Redesigned and reversed: architectural and functional oddities of the trypanosomal ATP synthase
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
33551002
PubMed Central
PMC8311965
DOI
10.1017/s0031182021000202
PII: S0031182021000202
Knihovny.cz E-zdroje
- Klíčová slova
- ATP synthase, cryo-EM, mitochondria, mitochondrial membrane potential, oxidative phosphorylation,
- MeSH
- genetické inženýrství * MeSH
- Leishmania enzymologie MeSH
- membránový potenciál mitochondrií MeSH
- mitochondriální protonové ATPasy genetika metabolismus MeSH
- protozoální proteiny genetika metabolismus MeSH
- Trypanosoma brucei brucei enzymologie MeSH
- Trypanosoma cruzi enzymologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- mitochondriální protonové ATPasy MeSH
- protozoální proteiny MeSH
Mitochondrial F-type adenosine triphosphate (ATP) synthases are commonly introduced as highly conserved membrane-embedded rotary machines generating the majority of cellular ATP. This simplified view neglects recently revealed striking compositional diversity of the enzyme and the fact that in specific life stages of some parasites, the physiological role of the enzyme is to maintain the mitochondrial membrane potential at the expense of ATP rather than to produce ATP. In addition, mitochondrial ATP synthases contribute indirectly to the organelle's other functions because they belong to major determinants of submitochondrial morphology. Here, we review current knowledge about the trypanosomal ATP synthase composition and architecture in the context of recent advances in the structural characterization of counterpart enzymes from several eukaryotic supergroups. We also discuss the physiological function of mitochondrial ATP synthases in three trypanosomatid parasites, Trypanosoma cruzi, Trypanosoma brucei and Leishmania, with a focus on their disease-causing life cycle stages. We highlight the reversed proton-pumping role of the ATP synthase in the T. brucei bloodstream form, the enzyme's potential link to the regulation of parasite's glycolysis and its role in generating mitochondrial membrane potential in the absence of mitochondrial DNA.
Biology Centre Czech Academy of Sciences Branišovská 31 České Budějovice 37005 Czech Republic
Faculty of Science University of South Bohemia Branišovská 31 České Budějovice 37005 Czech Republic
Zobrazit více v PubMed
Abrahams JP, Leslie AG, Lutter R and Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628. PubMed
Agbe A and Yielding KL (1995) Kinetoplasts play an important role in the drug responses of Trypanosoma brucei. Journal of Parasitology 81, 968–973. PubMed
Anselmi C, Davies KM and Faraldo-Gomez JD (2018) Mitochondrial ATP synthase dimers spontaneously associate due to a long-range membrane-induced force. The Journal of General Physiology 150, 763–770. PubMed PMC
Arnold I, Pfeiffer K, Neupert W, Stuart RA and Schagger H (1998) Yeast mitochondrial F1Fo-ATP synthase exists as a dimer: identification of three dimer-specific subunits. The EMBO Journal 17, 7170–7178. PubMed PMC
Asami K, Juniti K and Ernster L (1970) Possible regulatory function of a mitochondrial ATPase inhibitor in respiratory chain-linked energy transfer. Biochimica et Biophysica Acta 205, 307–311. PubMed
Atwood JA III, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R and Tarleton RL (2005). The Trypanosoma cruzi proteome. Science, 309, 473-476. PubMed
Bakker BM, Michels PA, Opperdoes FR and Westerhoff HV (1999) What controls glycolysis in bloodstream form Trypanosoma brucei? Journal of Biological Chemistry 274, 14551–14559. PubMed
Blum TB, Hahn A, Meier T, Davies KM and Kühlbrandt W (2019) Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. Proceedings of the National Academy of Sciences 116, 4250–4255. PubMed PMC
Bowler MW, Montgomery MG, Leslie AG and Walker JE (2007) Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 Å resolution. Journal of Biological Chemistry 282, 14238–14242. PubMed
