ATP Synthase: Structure, Function and Inhibition

1 Khakh BS, Burnstock G. The Double Life of ATP. Scientific American. 2009;301(6):84–92.10.1038/scientificamerican1209-84Search in Google Scholar PubMed

2 Capaldi RA, Aggeler R. Mechanism of the F(1)F(0)-type ATP synthase, a biological rotary motor. Trends in biochemical sciences.2002;27(3):154-60.10.1016/S0968-0004(01)02051-5Search in Google Scholar

3 Zimmerman JJ, Von Saint Andre-von Arnim A, McLaughin J. Cellular Respiration. In: Fuhrman BP, Zimmerman JJ, Editors. Pediatric Critical Crae (4th Ed.). 2011;1085-1072.10.1016/B978-0-323-07307-3.10074-6Search in Google Scholar

4 Bonora M, Patergnani S, Rimessi A, et al. ATP synthesis and storage. Purinergic Signal. 2012;8(3):343-57.10.1007/s11302-012-9305-8Search in Google Scholar PubMed

5 Devenish RJ, Prescott M, Rodgers AJW. The Structure and Function of Mitochondrial F1F0‐ATP Synthases. International review of cell and molecular biology. 2008;267:1-58.10.1016/S1937-6448(08)00601-1Search in Google Scholar PubMed

6 McCarty RE, Evron, Y, Johnson EA. The chloroplast ATP synthase: a rotary enzyme. Annual review of plant biology. 2000;51(1):83-109.10.1146/annurev.arplant.51.1.83Search in Google Scholar

7 Capaldi RA, Aggeler R, Turina P, Wilkens S. Coupling between catalytic sites and the proton channel in F1F0-type ATPases. Trends in biochemical sciences. 1994;19(7):284-289.10.1016/0968-0004(94)90006-XSearch in Google Scholar PubMed

8 Nijtmans LG, Klement P, Houštěk J, Van den Bogert C. Assembly of mitochondrial ATP synthase in cultured human cells: implications for mitochondrial diseases. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 1995;1272(3):190-198.10.1016/0925-4439(95)00087-9Search in Google Scholar

9 Zeviani M, Di Donato S. Mitochondrial disorders. Brain. 2004;127(10):2153-2172.10.1093/brain/awh259Search in Google Scholar PubMed

10 Ahmad Z, Cox JL. ATP Synthase: The Right Size Base Model for Nanomotors in Nanomedicine. The Scientific World Journal. 2014; 2014:567398. Published 2014 Jan 29.10.1155/2014/567398Search in Google Scholar PubMed PubMed Central

11 Yoshida M, Muneyuki E, Hisabori T. ATP synthase a marvellous rotary engine of the cell. Nature Reviews Molecular Cell Biology. 2001;2(9):669-677.10.1038/35089509Search in Google Scholar PubMed

12 Jonckheere AI, Smeitink JA, Rodenburg RJ. Mitochondrial ATP synthase: architecture, function and pathology. Journal of Inherited Metabolic Disease. 2011;35(2):211-225.10.1007/s10545-011-9382-9Search in Google Scholar PubMed

13 Rigoulet M, Mourier A, Devin A. Organization and Regulation of Mitochondrial Oxidative Phosphorylation. In Prof. Valdur Saks, Editor. Molecular System Bioenergetics: Energy for Life. New Jersey: John Wiley & Sons, Inc; 2007:29-58.10.1002/9783527621095.ch2Search in Google Scholar

14 Senior, AE, Nadanaciva S, Weber J. The molecular mechanism of ATP synthesis by F1F0-ATP synthase. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2002;1553(3):188-211.10.1016/S0005-2728(02)00185-8Search in Google Scholar

15 Schäfer G, Engelhard M, Müller V. Bioenergetics of the Archaea. Microbiology and Molecular Biology Reviews. 1999;63(3):570-620.10.1128/MMBR.63.3.570-620.1999Search in Google Scholar

16 Nelson DL, Cox MM. Lehninger Principles of biochemistry.5th Ed. NewYork: WH Freeman and Company; 2008.Search in Google Scholar

17 Feniouk BA. ATP Synthase FAQ. Web site. http://www.atpsynthase.info/FAQ.html Published 2012. Accessed March 26, 2018.Search in Google Scholar

