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Functional and Phenotypic Characterization of the Stearoyl Coa Desaturase Gene of Anopheles Coluzzii

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Functional and Phenotypic Characterization of the Stearoyl Coa Desaturase Gene of Anopheles Coluzzii Imperial College London Faculty of Natural Sciences, Department of Life Sciences Functional and phenotypic characterization of the Stearoyl CoA desaturase gene of Anopheles coluzzii Zannatul Ferdous Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy, Life Sciences Research, Department of Life Sciences,Imperial College London, January, 2016 1 Declaration of Originality I certify that the thesis and research to which it refers to are solely my own work and the works and ideas from other people which are being used in the thesis are fully acknowledged in accordance with standard referencing practices. Copyright Declaration ‘The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution Non-Commercial No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or redistribution, researchers must make clear to others the licence terms of this work’ 2 Abstract Malaria is an infectious disease caused by Plasmodium parasites that are transmitted by the bite of female Anopheles mosquitoes. Successful acquisition and transmission of malaria parasites requires a female mosquito obtaining a blood meal from human hosts. The blood meal, which is rich in protein, is required for egg development. Most of the ingested protein is converted to lipid and stored in the fat body where vitellogenesis takes place. In this process, saturated fatty acids are converted to unsaturated fatty acids by the stearoyl-CoA desaturase (SCD1). Unsaturated fatty acids are also essential for maintaining cell membrane fluidity and other housekeeping functions. The main aim of this thesis was to functionally and phenotypically characterize the function of SCD1 during blood meal metabolism in the African mosquito vector Anopheles coluzzii. RNA interference (RNAi) silencing of the SCD1 gene and administration of a small molecule inhibitor of SCD1 had a significant impact on the survival of female mosquitoes following a blood meal. SCD1 knockdown (KD) caused a 100% mortality within 48 h after a human blood meal, while addition of the SCD1 small molecule inhibitor sterculic acid (SA) in the blood meal caused a 50% mortality within 72 h of blood meal. Microscopic analysis showed that SCD1 KD mosquitoes failed to develop eggs in response to the blood meal, while their thorax was filled with blood at 24 h post blood meal. These findings were highly consistent with electron microscopy data that showed increased plasma membrane rigidity and depletion of lipid droplets in the midgut epithelial cells. Transcriptional profiling using A. coluzzii oligonucleotide DNA microarrays showed that genes involved in protein, lipid and carbohydrate metabolism, as well as a large number of immunity genes were the most affected in blood-fed SCD1 KD versus control mosquitoes. Metabolomics profiling highlighted the biochemical framework by which the SCD1 KD phenotype is manifested after a blood meal, revealing increased amounts of saturated fatty acids and TCA cycle (and other interlinked pathway) intermediates in SCD1 KD and SA-treated mosquitoes. The data reported in this thesis reveal that silencing of SCD1 in female A. coluzzii mosquitoes leads to a metabolic syndrome primarily associated with the increase of saturated fatty acids and TCA cycle intermediates, which affects important biological functions leading to premature mosquito death. The accumulation of saturated fatty acids is also the likely cause of a potent immune response observed in the absence of infection, 3 which resembles an auto-inflammatory reaction. These data provide important leads for the development of novel interventions aiming to block transmission of mosquito-borne diseases. To My Family 4 Table of Contents Declaration of Originality…………………………………………………………………………….2 Abstract………………………………………………………………………………………………..3 Dedication……………………………………………………………………………………………..4 Table of Contents……………………………………………………………………………………..5 List of figures………………………………………………………………………………………….8 List of Tables……………………………………………………………………………………......10 Acknowledgements ............................................................................................................................... 11 Abbreviations ........................................................................................................................................ 13 Chapter 1 ............................................................................................................................................... 16 General Introduction......................................................................................................................... 16 Summary ........................................................................................................................................... 16 Vector-borne diseases focusing malaria: .......................................................................................... 17 Vectors, global distribution and transmission of VBDs ................................................................. 17 Malaria .......................................................................................................................................... 23 VBD prevention and control ......................................................................................................... 30 A. coluzzii, a new member of A. gambiae complex: ......................................................................... 33 Metabolism of nutrients in the adult mosquitoes: ........................................................................... 33 Sugar digestion and metabolism: ................................................................................................. 34 Blood meal digestion and metabolism: ........................................................................................ 34 Lipolysis, absorption and export: .................................................................................................. 35 Fat storage in fat body: ................................................................................................................. 36 Lipid delivery to ovarian tissues: ................................................................................................... 36 Steroyl Co A desaturase enzyme: Rate limiting enzyme in fatty acid metabolism: ...................... 37 SCD1 inhibitors: ............................................................................................................................. 39 Chapter 2 ............................................................................................................................................... 41 Aims and Objectives .......................................................................................................................... 41 Chapter 3 ............................................................................................................................................... 42 Phenotypic characterization of the Stearoyl-CoA desaturase 1 (SCD1) gene in A. coluzzii mosquitoes........................................................................................................................................ 42 5 Summary ........................................................................................................................................... 42 Introduction ...................................................................................................................................... 43 Nutrient metabolism: .................................................................................................................... 43 Methods ............................................................................................................................................ 46 Anopheles mosquito colony and maintenance ............................................................................ 46 Bioinformatics analysis ................................................................................................................. 46 dsRNAs preparation and gene silencing ....................................................................................... 47 RNA extraction and qRT PCR ......................................................................................................... 47 Transmission electron microscopy ............................................................................................... 47 Results ............................................................................................................................................... 48 Identification of a putative A. coluzzii Stearoyl CoA desaturase .................................................. 48 Silencing SCD1 is lethal to both blood fed and sugar fed mosquitoes ......................................... 50 Silencing SCD1 causes defects at the organismal, tissue and cellular levels ................................ 52 Discussion.......................................................................................................................................... 56 Chapter 4 ............................................................................................................................................... 60 Gene expression and metabolic phenotypes in SCD1 KD A. coluzzii ..............................................
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