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Biophysical and Biochemical Characterization of Proteins Involved in Α-Glucan Biosynthesis in Mycobacteria

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Biophysical and Biochemical Characterization of Proteins Involved in Α-Glucan Biosynthesis in Mycobacteria Biophysical and biochemical characterization of proteins involved in α-glucan biosynthesis in mycobacteria Ali Asghar Kermani Supervisors: Dr. Klaus Fütterer and Professor Gurdyal Besra Doctoral Thesis Submitted to the School of Biosciences, University of Birmingham University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. Abbreviations AG…………………...arabinogalactan AUC…………………analytical ultracentrifugation BACTH……………...bacterial adenylate cyclase two-hybrid system BSA……………....….bovine serum albumin CAZy………………...Carbohydrate-Active enZYmes database CR3…………………..receptor type 3 DC……………...……dendritic cell DC-SIGN…...……… dendritic cell-specific intercellular adhesion molecule-3-grabbing non-integrin DGG………………... diglucosylglycerate DOT………………… directed observed therapy GlcNAc……………... N-acetyl-α- D -glucosamine IL-12………...……… interleukin-12 IPTG…………………isopropyl β- D -1-thiogalactopyranoside ITC…………………..isothermal titration calorimetry LAM……..………… lipoarabinomannan M1-P…………….…..maltose 1-phosphate mAGP………...……. mycolyl-arabinogalactan-peptidoglycan MDR……………….. multi-drug resistant MGLP……………… methylglucosyl lipopolysaccharides MHC……………….. major histocompatibility complex MR………………….molecular replacement Msm…………………Mycobacterium smegmatis Mtb………………….Mycobacterium tuberculosis NCS…………………non-crystallographic symmetry NF-kB……………….nuclear factor kappa-light-chain-enhancer of activated B cells PBS………………….phosphate buffer saline PEP………………….phosphoenolpyruvate PI3P………...……… phosphatidylinositol 3-phosphate II PMPS………..……... polymethylated polysaccharides PMSF…………….….phenyl methyl sulfonyl fluoride RMSD…………….…root mean square deviation RNI………………….reactive nitrogen intermediates ROI………………….reactive oxygen intermediates SAXS…………….….small angle X-ray scattering SEC……………….....size exclusion chromatography STD NMR…………..saturation transfer difference NMR TACO……………… tryptophan aspartate-containing coat protein TB…………………...tuberculosis TDR…………………totally drug-resistant TLC………………….thin layer chromatography TLR………...………. toll-like receptor TNF………………….tumor necrosis factor TPP……………...…. trehalose phosphate phosphatase TPS……………...…. trehalose phosphate synthase XDR……...………… extensively drug resistant III Abstract A capsule composed of mainly α-glucan forms the most outermost layer of cell envelope of Mycobacterium tuberculosis, the causing agent of tuberculosis. Capsule acts as an inert barrier to prevent the diffusion of macromolecules towards inner parts of the envelope. Also, there is growing evidence that capsular glucans mediate the adhesion and penetration of bacilli into the host cells. In GlgE pathway, one of the three pathways involved in α-glucan synthesis, trehalose in converted to glucan through the activity of four enzymes, trehalose synthase, maltokinase Pep2, maltosyltransferase GlgE and branching enzyme GlgB. The first two enzymes catalyze the conversion of trehalose to maltose, and phosphorylating maltose, respectively. It has shown that M. tuberculosis TreS and Pep2 form an octameric complex together. During this study we solved the structure of the complex at 3.6 Å in M. smegmatis. The structure reveals two pairs of Pep2 monomers bind to the opposite sides of the diamond shaped TreS tetramer in a 4 + 4 complex. However, studying the stoichiometry of the complex using other techniques such as: isothermal titration calorimetry (ITC), analytical ultracntrifugation (AUC) and X-ray scattering indicates a 4 + 2 complex formation in the solution. Moreover, our data using size exclusion chromatography would suggest that this complex formation is pH dependent and favors complex formation at more acidic pHs. This study is a step forward towards better understanding of the capsule synthesis in M. tuberculosis and highlights the role of complex formation between enzymes as an effective strategy to control the metabolic pathways in mycobacteria. IV DECLARATION The work presented in this thesis was carried out in the School of Biosciences at the University of Birmingham, U.K., B15 2TT during the period October 2012 to September 2015. The work in this thesis is original except where acknowledged by references. No part of the work is being, or has been submitted for a degree, diploma or any other qualification at any other University. V Acknowledgments My especial thanks go to Darwin Trust of Edinburgh and Professor Kenneth Murray for funding my Doctoral studies, without which it was only a dream would not come true. I would like to thank my supervisors Dr. Klaus Fütterer and Professor Del Besra for their support and encouragement throughout my PhD project. They taught me how to handle challenging scientific experiments and also, and more importantly, critical thinking and planning the experiments in such a fashion that they will provide me with the answer of scientific questions. I am indebted to Rosemary Parslow and Nick Cotton for their support in using analytical ultracentrifugation and isothermal titration calorimetry, respectively. And to Rana Roy because of his advice, training and friendship during my PhD project. I also would like to thank Del’s lab people in training me with necessary techniques and 8th floor and 7th people for their friendships and supports, especially Dr. Mike Tomlinson. I am also grateful to my parents who have always supported me with my dreams, emotionally and financially. To my brother and my sister who were always available to listen to my problems and challenges. VI Table of Contents 1 Introduction .......................................................................................................... 9 1.1 History of tuberculosis ................................................................................................................................ 1 1.2 Tuberculosis in modern era ...................................................................................................................... 3 1.3 The genus of Mycobacterium .................................................................................................................... 4 1.4 Pathology and immunology of M. tuberculosis infection ............................................................... 6 1.4.1 Phagocytosis of M. tuberculosis by macrophages ......................................................................... 6 1.4.2 Development of TB granuloma ............................................................................................................. 7 1.4.3 Survival inside macrophages ................................................................................................................. 9 1.4.4 Beyond phagocytes .................................................................................................................................. 13 1.5 Current treatment of TB and rise of MDR and XDR strains ...................................................... 13 1.6 The mycobacterial cell envelope .......................................................................................................... 18 1.6.1 Peptidoglycan ............................................................................................................................................ 18 1.6.2 Arabinogalactan ...................................................................................................................................... 21 1.6.3 Mycolic acids .............................................................................................................................................. 23 1.6.4 Capsular layer ........................................................................................................................................... 25 1.7 GlgE pathway enzymes ............................................................................................................................. 38 1.7.1 Trehalose synthase .................................................................................................................................. 38 1.7.2 Maltokinase Pep2 ..................................................................................................................................... 46 1.7.3 Maltosyltransferase GlgE ..................................................................................................................... 50 1.7.4 Branching enzyme GlgB ........................................................................................................................ 55 1.8 Rv3032 pathway .......................................................................................................................................... 57 1.9 Aims and objectives ................................................................................................................................... 61 2 Materials and methods ........................................................................................ 63 2.1 Cloning of Mtb and MsmglgE and glgB ............................................................................................... 64 2.2 Testing
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