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Research Articles

The physiological role of complex V in ATP synthesis: Murzyme functioning is viable whereas rotary conformation change model is untenable

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Pages 3993-4012 | Received 13 Dec 2021, Accepted 27 Mar 2022, Published online: 08 Apr 2022

References

  • Abrahams, J. P., Leslie, A. G., Lutter, R., & Walker, J. E. (1994). Structure at 2.8 Å resolution of F 1-ATPase from bovine heart mitochondria. Nature, 370(6491), 621–628. https://doi.org/10.1038/370621a0
  • Alavian, K., Beutner, G., Lazrove, E., Sacchetti, S., Park, H.-A., Licznerski, P., Li, H., Nabili, P., Hockensmith, K., Graham, M., Porter, G., & Jonas, E. (2014). An uncoupling channel within the c-subunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore. Proceedings of the National Academy of Sciences of the United States of America, 111(29), 10580–10585. https://doi.org/10.1073/pnas.1401591111
  • Alberty, R. А. (2003). Thermodynamics of biochemical reactions. Wiley.
  • Bai, C., & Warshel, A. (2019). Revisiting the protomotive vectorial motion of F0-ATPase. Proceedings of the National Academy of Sciences of the United States of America, 116(39), 19484–19489. https://doi.org/10.1073/pnas.1909032116
  • Bai, C., Asadi, M., & Warshel, A. (2020). The catalytic dwell in ATPases is not crucial for movement against applied torque. Nature Chemistry, 12(12), 1187–1192. https://doi.org/10.1038/s41557-020-0549-6
  • Bartussek, R., Hänggi, P., & Kissner, J. G. (1994). Periodically rocked thermal ratchets. Europhysics Letters (EPL), 28(7), 459–464. https://doi.org/10.1209/0295-5075/28/7/001
  • Bazhin, N. M. (2020). Standard values of the thermodynamic functions of the formation of ions in an aqueous solution and their change during colvation. The Journal of Physical Chemistry A, 124(52), 11051–11060. https://doi.org/10.1021/acs.jpca.0c08737
  • Bazhin, N., & Manoj, K. M. (2021). Thermodynamics of Hydronium, Zundel and Eigen ions. OSF Preprints. https://doi.org/10.31219/osf.io/b6v24.
  • Beke-Somfai, T., Lincoln, P., & Nordén, B. (2011). Double-lock ratchet mechanism revealing the role of alphaSER-344 in FoF1 ATP synthase. Proceedings of the National Academy of Sciences of the United States of America, 108(12), 4828–4833. https://doi.org/10.1073/pnas.1010453108
  • Benga, G., Popescu, O., Pop, V. I., & Holmes, R. P. (1986). p-(Chloromercuri)benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes. Biochemistry, 25(7), 1535–1538. https://doi.org/10.1021/bi00355a011
  • Berden, J. (2003). Rotary movements within the ATP synthase do not constitute an obligatory element of the catalytic mechanism. IUBMB Life, 55(8), 473–481. https://doi.org/10.1080/15216540310001612318
  • Bernal, R. A., & Stock, D. (2004). Three-dimensional structure of the intact Thermus thermophilus H+-ATPase/synthase by electron microscopy. Structure (London, England: 1993), 12(10), 1789–1798. https://doi.org/10.1016/j.str.2004.07.017
  • Bleier, L., & Dröse, S. (2013). Superoxide generation by complex III: from mechanistic rationales to functional consequences. Biochimica et Biophysica Acta, 1827(11–12), 1320–1331. https://doi.org/10.1016/j.bbabio.2012.12.002
  • Böttcher, B., Bertsche, I., Reuter, R., & Gräber, P. (2000). Direct visualisation of conformational changes in EF(0)F(1) by electron microscopy. Journal of Molecular Biology, 296(2), 449–457. https://doi.org/10.1006/jmbi.1999.3435
  • Boyer, P. D. (1997). The ATP synthase-a splendid molecular machine. Annual Review of Biochemistry, 66(1), 717–749. https://doi.org/10.1146/annurev.biochem.66.1.717
  • Cohn, M., & Drysdale, G. R. (1955). A study with O18 of adenosine triphosphate formation in oxidative phosphorylation. Journal of Biological Chemistry, 216(2), 831–846. https://doi.org/10.1016/S0021-9258(19)81437-0
  • Cope, F., & Glynn, I. (1977). Ion and water transport. Trends in Biochemical Sciences, 2(10), N225–N227. https://doi.org/10.1016/0968-0004(77)90102-5
  • Davis, G. A., & Kramer, D. M. (2019). Optimization of ATP synthase c-rings for oxygenic photosynthesis. Frontiers in Plant Science, 10, 1778. https://doi.org/10.3389/fpls.2019.01778
  • Devenish, R. J., Prescott, M., Boyle, G. M., & Nagley, P. (2000). The oligomycin axis of mitochondrial ATP synthase: OSCP and the proton channel. Journal of Bioenergetics and Biomembranes, 32(5), 507–515. https://doi.org/10.1023/A:1005621125812
  • Dröse, S. (2013). Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning. Biochimica et Biophysica Acta, 1827(5), 578–587. https://doi.org/10.1016/j.bbabio.2013.01.004
