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Evolution of the Pgc-1 Protein Family in the Control of Oxidative Metabolism in Vertebrates

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Evolution of the Pgc-1 Protein Family in the Control of Oxidative Metabolism in Vertebrates EVOLUTION OF THE PGC-1 PROTEIN FAMILY IN THE CONTROL OF OXIDATIVE METABOLISM IN VERTEBRATES by Christophe Marie Renaud Le Moine 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 (July, 2008) Copyright © Christophe Marie Renaud Le Moine, 2008 Abstract Mitochondrial biogenesis requires an intricate transcriptional coordination between the nuclear and mitochondrial genomes to establish the structural and functional components of the organelle. This coordination is paramount in vertebrate muscles where oxidative capacity must be adjusted to meet varying energy demands. I investigated the regulatory circuits controlling mitochondrial content in vertebrate muscle in the context of development, adaptation to nutritional status and temperature, and in an evolutionary perspective. Initial experiments focused on the role of transcriptional regulators in the metabolic changes in the myocardium of aging rat. I hypothesized that the changes in oxidative capacity associated with aging would be primarily driven by the peroxisome proliferator activated-receptors (PPARs), the nuclear respiratory factors (NRFs) and their common coactivator PPAR coactivator-1 (PGC-1 . However, the reduction in oxidative capacity in the heart of old rats was independent of these regulatory axes and occurred partially through post-transcriptional processes. The next series of experiments investigated the transcriptional networks regulating the metabolic remodelling in goldfish subjected to dietary and temperature stress. As a potent regulator of mitochondrial proliferation in mammals, I hypothesized that PGC-1 assumed a similar role in lower vertebrates. Similar to their mammalian homologues, PPAR and NRF-1 assumed their respective roles in regulating lipid metabolism and mitochondrial proliferation in goldfish. In contrast, PGC-1 was only a ii good predictor of the PPAR axis, while PGC-1 was a better indicator of the NRF-1 and mitochondrial gene expression axis. This apparent divergence of the PGC-1 homologues in vertebrates inspired the subsequent study, in which I investigated the evolutionary history of the PGC-1 family in vertebrates. Specifically, I sought to assess if PGC-1 functional divergence had a structural and evolutionary basis. PGC-1 phylogeny revealed asymmetric rates of evolution across the different domains of the protein. The domains essential to PGC-1 coactivating activity as well as PPARs interaction motifs were relatively well preserved in all lineages. In contrast, the NRF-1 interacting domain experienced accelerated rates of evolution in fish lineages compared to tetrapods. In addition, fish PGC-1 exhibited consequent insertions in this domain that could have important repercussions on its ability to bind NRF-1 and regulate mitochondrial gene expression. iii Co-Authorship Chapters 1-4 are coauthored with my supervisor Dr. Chris Moyes, who contributed to experimental design, analysis, writing and provided the funding, but thankfully no benchwork. Excerpts from Chapter 1 (sections 1.2.3-1.2.4) were excerted from a published review paper (Moyes and Le Moine 2005). Chapter 2 (Le Moine et al. 2006) is a large collaborative study in collaboration with: O. Mathieu-Costello from University of California San Diego coordinated animal care and tissue harvesting, Dr. G. McClelland (currently at McMaster University) participated in the analysis of lipid oxidation enzymes activities and mRNA, and C. Lyons participated in mitochondrial enzymes activities and mRNA analyses). Chapter 3 (Le Moine et al. 2008) is coauthored with C. Genge who collaborated on experimental design and preliminary RNA analyses. When published, Chapter 4 will be coauthored with Dr. S. Lougheed from Queen’s University who provided guidance in the evolutionary analyses. Moyes CD, and Le Moine CMR. Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes. J. Exp. Biol. 2005. 208: 1601-10. Le Moine CMR, McClelland GB, Lyons CN, Mathieu-Costello O, and Moyes CD. Control of mitochondrial gene expression in the aging rat myocardium. Biochem. Cell Biol. 2006. 84: 191-8. Le Moine CMR, Genge CE, and Moyes CD. Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J. Exp. Biol. 2008. 211: 1448- 55. iv Acknowledgements I would like to start by thanking Chris Moyes for his supervision, support, friendship over my time in his lab, and for even providing me with shelter over the past few months. The experience in the lab wouldn’t have been the same if it weren’t for all current and previous Moyesians who made this experience truly unique. Denise Michaud and Mel Fortner provided invaluable technical expertise and friendship. I also particularly thank the current members of the lab -Rhe, Alexander George, Skippy and Xtine- for their help in the lab and for enduring my rollercoasting mood and crazy tunes over the past few years! Big thanks to all my friends who passed through the department that made my time in Kingston not only studious but fun too, especially Justino, Sweets, Krautchy, Islamilne, James and many more who I hope won’t be offended if by chance they read these pages. Finally, I wouldn’t be there if it weren’t for the support and encouragements from my wife Laurence, and of course my son, Ben who provided additional motivation to be done on time in these last few months. v Table of Contents Abstract ............................................................................................................................................ ii Co-Authorship ................................................................................................................................ iv Acknowledgements .......................................................................................................................... v Table of Contents ............................................................................................................................ vi List of Figures ................................................................................................................................. ix List of Tables ................................................................................................................................... x List of abbreviations ....................................................................................................................... xi Chapter 1 . Introduction and General literature review.................................................................... 1 1.1 Overview ................................................................................................................................ 1 1.2 Mitochondria and oxidative metabolism ................................................................................ 2 1.2.1 Mitochondrial structure ................................................................................................... 4 1.2.2 Mitochondrial function ................................................................................................... 7 1.2.3 Mitochondrial biogenesis ................................................................................................ 8 1.2.4 DNA binding transcriptional regulators ........................................................................ 10 1.3 The PGC-1 family of coactivators ....................................................................................... 13 1.3.1 PGC-1 Structure ............................................................................................................ 14 1.3.2 Regulation of PGC-1 expression and transcriptional activity .................................... 16 1.3.3 Physiological roles of the PGC-1 family ...................................................................... 19 1.4 Evolution of transcriptional regulation ................................................................................ 22 1.4.1 Evolution of cis-elements ............................................................................................. 22 1.4.2 Evolution of transcription factors ................................................................................. 24 1.5 Thesis overview ................................................................................................................... 26 Chapter 2 : Control of mitochondrial gene expression in the aging rat myocardium .................... 29 2.1 Abstract ................................................................................................................................ 29 2.2 Introduction .......................................................................................................................... 30 2.3 Materials and Methods ......................................................................................................... 32 2.3.1 Animals and tissue collection ....................................................................................... 32 2.3.2 Enzyme assays .............................................................................................................. 33 2.3.3 Nucleic acids ................................................................................................................. 34 2.3.4 Statistical analysis ......................................................................................................... 35 2.4 Results and Discussion .......................................................................................................
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