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Download Thesis This electronic thesis or dissertation has been downloaded from the King’s Research Portal at https://kclpure.kcl.ac.uk/portal/ Mitochondrial retrograde signalling in the nervous system Hunt, Rachel Joanna Awarding institution: King's College London The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without proper acknowledgement. END USER LICENCE AGREEMENT Unless another licence is stated on the immediately following page this work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International licence. https://creativecommons.org/licenses/by-nc-nd/4.0/ You are free to copy, distribute and transmit the work Under the following conditions: Attribution: You must attribute the work in the manner specified by the author (but not in any way that suggests that they endorse you or your use of the work). Non Commercial: You may not use this work for commercial purposes. No Derivative Works - You may not alter, transform, or build upon this work. Any of these conditions can be waived if you receive permission from the author. Your fair dealings and other rights are in no way affected by the above. Take down policy If you believe that this document breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 04. Oct. 2021 Mitochondrial retrograde signalling in the nervous system Thesis submitted to King’s College London for the degree of Doctor of Philosophy in Molecular Biology Rachel J. Hunt Wolfson Centre for Age-Related Diseases The Institute of Psychiatry, Psychology & Neuroscience King’s College London 2014-18 1 Declaration I hereby declare that all the work presented in this thesis is a result of my own research, and has not been accepted for any other degree. Contributions from others have been clearly acknowledged throughout. Rachel Hunt September 2018 2 Acknowledgements Firstly, I express my immense gratitude to my supervisor, Dr. Joe Bateman, for all his patient guidance, help, support and tolerance; it has made an enormous difference to my work. Many thanks go also to the fabulous members of the Bateman lab, who made the place so friendly. Olivia Duncan, Ariana Gatt, Katja Maierbrugger and Elin Vinsland, for puzzles, laughs, dining extravaganzas and general support. To Olivia and Ariana in particular for their help with dissections and imaging. More recently, thanks to new lab members Prane, Lucy, Ramya and Simo for being equally humorous and helpful, and my new office mates Earl and Jianne for being so welcoming and willing to chat. I thank King’s College London students Jordan Briscoe and Rhian Ford for assistance with climbing assays and optimising aspects of other experiments, and gap-year volunteer Rachel Finlay for preparing gels, solutions, flipping flies and generally giggling. The Wolfson CARD is a lovely place to work, and I also thank the wider Wolfson community, in particular John Chesson for his assistance in the lab and frequent, enjoyable chats on sport, politics and humanity. I thank John G, Brenda, Carl and Fiona for ensuring that everything in the building and the lab ran smoothly, and that nothing was a problem so long as you owned up. And, amongst many others, I thank Leanne, Supanida, Lizzie, Emily B, Keshi, and Elisa for being supportive and friendly fellow students. I am grateful for the approachability of my second supervisor, Prof. Clive Ballard, despite his exile to Devon. I am also indebted to Drs Alison Snape, Stuart Knight and Steve Jones, for inspiring my interest in molecular biology in the first place, and for their subsequent guidance as I attempted to teach it. Lastly and most importantly, I express my utmost gratitude to my parents, Claire and Richard, for being a constant support, and always striving to ensure that I would have as many opportunities as they could provide. I thank my siblings, Rob and Laura, for their sarcasm and gentle ridicule. 3 Abstract Mitochondrial retrograde signalling communicates the functional status of mitochondria to the cell by regulating nuclear gene transcription. Mitochondrial dysfunction is strongly associated with several neurodegenerative diseases, but little is known about mitochondrial retrograde signalling in the nervous system. Mitochondria and the endoplasmic reticulum (ER) share physical and functional links, but the impact of mitochondrial dysfunction on ER biology has been underexplored. In this thesis, I harnessed the array of genetic and functional tools available in the fruit fly, Drosophila melanogaster, to investigate mitochondrial retrograde signalling via the ER in the nervous system. I employed overexpression of mitochondrial transcription factor A (TFAM) as a model of mitochondrial dysfunction. The mitochondrial network was fragmented in the cell bodies of motor neurons overexpressing TFAM, and the morphology of the ER was also changed. There was an increase in the number of candidate ER-mitochondrial contact sites. Mitochondrial Ca2+ levels were substantially increased by TFAM overexpression, as were the levels of cytosolic Ca2+ in stimulated neurons. Mitochondrial dysfunction activated the ER stress signalling pathway, the unfolded protein response (UPR), in Drosophila motor neurons. Genetic manipulation of the UPR revealed that multiple components modify the function of Drosophila motor neurons with mitochondrial dysfunction. In particular, knock-down of the UPR transcription factors ATF4, XBP1 and ATF6 suppressed the neuronal functional impairments caused by mitochondrial dysfunction. Characterisation of the transcriptional response to mitochondrial dysfunction suggested that ATF4 is a key regulator of retrograde signalling in the Drosophila nervous system; 58% of genes that were significantly regulated by TFAM overexpression, were similarly regulated by overexpression of ATF4. Knock-down of ATF4 in conjunction with TFAM overexpression reversed the transcriptional changes caused by TFAM overexpression for 30% of genes. Therefore, I have established that the ER UPR is a mitochondrial retrograde signalling pathway in Drosophila neurons, and importantly, that targeting the UPR can alleviate the effects of mitochondrial dysfunction in neurons. 4 Contents Declaration .................................................................................................................... 2 Acknowledgements ....................................................................................................... 3 Abstract ......................................................................................................................... 4 List of Figures ............................................................................................................. 10 List of Tables ............................................................................................................... 12 List of abbreviations .................................................................................................... 13 1. Introduction ................................................................................................................. 15 1.1 Mitochondria ..................................................................................................... 15 1.1.1 Origins and discovery ..................................................................................... 15 1.1.2 Energy production pathways in mitochondria ................................................ 16 1.1.2.1 Fatty acid oxidation and the Krebs cycle (Citric acid cycle) .................... 17 1.1.2.2 Oxidative phosphorylation (OXPHOS) .................................................... 18 1.1.2.2.1 Generation of reactive oxygen species (ROS) ................................... 20 1.1.3 Mitochondria structure and function ............................................................... 21 1.1.3.1 Composition and permeability of mitochondrial membranes .................. 21 1.1.3.2 Mitochondrial DNA (mtDNA) ................................................................. 22 1.1.3.3 Mitochondrial Ca2+ handling .................................................................... 25 1.1.3.4 Mitochondrial dynamics ........................................................................... 26 1.1.4 Mitochondrial dysfunction and disease ........................................................... 27 1.1.5 Mitochondrial retrograde signalling ................................................................ 29 1.1.5.1 Mitochondrial retrograde signalling in yeast [adapted excerpt from (Hunt and Bateman 2018)] .............................................................................................. 29 1.1.5.2 Calcium ..................................................................................................... 32 1.1.5.3 ROS .......................................................................................................... 33 1.1.5.4 The mitochondrial unfolded protein response (mtUPR) [adapted excerpt from (Hunt and Bateman 2018)] .......................................................................... 33 1.1.5.5 Mitochondrial retrograde signalling in the nervous system ..................... 37 1.2 Drosophila as a model organism ...................................................................... 39 1.2.1 Drosophila models of neuronal mitochondrial dysfunction and retrograde signalling .................................................................................................................
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