18 McCarty RE. A plant biochemist’s view of H+-ATPases and ATP synthases. Journal of Experimental Biology. 1992;172(1):431-441.10.1242/jeb.172.1.431Search in Google Scholar

19 Noji H, Yoshida M. The rotary machine in the cell, ATP synthase. Journal of Biological Chemistry. 2001;276(3):1665-1668.10.1074/jbc.R000021200Search in Google Scholar

20 Walker JE, Dickson VK. The peripheral stalk of the mitochondrial ATP synthase. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2006;1757(5-6):286-296.10.1016/j.bbabio.2006.01.001Search in Google Scholar

21 Boyer PD. The binding change mechanism for ATP synthase - some probabilities and possibilities. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 1993;1140(3):215-250.10.1016/0005-2728(93)90063-LSearch in Google Scholar

22 Masamitsu F, Mayumi N, Okamoto H, Sekiya M, Nakamoto RK. Rotational catalysis in proton pumping ATPases: From E. coli F-ATPase to mammalian V-ATPase. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 2012;1817(10):1711-1721.10.1016/j.bbabio.2012.03.015Search in Google Scholar PubMed

23 Abrahams JP, Leslie AGW, Lutter R, Walker JE. Structure at 2.8 Â resolution of F1. Nature. 1994;64(2):10-12.Search in Google Scholar

24 Nakamoto RK, Scanlon JAB, Al-Shawi MK. The rotary mechanism of the ATP synthase. Archives of biochemistry and biophysics. 2008;476(1):43-50.10.1016/j.abb.2008.05.004Search in Google Scholar PubMed PubMed Central

25 Duncan TM, Bulygin VV, Zhou Y, Hutcheon ML, Cross RL. Rotation of subunits during catalysis by Escherichia coli F1-ATPase. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(24):10964–10968.10.1073/pnas.92.24.10964Search in Google Scholar PubMed PubMed Central

26 Itoh H, Takahashi A, Adachi K, Noji H, Yasuda R, Yoshida M, et al. Mechanically driven ATP synthesis by F 1-ATPase. Nature. 2004;427(6973):465-468.10.1038/nature02212Search in Google Scholar PubMed

27 Houštek J, Klement P, Floryk D, Antonická H, Hermanská J, Kalous M, et al. A novel deficiency of mitochondrial ATPase of nuclear origin. Human molecular genetics. 1999;8(11):1967-1974.10.1093/hmg/8.11.1967Search in Google Scholar PubMed

28 Kucharczyk R, Zick M, Bietenhader M, Rak M, Couplan E, Blondel M, et al. Mitochondrial ATP synthase disorders: molecular mechanisms and the quest for curative therapeutic approaches. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2009;1793(1):186-199.10.1016/j.bbamcr.2008.06.012Search in Google Scholar PubMed

29 de Vries DD, van Engelen BG, Gabreëls FJ, Ruitenbeek W, van Oost BA. A second missense mutation in the mitochondrial ATPase 6 gene in Leigh’s syndrome. Annals of neurology. 1993;34(3):410-412.10.1002/ana.410340319Search in Google Scholar PubMed

30 Hong S, Pedersen PL. ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas. Microbiology and Molecular Biology Reviews. 2008;72(4):590-641.10.1128/MMBR.00016-08Search in Google Scholar PubMed PubMed Central

31 Houštěk J, Mráček T, Vojtıšková A, Zeman J. Mitochondrial diseases and ATPase defects of nuclear origin. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2004;1658(1-2):115-121.10.1016/j.bbabio.2004.04.012Search in Google Scholar PubMed

32 Johnson KM, Chen X, Boitano A, Swenson L, Opipari AW, Glick GD. Identification and validation of the mitochondrial F1F0-ATPase as the molecular target of the immunomodulatory benzodiazepine Bz-423. Chemistry & biology. 2005;12(4):485-496.10.1016/j.chembiol.2005.02.012Search in Google Scholar PubMed

33 Blatt NB, Bednarski, JJ, Warner RE, Leonetti F, Johnson KM, Boitano A, et al. Benzodiazepine-induced superoxide signalsB cell apoptosis: mechanistic insight and potential therapeutic utility. The Journal of clinical investigation. 2002; 110(8): 1123-1132.10.1172/JCI0216029Search in Google Scholar PubMed

