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Protein and Lipid Interactions Within the Respiratory Chain

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Protein and Lipid Interactions Within the Respiratory Chain Tobias Nilsson Protein and lipid interactions within the respiratory chain Protein and lipid interactions within the respiratory chain the respiratory within and lipid interactions Protein Studies using membrane-mimetic systems Tobias Nilsson Tobias Nilsson Recieved his M.Sc. in Biochemistry from the department of Biochemistry and Biophysics at Stockholm University in 2014. Stopped drinking coffee in 2009. This thesis was produced on tremendous amounts of tea. ISBN 978-91-7797-845-9 Department of Biochemistry and Biophysics Doctoral Thesis in Biochemistry at Stockholm University, Sweden 2019 Protein and lipid interactions within the respiratory chain Studies using membrane-mimetic systems Tobias Nilsson Academic dissertation for the Degree of Doctor of Philosophy in Biochemistry at Stockholm University to be publicly defended on Friday 22 November 2019 at 10.00 in Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B. Abstract Energy conversion from nutrients to ATP is a vital process in cells. The process, called oxidative phosphorylation (OXPHOS) is performed by a combination of membrane-bound proteins. These proteins have been studied in great detail in the past, however much is still unknown about how they interact with each other. Studying the OXPHOS proteins in their native environment can be difficult due to the complexity of living cells. By isolating parts of the OXPHOS system and inserting them into membrane-mimetic systems it is possible to investigate their functions in a controlled environment. In the work presented here, we co-reconstituted several of these proteins into liposomes made from synthetic lipids. We demonstrated production of ATP at steady-state conditions with the ATP synthase, driven by proton pumping by cytochrome bo3. Introduction of anionic lipids decreased the coupled activity and we could correlate this effect to weaker interactions between ATP synthase and cytochrome bo3 in the membrane. We also reconstituted cytochrome c oxidase (CytcO) from Saccharomyces cerevisiae with Respiratory supercomplex factor 1 (Rcf1) into liposomes and submitochondrial particles (SMPs). Loss of Rcf1 has previously been found to result in a lower CytcO activity. We found that activity could be restored upon co-reconstitution of CytcO with Rcf1, but only after unfolding and re-folding of the latter, which shows that Rcf1 can adopt two configurations in the membrane. Keywords: Cytochrome c oxidase, ATP synthase, Bioenergetics, membrane-mimetics, Rcf1, liposomes, oxidative phosphorylation, lipids, protein-protein interactions. Stockholm 2019 http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-173617 ISBN 978-91-7797-845-9 ISBN 978-91-7797-846-6 Department of Biochemistry and Biophysics Stockholm University, 106 91 Stockholm PROTEIN AND LIPID INTERACTIONS WITHIN THE RESPIRATORY CHAIN Tobias Nilsson Protein and lipid interactions within the respiratory chain Studies using membrane-mimetic systems Tobias Nilsson ©Tobias Nilsson, Stockholm University 2019 ISBN print 978-91-7797-845-9 ISBN PDF 978-91-7797-846-6 Printed in Sweden by Universitetsservice US-AB, Stockholm 2019 “It is well known that a vital ingredient of success is not knowing that what you're attempting can't be done.” - Terry Pratchett List of publications & manuscripts I. Von Ballmoos, C., Biner, O*., Nilsson, T.*, & Brzezinski, P. ( 2016 ). Mimicking respiratory phosphorylation using purified enzymes. Biochimica et Biophysica Acta - Bioenergetics, 1857(4), 321–331. II. Nilsson, T., Lundin, C. R., Nordlund, G., Ädelroth, P., Von Ball- moos, C., & Brzezinski, P. ( 2016 ). Lipid-mediated Protein-protein Interactions Modulate Respiration-driven ATP Synthesis. Scien- tific Reports, 6(March), 1–11. III. Sjöholm, J., Bergstrand, J., Nilsson, T., Šachl, R., Von Ballmoos, C., Widengren, J., & Brzezinski, P. ( 2017 ). The lateral distance be- tween a proton pump and ATP synthase determines the ATP- synthesis rate. Scientific Reports, 7(1), 1–12. IV. Nilsson, T., Schäfer, J., Zhou, S., Ädelroth P., & Brzezinski, P. Ac- tivation of Cytochrome c Oxidase from Saccharomyces cere- visiae by Addition of Respiratory Supercomplex Factor 1. (Manuscript) *Equal contributions Additional papers • Knopp, M., Gudmundsdottir, J., Nilsson, T., König, F., Warsi, O., Rajer, F., Ädelroth, P. & Andersson, D. (2019) De novo emergence of peptides conferring antibiotic resistance. mBio, 10 (3) e00837- 19; DOI: 10.1128/mBio.00837-19 Contents Introduction ............................................................................................................... 15 The respiratory chain ................................................................................................ 16 Terminal oxidases ..................................................................................................... 19 Cytochrome c oxidase ............................................................................................................... 20 Ubiquinol oxidase ..................................................................................................................... 23 ATP synthesis ........................................................................................................... 25 Oxidative phosphorylation ........................................................................................................ 25 F1FO ATP synthase .................................................................................................................... 26 Biological membranes .............................................................................................. 29 Fluid mosaic model ................................................................................................................... 29 Membrane phase transitions ...................................................................................................... 30 Lateral proton translocation ...................................................................................................... 31 Lipid properties and membrane compositions ........................................................................... 31 Membrane-mimetic systems ..................................................................................................... 33 Arrangement of respiratory enzymes ........................................................................................ 35 Respiratory supercomplexes ..................................................................................... 37 Respiratory supercomplex factors ............................................................................................. 39 Energy coupling ........................................................................................................ 41 Methods .................................................................................................................... 43 Protein reconstitution in liposomes ........................................................................................... 43 Bioluminescence assay to measure ATP synthase rates ............................................................ 43 Oxygen reduction rates ............................................................................................................. 44 Tunable resistive pulse sensing ................................................................................................. 45 Detection of pH gradients ......................................................................................................... 46 Fluorescence correlation spectroscopy ...................................................................................... 47 Main findings ............................................................................................................ 49 Populärvetenskaplig sammanfattning ....................................................................... 53 Acknowledgements ................................................................................................... 55 References ................................................................................................................. 57 Abbreviations CL – Cardiolipin Cryo-EM – Cryogenic electron microscopy cyt. c – Cytochrome c Cyt cO – Cytochrome c oxidase IMM – Inner mitochondrial membrane IMS – Intermembrane space PA – Phosphatidic acid PC – Phosphatidylcholine PE – Phosphatidylethanolamine PG – Phosphatidyl-glycerol pmf – Proton motive force PS – Phosphatidylserine Rcf – Respiratory supercomplex factor TMH – Transmembrane helix 13 14 Introduction Just like all our home devices need electricity to run, cellular processes need to obtain energy from the molecule ATP. But just like electricity from our power outlets at home isn’t the actual source of energy, ATP is simply the converted form of energy derived from various food sources. The final steps of the process of converting the free energy stored in food to ATP takes place at biological membranes and are performed by a number of enzymes working in tandem. These were discovered and characterized during the last decades, however many aspects of their function are still unknown, especially in regards to how they interact with each other and how they are regulated. In the work presented in this thesis we have attempted to expand the knowledge of how this interplay and regulation may work by studying mainly other processes than the enzymes themselves. In Paper I we developed a method for mimicking parts of the energy- conversion process in vitro by co-reconstituting terminal oxidases
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