Brown SV, Hosking P, Li J and Williams N (2006) ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryotic Cell 5, 45–53. PubMed PMC
Brun R, Hecker H and Lun ZR (1998) Trypanosoma evansi and T. equiperdum: distribution, biology, treatment and phylogenetic relationship (a review). Veterinary Parasitology 79, 95–107. PubMed
Bultema JB, Braun HP, Boekema EJ and Kouril R (2009) Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochimica et Biophysica Acta 1787, 60–67. PubMed
Burki F, Roger AJ, Brown MW and Simpson AGB (2020) The new tree of eukaryotes. Trends in Ecology & Evolution 35, 43–55. PubMed
Campanella M, Parker N, Tan CH, Hall AM and Duchen MR (2009) IF1: setting the pace of the F1Fo-ATP synthase. Trends in Biochemical Sciences 34, 343–350. PubMed
Cotter PD and Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiology and Molecular Biology Reviews 67, 429–453. PubMed PMC
Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, Rycovska A, Zickermann V and Kuhlbrandt W (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proceedings of the National Academy of Sciences 108, 14121–14126. PubMed PMC
Davies KM, Anselmi C, Wittig I, Faraldo-Gomez JD and Kuhlbrandt W (2012) Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proceedings of the National Academy of Sciences 109, 13602–13607. PubMed PMC
Dean S, Gould MK, Dewar CE and Schnaufer AC (2013) Single point mutations in ATP synthase compensate for mitochondrial genome loss in trypanosomes. Proceedings of the National Academy of Sciences 110, 14741–14746. PubMed PMC
de Souza W, de Carvalho TM and Barrias ES (2010) Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 2010, 295394. PubMed PMC
Dewar CE, MacGregor P, Cooper S, Gould MK, Matthews KR, Savill NJ and Schnaufer A (2018) Mitochondrial DNA is critical for longevity and metabolism of transmission stage Trypanosoma brucei. PLoS Pathogens 14, e1007195. PubMed PMC
Dey R, Meneses C, Salotra P, Kamhawi S, Nakhasi HL and Duncan R (2010) Characterization of a Leishmania stage-specific mitochondrial membrane protein that enhances the activity of cytochrome c oxidase and its role in virulence. Molecular Microbiology 77, 399–414. PubMed PMC
Dolezelova E, Kunzova M, Dejung M, Levin M, Panicucci B, Regnault C, Janzen CJ, Barrett MP, Butter F and Zikova A (2020) Cell-based and multi-omics profiling reveals dynamic metabolic repurposing of mitochondria to drive developmental progression of Trypanosoma brucei. PLoS Biology 18, e3000741. PubMed PMC
Dudkina NV, Heinemeyer J, Keegstra W, Boekema EJ and Braun HP (2005) Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Letters 579, 5769–5772. PubMed
Dudkina NV, Sunderhaus S, Braun HP and Boekema EJ (2006) Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Letters 580, 3427–3432. PubMed
Dudkina NV, Oostergetel GT, Lewejohann D, Braun HP and Boekema EJ (2010) Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochimica et Biophysica Acta 1797, 272–277. PubMed
Flygaard RK, Mühleip A, Tobiasson V and Amunts A (2020) Type III ATP synthase is a symmetry-deviated dimer that induces membrane curvature through tetramerization. Nature Communications 11, 1–11. PubMed PMC
Formentini L, Sanchez-Arago M, Sanchez-Cenizo L and Cuezva JM (2012) The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Molecular Cell 45, 731–742. PubMed
Gahura O and Zikova A (2019) Isolation of F1-ATPase from the parasitic protist Trypanosoma brucei. Journal of Visualized Experiments 143, e58334. doi: 10.3791/58334 PubMed DOI
Gahura O, Panicucci B, Vachova H, Walker JE and Zikova A (2018a) Inhibition of F1-ATPase from Trypanosoma brucei by its regulatory protein inhibitor TbIF1. The FEBS Journal 285, 4413–4423. PubMed
Gahura O, Subrtova K, Vachova H, Panicucci B, Fearnley IM, Harbour ME, Walker JE and Zikova A (2018b) The F1-ATPase from Trypanosoma brucei is elaborated by three copies of an additional p18-subunit. The FEBS Journal 285, 614–628. PubMed