34 Blatt NB, Boitano AE, Lyssiotis CA, Opipari AW, Glick GD. Bz-423 superoxide signals B cell apoptosis via Mcl-1, Bak, and Bax. Biochemical pharmacology. 2009;78(8):966-973.10.1016/j.bcp.2009.05.025Search in Google Scholar PubMed

35 Datiles MJ, Johnson EA, McCarty RE. Inhibition of the ATPase activity of the catalytic portion of ATP synthases by cationic amphiphiles. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2008;1777(4):362-368.10.1016/j.bbabio.2008.01.010Search in Google Scholar

36 Cabezon E, Butler PJ, Runswick MJ, Carbajo RJ, Walker JE. Homologous and heterologous inhibitory effects of ATPase inhibitor proteins on F-ATPases. J. Biol. Chem. 2002;277:41334–41341.10.1074/jbc.M207169200Search in Google Scholar PubMed

37 Pullman ME, Monroy GC. A Naturally Occurring Inhibitor of Mitochondrial Adenosine Triphosphatase. The Journal of Biological Chemistry. 1963;283(11):3762-3769.10.1016/S0021-9258(19)75338-1Search in Google Scholar

38 Cabezón E, Montgomery MG, Leslie AG, Walker JE. The structure of bovine F1-ATPase in complex with its regulatory protein IF 1. Nature Structural and Molecular Biology. 2003;10(9):744-750.10.1038/nsb966Search in Google Scholar

39 Zheng J, Ramirez VD. Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. British Journal of Pharmacology. 2000; 130(5): 1115-23.10.1038/sj.bjp.0703397Search in Google Scholar PubMed

40 Fewtrell CMS, Gomperts BD. Quercetin: A novel inhibitors of Ca2+ influx and exocytosis in rat peritoneal mast cells. Biochimica et Biophysica Acta (BBA) – Biomembranes. 1977;469(1):52-60.10.1016/0005-2736(77)90325-XSearch in Google Scholar

41 Lang DR, Racker E. Effect of quercetin and F1 inhibitor on mitochondrial ATPase and energy-linked reactions in submitochondrial particles. Biochim. Biophys. Acta. 1974;333(2):180–186.10.1016/0005-2728(74)90002-4Search in Google Scholar PubMed

42 Di Pietro A, Godinot C, Bouillant ML, Gautheron DC. Pig heart mitochondrial ATPase: properties of purified and membrane-bound enzyme: Effects of flavonoids. Biochemie. 1975;57(8):959–967.10.1016/S0300-9084(75)80218-5Search in Google Scholar

43 Krasnoff SB, Gupta S, Leger RJ, Renwick JAA, Roberts DW. Antifungal and insecticidal properties of the efrapeptins: Metabolites of the fungus Tolypocladium niveum. Journal of Invertebrate Pathology. 1991;58(2):180-188.10.1016/0022-2011(91)90062-USearch in Google Scholar

44 Lodeyro A, Calcaterra N, Roveri O. Inhibition of steady-state mitochondrial ATP synthesis by bicarbonate, an activating anion of ATP hydrolysis. Biochimica et biophysica acta. 2001;1506(3):236-243.10.1016/S0005-2728(01)00221-3Search in Google Scholar PubMed

45 Arntzen, CJ. Inhibition of photophosphorylation by tentoxin, a cyclic tetrapeptide. Biochimica et biophysica acta. 1972;283(3):539-542.10.1016/0005-2728(72)90273-3Search in Google Scholar PubMed

46 Yarlett N, Lloyd D. Effects of inhibitors on mitochondrial adenosine triphosphatase of Crithidia fasciculata: an unusual pattern of specificities. Molecular and Biochemical Parasitology. 1981;3(1):13–17.10.1016/0166-6851(81)90073-6Search in Google Scholar PubMed

47 Feniouk BA, Skulachev VP. Cellular and Molecular Mechanisms of Action of Mitochondria-Targeted Antioxidants. Current aging science. 2016;10(1):41-48.10.2174/1874609809666160921113706Search in Google Scholar

