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Environmental Sensitivity of Mitochondrial Gene Expression in Fish

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Environmental Sensitivity of Mitochondrial Gene Expression in Fish ENVIRONMENTAL SENSITIVITY OF MITOCHONDRIAL GENE EXPRESSION IN FISH by Katharina Bremer A thesis submitted to the Department of Biology In conformity with the requirements for the degree of Doctor of Philosophy Queen’s University Kingston, Ontario, Canada (October, 2013) Copyright ©Katharina Bremer, 2013 Abstract Maintaining energy organismal homeostasis under changing physiological and environmental conditions is vital, and requires constant adjustments of the energy metabolism. Central to meeting energy demands is the regulation of mitochondrial oxidative capacity. When demands increase, animals can increase mitochondrial content/enzymes, known as mitochondrial biogenesis. Central to mammalian mitochondrial biogenesis is the transcriptional master regulator PPARγ (peroxisome proliferator-activated receptor γ) coactivator-1α (PGC-1α), and the network of DNA-binding proteins it coactivates (e.g. nuclear respiratory factor 1 and 2 [NRF-1, NRF-2], estrogen-related receptor α [ERRα], thyroid receptor α [TRα-1], retinoid X receptor α [RXRα]). However, the mechanisms by which mitochondrial content in lower vertebrates such as fish is controlled are less studied. In my study I investigate underlying mechanisms of the phenomenon that many fish species alter mitochondrial enzyme activities, such as cytochrome c oxidase (COX) in response to low temperatures. In particular, I investigated (i) if the phenomenon of mitochondrial biogenesis during cold-acclimation is related to fish phylogeny, (ii) what role PGC-1α and other transcription factors play in mitochondrial biogenesis in fish, and (iii) if mRNA decay rates are important in the transcriptional control of a multimeric protein like COX. This study shows that mitochondrial biogenesis does not follow a phylogenetic pattern: while distantly related species displayed the same response to low temperatures, closely related species showed opposite responses. In species exhibiting mitochondrial biogenesis, little evidence was found for PGC-1α as a master regulator, whereas NRF-1 is supported to be an important regulator in mitochondrial biogenesis in fish. Further, there was little support for other transcription factors (NRF-2, ERRα, TRα-1, RXRα) to be part of the regulatory network. ii Lastly, results on the post-transcriptional control mechanism of mRNA decay indicate that this mechanism is important in the regulation of COX under mitochondrial biogenesis: it accounts for up to 30% of the change in subunit transcript levels. In summary, there is no simple temperature-dependent mitochondrial response ubiquitous in fish. Further, the pathways controlling mitochondrial content in fish differ from mammals in the important master regulator PGC-1α, however, NRF-1 is important in regulating cold-induced mitochondrial biogenesis in fish. Lastly, COX subunit mRNA decay rates seem to have a part in controlling COX amounts during mitochondrial biogenesis. iii Co-Authorship This thesis is structured according to the manuscript format as outlined in the guidelines provided by The School of Graduate Studies and Research. All data chapters (2-4) are co- authored by Dr. Christopher D. Moyes, whose contributions include intellectual support in project design, project development, financial support for lab and field work, and manuscript design and editing. The second data chapter was co-authored by Christopher T. Monk, an undergraduate student who collected a subset of the data for his undergraduate thesis project, and Dr. Brendon J. Gurd who provided laboratory resources and manuscript editing. Publications arising from and included in this thesis: Bremer K & Moyes CD (2011). Origins of variation in muscle cytochrome c oxidase activity within and between fish species. The Journal of Experimental Biology 214, 1888-1895. Bremer K, Monk CT, Gurd BJ & Moyes CD (2012). Transcriptional regulation of temperature- induced remodeling of muscle bioenergetics in goldfish. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 303, R150-R158. Unpublished manuscripts included in this thesis: Bremer K & Moyes CD (2013). mRNA degradation: an underestimated factor on steady-state transcript levels of cytochrome c oxidase subunits? iv Publications arising from, but not included in this thesis: Duggan AT, Kocha KM, Monk CT, Bremer K & Moyes CD (2011). Coordination of cytochrome c oxidase gene expression in the remodelling of skeletal muscle. The Journal of Experimental Biology 214, 1880-1887. Davies R, Mathers KE, Hume AD, Bremer K, Wang Y & Moyes CD (2012). Hybridization in sunfish influences the muscle metabolic phenotype. Physiological and Biochemical Zoology 85, 321-331. v Acknowledgements First and foremost I would