Garcia-Bermudez J and Cuezva JM (2016) The ATPase inhibitory factor 1 (IF1): a master regulator of energy metabolism and of cell survival. Biochimica et Biophysica Acta 1857, 1167–1182. PubMed
Goes GR, Rocha PS, Diniz AR, Aguiar PH, Machado CR and Vieira LQ (2016) Trypanosoma cruzi needs a signal provided by reactive oxygen species to infect macrophages. PLoS Neglected Tropical Diseases 10, e0004555. PubMed PMC
Goncalves RL, Barreto RF, Polycarpo CR, Gadelha FR, Castro SL and Oliveira MF (2011) A comparative assessment of mitochondrial function in epimastigotes and bloodstream trypomastigotes of Trypanosoma cruzi. Journal of Bioenergetics and Biomembranes 43, 651–661. PubMed
Gu J, Zhang L, Zong S, Guo R, Liu T, Yi J, Wang P, Zhuo W and Yang M (2019) Cryo-EM structure of the mammalian ATP synthase tetramer bound with inhibitory protein IF1. Science 364, 1068–1075. PubMed
Guo H, Bueler SA and Rubinstein JL (2017) Atomic model for the dimeric Fo region of mitochondrial ATP synthase. Science 358, 936–940. PubMed PMC
Hahn A, Vonck J, Mills DJ, Meier T and Kuhlbrandt W (2018) Structure, mechanism, and regulation of the chloroplast ATP synthase. Science 360, eaat4318. PubMed PMC
Harris DA, von Tscharner V and Radda GK (1979) The ATPase inhibitor protein in oxidative phosphorylation. The rate-limiting factor to phosphorylation in submitochondrial particles. Biochimica et Biophysica Acta 548, 72–84. PubMed
He J, Carroll J, Ding S, Fearnley IM and Walker JE (2017) Permeability transition in human mitochondria persists in the absence of peripheral stalk subunits of ATP synthase. Proceedings of the National Academy of Sciences 114, 9086–9091. PubMed PMC
Hierro-Yap C, Subrtová K, Gahura O, Panicucci B, Dewar C, Chinopoulos C, Schnaufer A and Zikova A (2021) Bioenergetic consequences of FoF1-ATP synthase/ATPase deficiency in two life cycle stages of Trypanosoma brucei. Journal of Biological Chemistry 1, 100357. doi: 10.1016/j.jbc.2021.100357. PubMed DOI PMC
Hoare CABSCJ (1937) Spontaneous occurrence of strains of Trypanosoma evansi devoid of kinetonucleus. Parasitology 29, 43–56.
Huang G and Docampo R (2020) The mitochondrial calcium uniporter interacts with subunit c of the ATP synthase of trypanosomes and humans. mBio 11, e00168–20. PubMed PMC
Huet D, Rajendran E, van Dooren GG and Lourido S (2018) Identification of cryptic subunits from an apicomplexan ATP synthase. eLife 7, e38097. PubMed PMC
Inbar E, Hughitt VK, Dillon LA, Ghosh K, El-Sayed NM and Sacks DL (2017) The transcriptome of Leishmania major developmental stages in their natural sand fly vector. mBio 8, e00029–17. PubMed PMC
Jennings RB, Reimer KA and Steenbergen C (1991) Effect of inhibition of the mitochondrial ATPase on net myocardial ATP in total ischemia. Journal of Molecular and Cellular Cardiology 23, 1383–1395. PubMed
Jensen RE, Simpson L and Englund PT (2008) What happens when Trypanosoma brucei leaves Africa. Trends in Parasitology 24, 428–431. PubMed PMC
Junge W and Nelson N (2015) ATP synthase. Annual Reviews of Biochemistry 84, 631–657. PubMed
Khare S, Roach SL, Barnes SW, Hoepfner D, Walker JR, Chatterjee AK, Neitz RJ, Arkin MR, McNamara CW, Ballard J, Lai Y, Fu Y, Molteni V, Yeh V, McKerrow JH, Glynne RJ and Supek F (2015) Utilizing chemical genomics to identify cytochrome b as a novel drug target for Chagas disease. PLoS Pathogens 11, e1005058. PubMed PMC
Klodmann J, Senkler M, Rode C and Braun HP (2011) Defining the protein complex proteome of plant mitochondria. Plant Physiology 157, 587–598. PubMed PMC
Kloehn J, Saunders EC, O'Callaghan S, Dagley MJ and McConville MJ (2015) Characterization of metabolically quiescent Leishmania parasites in murine lesions using heavy water labeling. PLoS Pathogens 11, e1004683. PubMed PMC