48 Weber J, Senior AE. Effects of the inhibitors azide, dicyclohexylcarbodiimide, and aurovertin on nucleotide binding to the three F1- ATPase catalytic sites measured using specific tryptophan probes. The Journal of Biological Chemistry. 1998;273:33210–33215.10.1074/jbc.273.50.33210Search in Google Scholar PubMed

49 Bowler MW, Montgomery MG, Leslie AG, Walker JE. How azide inhibits ATP hydrolysis by the F-ATPases. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(23):8646-8649.10.1073/pnas.0602915103Search in Google Scholar PubMed

50 Ahmad Z, Senior AE. Inhibition of the ATPase activity of Escherichia coli ATP synthase by magnesium fluoride. FEBS Letters. 2006;580(2):517– 520.10.1016/j.febslet.2005.12.057Search in Google Scholar PubMed

51 Beil, W, Birkholz C, Wagner S, Sewing KF. Bismuth subcitrate and omeprazole inhibit Helicobacter pylori F1-ATPase. Pharmacology.1995;50(5):333–337.10.1159/000139299Search in Google Scholar PubMed

52 Crosby B, Boutry M, Goffeau A. Inhibition of soluble yeast mitochondria ATPase by ethidium-bromide. Biochemical and Biophysical Research Communications. 1979;88(2):448–455.10.1016/0006-291X(79)92069-2Search in Google Scholar PubMed

53 Gresser MJ, Beharry S, Moennich DM. Inhibition of mitochondrial F1-ATPase by adenylyl imidodiphosphate. Curr. Top. Cell. Regul. 1984;24:365–378.10.1016/B978-0-12-152824-9.50039-3Search in Google Scholar PubMed

54 Mitchell RA, Chang BF, Huang CH, DeMaster EG. Inhibition of mitochondrial energy-linked functions by arsenate: Evidence for a non hydrolytic mode of inhibitor action. Biochemistry. 1971;10:2049–2054.10.1021/bi00787a013Search in Google Scholar

55 Moser TL, Stack MS, Asplin, I, Enghild JJ, Hojrup P, Everitt L, et al. Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc. Natl. Acad. Sci. 1999; 96:2811–2816.10.1073/pnas.96.6.2811Search in Google Scholar

56 Perlin DS, Latchney LR, Senior AE. Inhibition of Escherichia coli H-ATPase by venturicidin, oligomycin and ossamycin. Biochim. Biophys. Acta.1985; 807:238–244.10.1016/0005-2728(85)90254-3Search in Google Scholar PubMed

57 Ren HM, Allison WS, Photoinactivation of the F1-ATPase from spinach chloroplasts by dequalinium is accompanied by derivatization of methionine 183. J. Biol. Chem.1997; 272:32294–32300.10.1074/jbc.272.51.32294Search in Google Scholar

58 Rigoulet M, Ouhabi R, Leverve X, Putod-Paramelle F, Guerin B. Almitrine, a new kind of energy-transduction inhibitor acting on mitochondrial ATP synthase. Biochim. Biophys. Acta. 1989;975:325–329.10.1016/S0005-2728(89)80339-1Search in Google Scholar PubMed

59 Salomon AR, Voehringer DW, Herzenberg LA, Khosla C. Apoptolidin, a selective cytotoxic agent, is an inhibitor of F0F1-ATPase. Chem. Biol. 2001;8:71–80.10.1016/S1074-5521(00)00057-0Search in Google Scholar PubMed

60 Wieker HJ, Kuschmitz D, Hess B. Inhibition of yeast mitochondrial F1-ATPase, F0F1-ATPase and submitochondrial particles by rhodamines and ethidium bromide. Biochim. Biophys. Acta.1987;892:108–117.10.1016/0005-2728(87)90253-2Search in Google Scholar PubMed

61 Zhang S, Letham DD, Jagendorf AT. Inhibition of thylakoid ATPase by venturicidin as an indicator of CF1-CF0 interaction. Plant Physiol. 1993;101:127–133.10.1104/pp.101.1.127Search in Google Scholar PubMed

62 Zheng J, Ramirez VD. Rapid inhibition of rat brain mitochondrial proton F0F1-ATPase activity by estrogens: comparison with Na, K-ATPase of porcine cortex. Eur. J. Pharmacol. 1999;368:95– 102.10.1016/S0014-2999(99)00012-6Search in Google Scholar PubMed