like to thank my supervisor Chris Moyes. Chris took me on as a PhD student in his lab without any previous encounters in person or on the phone. So it was a little surprise when we first met and the start of an adventurous time, not only in his lab, but also here in Canada. After the first year of quite some cultural acclimatization I got to know Chris much better, and despite the many times of being lost in translation both, literally and culturally, he knew how to ask for the best I could do. Sometimes it was very challenging but everything always had an amazing turn-out, if it was getting a manuscript done, presenting at a conference, or going to get fish once a week over the course of a whole winter…. His intellectual support and unique way of showing excitement encouraged me to trust myself and find my way. Now, I am ready to take all I have learned about lab work, science, and myself and move on to new challenges. So, all that is left for me to say to Chris is thank you, you are a great Doktorvater. Besides, Chris, I am thankful for the time, advice, and effort, all my committee members, William Bendena, Don Maurice, and Bruce Tufts, invested and gave me during the course of my thesis. Further, I would like to thank Tika Kocha who introduced me to the Moyes’ lab specific customs and patiently answering my never-ending questions. Also, she was a great lab mate with whom it was fun discussing scientific questions and troubleshooting in the lab. I thank Mel Fortner for being such a great real-timing and western blotting sister and, thinking of western blotting, I will not forget the numerous times Brittany Edgett gave me valuable advice. For my first data chapter, field sampling at QUBS would not have happened without the support of Frank Phelan and Floyd Connor. They always had great tips on where to find the fish. For helping catch them, I thank many people and friends for their patience, sitting with me in a vi boat or freezing with me stumbling through the marshes in summer and winter time and going real ice fishing: Sarah Wyness, Tika Kocha, my supervisor Chris, Paul Debes, and Bruce Tufts. Tice Post and Ron Kerr from the loading dock: thanks a lot for your immense assistance regarding all technical animal care facility problems, and for always having a smile and good chats for me. Emotional support and fun times were ensured by all the past and present Moyes’ lab members. When I arrived in Canada and joined the Moyes lab, especially Rhiannon was a good friend to me introducing me to the city and Queen’s. Finally, but not forgotten, I would like to thank my family at home and here in Canada, Paul. Mama und Papa, seid ich klein bin habt Ihr mir immer vertraut, die richtgen Entscheidungen zu treffen. Als es darum ging nach Kanada zu gehen, brauchte ich kein schlechtes Gewissen zu haben, dass ich Euch verlasse und egoistisch handel, Ihr habt mir immer das Gefühl gegeben, hinter mir zu stehen und mich bei Allem unterstützt was mir wichtig ist. Ohne Eure Unterstützung, hätte ich mir diesen Schritt, in Kanada meine Doktorarbeit zu schreiben, nicht so einfach zugetraut. Danke! Auch dafür, dass Ihr die letzten fünf Jahre immer für mich da ward. Wenn auch nur über skype, so hat es in manchen Situationen sehr geholfen. Paul, ohne das Wissen, dass Du da bist und Deine ständige Unterstützung in der gesamten Zeit, die wir hier in Kanada waren hätte ich wohl so manche Zeit nicht so einfach überstanden. vii Table of Contents Abstract ......................................................................................................................................................... ii Co-Authorship .............................................................................................................................................. iv Acknowledgements ...................................................................................................................................... vi List of Figures ............................................................................................................................................... xi List of Tables ............................................................................................................................................... xii List of Abbreviations ...................................................................................................................................xiii Chapter 1 : General introduction .................................................................................................................. 1 1.1 Mitochondria ...................................................................................................................................... 2 1.1.1 A brief history ..............................................................................................................................
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