Klusch N, Murphy BJ, Mills DJ, Yildiz O and Kuhlbrandt W (2017) Structural basis of proton translocation and force generation in mitochondrial ATP synthase. eLife 6, e33274. PubMed PMC
Kolev NG, Ramey-Butler K, Cross GA, Ullu E and Tschudi C (2012) Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science 338, 1352–1353. PubMed PMC
Kuhlbrandt W (2019) Structure and mechanisms of F-type ATP synthases. Annual Reviews of Biochemistry 88, 515–549. PubMed
Lai DH, Hashimi H, Lun ZR, Ayala FJ and Lukes J (2008) Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proceedings of the National Academy of Sciences 105, 1999–2004. PubMed PMC
Li Y, Shah-Simpson S, Okrah K, Belew AT, Choi J, Caradonna KL, Padmanabhan P, Ndegwa DM, Temanni MR, Corrada Bravo H, El-Sayed NM and Burleigh BA (2016) Transcriptome remodeling in Trypanosoma cruzi and human cells during intracellular infection. PLoS Pathogens 12, e1005511. PubMed PMC
Luevano-Martinez LA, Girard R, Alencar MB and Silber AM (2020) ATP Regulates the activity of an alternative oxidase in Trypanosoma brucei. FEBS Letters 594, 2150–2158. PubMed
Lun ZR and Desser SS (1995) Is the broad range of hosts and geographical distribution of Trypanosoma evansi attributable to the loss of maxicircle kinetoplast DNA? Parasitology Today 11, 131–133. PubMed
Luque-Ortega JR, van't Hof W, Veerman EC, Saugar JM and Rivas L (2008) Human antimicrobial peptide histatin 5 is a cell-penetrating peptide targeting mitochondrial ATP synthesis in Leishmania. The FASEB Journal 22, 1817–1828. PubMed
McConville MJ, Saunders EC, Kloehn J and Dagley MJ (2015) Leishmania carbon metabolism in the macrophage phagolysosome- feast or famine? F1000Research 4, 938. PubMed PMC
Montgomery MG, Gahura O, Leslie AGW, Zikova A and Walker JE (2018) ATP Synthase from Trypanosoma brucei has an elaborated canonical F1-domain and conventional catalytic sites. Proceedings of the National Academy of Sciences 115, 2102–2107. PubMed PMC
Muhleip AW, Joos F, Wigge C, Frangakis AS, Kuhlbrandt W and Davies KM (2016) Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria. Proceedings of the National Academy of Sciences 113, 8442–8447. PubMed PMC
Muhleip AW, Dewar CE, Schnaufer A, Kuhlbrandt W and Davies KM (2017) In situ structure of trypanosomal ATP synthase dimer reveals a unique arrangement of catalytic subunits. Proceedings of the National Academy of Sciences 114, 992–997. PubMed PMC
Muhleip A, McComas SE and Amunts A (2019) Structure of a mitochondrial ATP synthase with bound native cardiolipin. eLife 8, e51179. PubMed PMC
Mühleip A, Kock Flygaard R, Ovciarikova J, Lacombe A, Fernandes P, Sheiner L and Amunts A (2021) ATP Synthase hexamer assemblies shape cristae of Toxoplasma mitochondria. Nature Communications 12, 1–13. PubMed PMC
Murphy BJ, Klusch N, Langer J, Mills DJ, Yildiz O and Kuhlbrandt W (2019) Rotary substates of mitochondrial ATP synthase reveal the basis of flexible F1–Fo coupling. Science 364, eaaw9128. PubMed
Nelson RE, Aphasizheva I, Falick AM, Nebohacova M and Simpson L (2004) The I-complex in Leishmania tarentolae is an uniquely-structured F1-ATPase. Molecular and Biochemical Parasitology 135, 221–224. PubMed
Nolan DP and Voorheis HP (1992) The mitochondrion in bloodstream forms of Trypanosoma brucei is energized by the electrogenic pumping of protons catalysed by the F1Fo-ATPase. European Journal of Biochemistry 209, 207–216. PubMed
Opperdoes FR, Borst P and Spits H (1977) Particle-bound enzymes in the bloodstream form of Trypanosoma brucei. European Journal of Biochemistry 76, 21–28. PubMed
Paiva CN and Bozza MT (2014) Are reactive oxygen species always detrimental to pathogens? Antioxidants & Redox Signaling 20, 1000–1037. PubMed PMC
Panek T, Elias M, Vancova M, Lukes J and Hashimi H (2020) Returning to the fold for lessons in mitochondrial Crista diversity and evolution. Current Biology 30, R575–R588. PubMed
Panicucci B, Gahura O and Zikova A (2017) Trypanosoma brucei TbIF1 inhibits the essential F1-ATPase in the infectious form of the parasite. PLoS Neglected Tropical Diseases 11, e0005552. PubMed PMC
