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Farren 2020.Pdf (3.918Mb) This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Investigating the effects of preclinical prion disease on blood protein composition and infectivity Ciara Farren Thesis presented for the degree of Doctor of Philosophy College of Medicine and Veterinary Medicine The University of Edinburgh 2020 Declaration I certify: (a) that the thesis has been composed by me, and (b) either that the work is my own, or, where I have been a member of a research group, that I have made a substantial contribution to the work, such contribution being clearly indicated, and (c) that the work has not been submitted for any other degree or professional qualification except as specified. Ciara Farren 01/03/2020 2 Acknowledgments I would like to express my sincere gratitude to the following people who have helped me in pursuing my interest in prion diseases. My supervisors, Dr Fiona Houston and Dr Andy Gill, I appreciate their constructive feedback and for affording me the opportunity to gain invaluable experience. My lab group, Dr Khalid Salamat and Boon Chin Tan, for their unwavering support and unselfish assistance in my times of need, always going above and beyond to help me. Dr Dominic Kurian and Sam Eaton, for their input with the proteomics work - especially when things did not go to plan and I needed advice in overcoming numerous obstacles. Without their help I would not have been able to complete this project. I am especially grateful for the kindness and compassion of the incredible friends I have made at the Roslin Institute and in Edinburgh. In particular, Ale, Omar, Lukas, Selene, Charity, Deepti, Imogen, Jess and James. My time spent with them has been uplifting, memorable and inspiring. I will miss them all immensely. I would also like to take this opportunity to thank my wonderful and caring friends from London, especially Sanj, Monika and Jaymini. I am thankful for their many Skype chats, phone calls and visits but most of all for our enduring friendship. I would like to thank my Godparents Charles and Mala Davison, as well as my parents Patrick and Suraya Farren, for their unconditional love and support. Above all, they motivated me to focus and persevere. Additionally, I would like to mention my appreciation for the honourable efforts of Mr Babak Arvin, the amazingly kind and empathetic neurosurgeon who got me back on my feet. Also, Dr Lakshumy Sivasegaran and Ms Roopa Nair (as well as their proficient medical teams) for the professional skills and care. Finally, I would like to dedicate this thesis to my late friend Arun Viswambaran. I am grateful for the precious times we spent together and miss him for the exceptionally talented, creative, fun and generous person he was. 3 Abstract Since 1996 there have been 226 cases of variant Creutzfeldt-Jakob disease (vCJD) in the UK following dietary exposure to bovine spongiform encephalopathy (BSE) in the late 80s to early 90s. A recent study on archived appendix tissue has suggested that up to 1/2000 of the UK population may be silent carriers of infection. This is a significant portion of the UK population who may be incubating the disease and thus potentially passing it on to others via blood transfusion. As there is currently no effective screening method to test donated blood this is a major public health concern. The aim of this project was to utilize archived blood samples from transfusion experiments performed with BSE infected sheep, identify protein expression differences between uninfected and infected blood and discover potential diagnostic markers besides the abnormal prion protein (PrPSc). Infected samples were taken from sheep 10 months after oral inoculation with BSE, when their blood was proven to be infectious but the sheep lacked clinical signs. Uninfected samples were taken from the same sheep prior to BSE exposure. Samples from 9 sheep were pooled to control for genetic and metabolic differences. The plasma was processed using ProteoMiner columns to deplete highly abundant proteins while simultaneously enriching for low abundant proteins. Subsequently, isotopic labelling was used to distinguish between the two samples and levels of protein expression were compared by mass spectrometry. Initially 153 proteins were identified based on one unique peptide match. The extent of differential expression was assessed by filtering the median H/L (heavy/light isotopes) and proteins between >1.5 and <0.666 were retained, leaving a dataset of 44 proteins. Elimination of the most common proteins reduced this to 37 proteins and after considering the current literature a candidate shortlist of 8 proteins were chosen to validate by western blotting and LI-COR imaging. The buffy coat fraction of blood from the same 9 sheep were similarly processed. The original dataset of 1148 proteins was cut down to 124 and Ingenuity Pathway Analysis (IPA) employed. This highlighted 191 biological processes of potential interest, including LXR/RXR activation, acute phase response signalling, leukocyte extraversion signalling and mitochondrial dysfunction. A shortlist of 8 candidate proteins were then determined for validation. These findings are the basis for a proposed biomarker panel for an effective preclinical diagnostic blood test. Additionally, in order to investigate how cells pass infection by the human blood transfusion route, blood components from the natural scrapie flock were utilised to infect the Rov9 cell line. The aim of this work was to develop a system to study the processes by which live 4 white blood cells (WBCs) transfer infection to other cells. A cell culture model to study infectivity from scrapie infected WBCs of the Roslin Scrapie Flock was achieved. Further work is needed to examine whether membrane based cellular interactions are essential for efficient propagation of infection and thus spread of disease. 5 Lay summary Compared to other neurodegenerative diseases, prion diseases are unique in that some forms are infectious. Following exposure of the UK population to bovine spongiform encephalopathy (BSE) there have been 226 cases of variant Creutzfeldt-Jakob disease (vCJD), the human form of BSE. It has been suggested that 1 in 2000 people in the age relevant population may be silent carries of vCJD. This figure has been estimated from detection of abnormal prion protein (PrPSc) in appendix tissue samples. It means that a substantial portion of the UK population may be incubating the disease and thus potentially passing it on to others via blood transfusion. This is a major health concern as there is currently no effective screening method to test for these individuals and thus it is a possibility that infected blood will be unknowingly given to a naïve recipient. The aim of this project was to utilize archived blood samples from transfusion experiments performed with BSE infected sheep and screen for differences in protein expression between uninfected and infected blood to identify diagnostic markers besides PrPSc. Donor sheep were orally infected with BSE, their blood collected and transfused to recipient sheep. Since it is established which of the recipients developed BSE, donors with infectious blood can be identified. Infected samples were taken when blood was proven to be infectious but the sheep lacked clinical signs (mimicking the human silent carrier status). Uninfected samples were taken from the same sheep at a time point prior to their exposure to BSE. Samples from 9 sheep were pooled to control for genetic and metabolic differences. A signature of protein expression in the blood of animals that transmitted disease may be of potential significance for diagnostics. This can be determined by use of mass spectrometry and isotopic labelling to distinguish the two groups. Before mass spectrometry samples were treated. Blood is a highly complex and may be separated into distinct fractions by centrifugation. Within plasma around twenty proteins (including albumin, transferrin and fibrinogen) constitute more than 98% of protein. Their presence can obscure detection of low abundant proteins. ProteoMiner technology utilizes a highly diverse library of hexapeptide ligands bound to beads within a small column. Each bead has an affinity for a specific protein. When samples are applied to the column high abundant proteins are concentrated on their beads while simultaneously, low abundant proteins are concentrated on theirs. This creates a final output that is more homogeneous. Following mass spectrometry, 35 proteins were identified as differentially expressed in 6 plasma. From this list candidate proteins were chosen to validate (confirm up or down expression in infected blood) based on previous literature on proteomics of prion diseases. The buffy coat layer of blood contains most of the white blood cells. Pooled buffy coat samples from the same 9 sheep were processed in the same manner, and 122 proteins were identified by mass spectrometry. This larger dataset was then placed into Ingenuity Pathway Analysis (IPA) to investigate the biological context of changes in protein expression. From the suggested disease pathways of IPA and current literature, a shortlist of candidate biomarkers were chosen to follow up on. In total 4 biomarkers for plasma and buff coat samples were validated.
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