis is a rapidly emerging, zoonotic, infectious disease causing potentially life- threatening malaria-like symptoms in humans. Disease prevalence has escalated over the past 50 years from a few isolated cases to endemic areas now being recognized. Early disease detection, diagnosis and treatment with effective anti-babesiacidal compounds are vital for both human and animal health. In humans, Babesia parasites can be cleared by anti-malarials including atovaquone (with azithromycin) or quinine (plus clindamycin) but highly immune- compromised individuals respond poorly to these treatments. In the past few years, reports of resistance against these combinations have emerged, stressing the need for alternative treatments. Ideally one would prefer one drug compound to be effective against numerous pathogens based on a single, commonly shared target feature within the cells. In the post- genomic era, bioinformatics along with several computational strategies have become invaluable for drug discovery to aid in drug target identification followed by in vitro and in vivo validation. The precise progression and duration of the intra-erythrocytic, asexual developmental cycle (IDC) of Babesia has not been clarified to date and current understanding is fraught with uncertainties. This study focuses on the application of sensitive cell- biological -and molecular functional genomics tools to describe the IDC of B. divergens parasites from immature, mono- nucleated ring forms to bi-nucleated paired piriforms and ultimately multi-nucleated tetrads which was further correlated for the first time to nuclear content increases during intra- erythrocytic development progression. This provides insight into the life cycle that occurs during human infection. This study provides the first temporal evaluation of the functional transcriptome of B. divergens parasites. 7 This study contributes to anti-babesiacidal control strategies by evaluating a promising anti- Plasmodium, apicoplast specific piperidinyl-benzimidazolone analogue (A51B1C1_1) as potential therapeutic with low toxicity, against one of the causative agents of human babesiosis, B. divergens. This study set out to describe the global transcriptome of B. divergens parasites (under treated conditions) through its IDC as an indicator of the physiological processes involved. By unravelling the Babesia transcriptome, key gene expression transcripts were defined and conserved gene expression networks between P. falciparum and B. divergens parasites treated with the same compound (A51B1C1_1) identified. This study ultimately contributed to the identification of an apicomplexan parasitic response to treatment. Additionally, it established the investigated compounds’ mode-of-action. 8 Table of Contents Table of Contents ........................................................................................................................ 9 Appendixes (provided in electronic format on accompanying CD) ..................................... 11 List of Tables ............................................................................................................................. 12 List of Figures ........................................................................................................................... 13 List of Abbreviations ................................................................................................................ 15 Chapter 1 ................................................................................................................................... 19 Literature Review ...................................................................................................................... 19 1.1 Introduction ................................................................................................................................................ 19 1.2 Ticks as vectors of both animal and human disease .................................................................................. 20 1.3 The Babesia parasite and pathogenesis of babesiosis ............................................................................... 23 1.3.2 Human babesiosis........................................................................................................................................... 25 1.3.3 Bovine babesiosis ....................................................................................................................................... 35 1.4 Apicomplexa and the apicoplast ................................................................................................................ 37 1.5 Piperidinyl‐benzimidazolone analogues and compound A51B1C1_1 used in this study ............................ 47 1.6 Hypothesis .................................................................................................................................................. 50 1.7 Aims and Objectives ................................................................................................................................... 50 1.8 List of conferences ...................................................................................................................................... 51 1.9 List of research visits .................................................................................................................................. 52 1.10 List of awards ............................................................................................................................................
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