Perez E, Lapaille M, Degand H, Cilibrasi L, Villavicencio-Queijeiro A, Morsomme P, Gonzalez-Halphen D, Field MC, Remacle C, Baurain D and Cardol P (2014) The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae. Mitochondrion 19, 338–349. PubMed
Pinke G, Zhou L and Sazanov LA (2020) Cryo-EM structure of the entire mammalian F-type ATP synthase. Nature Structural & Molecular Biology 27, 1077–1085. PubMed
Preiss L, Langer JD, Yildiz O, Eckhardt-Strelau L, Guillemont JE, Koul A and Meier T (2015) Structure of the mycobacterial ATP synthase Fo rotor ring in complex with the anti-TB drug bedaquiline. Science Advances 1, e1500106. PubMed PMC
Pullman ME and Monroy GC (1963) A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. Journal of Biological Chemistry 238, 3762–3769. PubMed
Ramrath DJF, Niemann M, Leibundgut M, Bieri P, Prange C, Horn EK, Leitner A, Boehringer D, Schneider A and Ban N (2018) Evolutionary shift toward protein-based architecture in trypanosomal mitochondrial ribosomes. Science 362, eaau7735. PubMed
Riou G and Benard J (1980) Berenil induces the complete loss of kinetoblast DNA sequences in Trypanosoma equiperdum. Biochemical and Biophysical Research Communications 96, 350–354. PubMed
Riou GF, Belnat P and Benard J (1980) Complete loss of kinetoplast DNA sequences induced by ethidium bromide or by acriflavine in Trypanosoma equiperdum. Journal of Biological Chemistry 255, 5141–5144. PubMed
Rouslin W, Erickson JL and Solaro RJ (1986) Effects of oligomycin and acidosis on rates of ATP depletion in ischemic heart muscle. American Journal of Physiology 250, H503–H508. PubMed
Salunke R, Mourier T, Banerjee M, Pain A and Shanmugam D (2018) Highly diverged novel subunit composition of apicomplexan F-type ATP synthase identified from Toxoplasma gondii. PLoS Biology 16, e2006128. PubMed PMC
Sathish Yadav KN, Miranda-Astudillo HV, Colina-Tenorio L, Bouillenne F, Degand H, Morsomme P, Gonzalez-Halphen D, Boekema EJ and Cardol P (2017) Atypical composition and structure of the mitochondrial dimeric ATP synthase from Euglena gracilis. Biochimica et Biophysica Acta 1858, 267–275. PubMed
Saunders EC and McConville MJ (2020) Immunometabolism of Leishmania granulomas. Immunology and Cell Biology 98, 832–844. PubMed
Saunders EC, Ng WW, Kloehn J, Chambers JM, Ng M and McConville MJ (2014) Induction of a stringent metabolic response in intracellular stages of Leishmania mexicana leads to increased dependence on mitochondrial metabolism. PLoS Pathogens 10, e1003888. PubMed PMC
Schnaufer A, Domingo GJ and Stuart K (2002) Natural and induced dyskinetoplastic trypanosomatids: how to live without mitochondrial DNA. International Journal of Parasitology 32, 1071–1084. PubMed
Schnaufer A, Clark-Walker GD, Steinberg AG and Stuart K (2005) The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. The EMBO Journal 24, 4029–4040. PubMed PMC
Schwerzmann K and Pedersen PL (1981) Proton-adenosine triphosphatase complex of rat liver mitochondria: effect of energy state on its interaction with the adenosine triphosphatase inhibitory peptide. Biochemistry 20, 6305–6311. PubMed
Senkler J, Senkler M, Eubel H, Hildebrandt T, Lengwenus C, Schertl P, Schwarzlander M, Wagner S, Wittig I and Braun HP (2017) The mitochondrial complexome of Arabidopsis thaliana. The Plant Journal 89, 1079–1092. PubMed
Serricchio M, Hierro-Yap C, Schadeli D, Ben Hamidane H, Hemphill A, Graumann J, Zikova A and Butikofer P (2020) Depletion of cardiolipin induces major changes in energy metabolism in Trypanosoma brucei bloodstream forms. The FASEB Journal 1–16. PubMed
Shah-Simpson S, Pereira CF, Dumoulin PC, Caradonna KL and Burleigh BA (2016) Bioenergetic profiling of Trypanosoma cruzi life stages using seahorse extracellular flux technology. Molecular and Biochemical Parasitology 208, 91–95. PubMed
Silber AM, Tonelli RR, Lopes CG, Cunha-e-Silva N, Torrecilhas AC, Schumacher RI, Colli W and Alves MJ (2009) Glucose uptake in the mammalian stages of Trypanosoma cruzi. Molecular and Biochemical Parasitology 168, 102–108. PubMed
Silva Pereira S, Trindade S, De Niz M and Figueiredo LM (2019) Tissue tropism in parasitic diseases. Open Biology 9, 190036. PubMed PMC
Skodova-Sverakova I, Horvath A and Maslov DA (2015) Identification of the mitochondrially encoded subunit 6 of F1Fo ATPase in Trypanosoma brucei. Molecular and Biochemical Parasitology 201, 135–138. PubMed PMC
Sobti M, Ishmukhametov R, Bouwer JC, Ayer A, Suarna C, Smith NJ, Christie M, Stocker R, Duncan TM and Stewart AG (2019) Cryo-EM reveals distinct conformations of E. coli ATP synthase on exposure to ATP. eLife 8, e43864. PubMed PMC
Speijer D, Breek CK, Muijsers AO, Hartog AF, Berden JA, Albracht SP, Samyn B, Van Beeumen J and Benne R (1997) Characterization of the respiratory chain from cultured Crithidia fasciculata. Molecular and Biochemical Parasitology 85, 171–186. PubMed
Spikes TE, Montgomery MG and Walker JE (2020) Structure of the dimeric ATP synthase from bovine mitochondria. Proceedings of the National Academy of Sciences 117, 23519–23526. PubMed PMC
St-Pierre J, Brand MD and Boutilier RG (2000) Mitochondria as ATP consumers: cellular treason in anoxia. Proceedings of the National Academy of Sciences 97, 8670–8674. PubMed PMC
Stuart KD (1971) Evidence for the retention of kinetoplast DNA in an acriflavine-induced dyskinetoplastic strain of Trypanosoma brucei which replicates the altered central element of the kinetoplast. Journal of Cell Biology 49, 189–195. PubMed PMC
Stuart K (1983) Mitochondrial DNA of an African trypanosome. Journal of Cellular Biochemistry 23, 13–26. PubMed
Subramanian A, Jhawar J and Sarkar RR (2015) Dissecting Leishmania infantum energy metabolism – a systems perspective. PLoS ONE 10, e0137976. PubMed PMC
Subrtova K, Panicucci B and Zikova A (2015) ATPasetb2, a unique membrane-bound FoF1-ATPase component, is essential in bloodstream and dyskinetoplastic trypanosomes. PLoS Pathogens 11, e1004660. PubMed PMC
Timms MW, van Deursen FJ, Hendriks EF and Matthews KR (2002) Mitochondrial development during life cycle differentiation of African trypanosomes: evidence for a kinetoplast-dependent differentiation control point. Molecular Biology of the Cell 13, 3747–3759. PubMed PMC
Tobie EJ (1951) Loss of the kinetoplast in a strain of Trypanosoma equiperdum. Transactions of the American Microscopical Society 70, 251–254.
Vazquez-Acevedo M, Cardol P, Cano-Estrada A, Lapaille M, Remacle C and Gonzalez-Halphen D (2006) The mitochondrial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stator-stalk and in the dimerization of the complex. Journal of Bioenergetics and Biomembranes 38, 271–282. PubMed
Walker JE (1994) The regulation of catalysis in ATP synthase. Current Opinion in Structural Biology 4, 912–918. PubMed
Walker JE (2017) Structure, mechanism and regulation of ATP synthases. In Wikstrom M (ed.), Mechanisms of Primary Energy Transduction in Biology. Cambridge, UK: The Royal Society of Chemistry, pp. 338–373.
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R and Schwede T (2018) Swiss-model: homology modelling of protein structures and complexes. Nucleic Acids Research 46, W296–W303. PubMed PMC
Wittig I, Meyer B, Heide H, Steger M, Bleier L, Wumaier Z, Karas M and Schagger H (2010) Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochimica et Biophysica Acta 1797, 1004–1011. PubMed
Zikova A, Schnaufer A, Dalley RA, Panigrahi AK and Stuart KD (2009) The FoF1-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathogens 5, e1000436. PubMed PMC
Zikova A, Verner Z, Nenarokova A, Michels PAM and Lukes J (2017) A paradigm shift: the mitoproteomes of procyclic and bloodstream Trypanosoma brucei are comparably complex. PLoS Pathogens 13, e1006679. PubMed PMC