  • Fu, D., & Lu, M. (2007). The structural basis of water permeation and proton exclusion in aquaporins. Molecular Membrane Biology, 24(5–6), 366–374. https://doi.org/10.1080/09687680701446965
  • Giorgio, V., Fogolari, F., Lippe, G., & Bernardi, P. (2019). OSCP subunit of mitochondrial ATP synthase: role in regulation of enzyme function and of its transition to a pore. British Journal of Pharmacology, 176(22), 4247–4257. https://doi.org/10.1111/bph.14513
  • Giraud, M. F., Paumard, P., Sanchez, C., Brèthes, D., Velours, J., & Dautant, A. (2012). Rotor architecture in the yeast and bovine F1-c-ring complexes of F-ATP synthase. Journal of Structural Biology, 177(2), 490–497. https://doi.org/10.1016/j.jsb.2011.10.015
  • Grivennikova, V. G., & Vinogradov, A. D. (2006). Generation of superoxide by the mitochondrial Complex I. Biochimica et Biophysica Acta, 1757(5–6), 553–561. https://doi.org/10.1016/j.bbabio.2006.03.013
  • Hayashi, K., Yamasaki, H., & Takano, M. (2009). Rocking ratchet based on F1-ATPase in the absence of ATP. arXiv Preprint. https://doi.org/10.48550/arXiv.0901.0979
  • Haynes, W. M., Editor-in-Chief, Lido, D. R., Bruno, T. J., Associate Editors. (2014). CRC handbook of chemistry and physics (95th ed.). CRC Press.
  • Hinkle, P. C. (2005). P/O ratios of mitochondrial oxidative phosphorylation. Biochimica et Biophysica Acta, 1706(1–2), 1–11. https://doi.org/10.1016/j.bbabio.2004.09.004
  • Hwang, W., & Karplus, M. (2019). Structural basis for power stroke vs. Brownian ratchet mechanisms of motor proteins. Proceedings of the National Academy of Sciences of the United States of America, 116(40), 19777–19785. https://doi.org/10.1073/pnas.1818589116
  • Jaeken, L. (2021). The coacervate-coherence nature of life in fundamentals of cell physiology. BioMedES.
  • Kasumov, E. A., Kasumov, R. E., & Kasumova, I. V. (2015). A mechano-chemiosmotic model for the coupling of electron and proton transfer to ATP synthesis in energy-transforming membranes: a personal perspective. Photosynthesis Research, 123(1), 1–22. https://doi.org/10.1007/s11120-014-0043-3
  • Khananshvili, D., & Gromet-Elhanan, Z. (1984). Demonstration of two binding sites for ADP on the isolated β-subunit of the Rhodospirillum rubrum R1F0F1‐ATP synthase. FEBS Letters, 178(1), 10–14. https://doi.org/10.1016/0014-5793(84)81229-6
  • Krah, A., & Takada, S. (2016). On the ATP binding site of the ε subunit from bacterial F-type ATP synthases. Biochimica et Biophysica Acta, 1857(4), 332–340. https://doi.org/10.1016/j.bbabio.2016.01.007
  • Ksenzenko, M. Y., Vygodina, T. V., Berka, V., Ruuge, E. K., & Konstantinov, A. A. (1992). Cytochrome oxidase‐catalyzed superoxide generation from hydrogen peroxide. FEBS Letters, 297(1–2), 63–66. https://doi.org/10.1016/0014-5793(92)80328-E
  • Kuchel, P. W. (2006). The story of the discovery of aquaporins: convergent evolution of ideas—but who got there first. Cell and Molecular Biology (Noisy-le-Grand), 52(7), 2–5.
  • Lehninger, A., Nelson, D. L., & Cox, M. M. (2004). Lehninger principles of biochemistry (4th ed.). Macmillan.
  • Ling, G. N. (1981). Oxidative phosphorylation and mitochondrial physiology: a critical review of chemiosmotic theory, and reinterpretation by the association-induction hypothesis. Physiological Chemistry and Physics, 13(1), 29–96.
  • López-Beltrán, E. A., Maté, M. J., & Cerdán, S. (1996). Dynamics and environment of mitochondrial water as detected by 1H NMR. The Journal of Biological Chemistry, 271(18), 10648–10653. https://doi.org/10.1074/jbc.271.18.10648
  • Mailer, K. (1990). Superoxide radical as electron donor for oxidative phosphorylation of ADP. Biochemical and Biophysical Research Communications, 170(1), 59–64. https://doi.org/10.1016/0006-291X(90)91240-S
  • Manoj, K. M. (2018a). Debunking chemiosmosis and proposing murburn concept as the operative principle for cellular respiration. Biomedical Reviews, 28(0), 31–48. https://doi.org/10.14748/bmr.v28.4450
  • Manoj, K. M. (2018b). Aerobic respiration: Criticism of the proton-centric explanation involving rotary adenosine triphosphate synthesis, chemiosmosis principle, proton pumps and electron transport chain. Biochemistry Insights, 11, 1178626418818442. https://doi.org/10.1177/1178626418818442
  • Manoj, K. M. (2018c). The ubiquitous biochemical logic of murburn concept. Biomedical Reviews, 29, 89–97. https://doi.org/10.14748/bmr.v29.5854
  • Manoj, K. M. (2021). Some living beings speak up against ‘electron transport chain–chemiosmosis–rotary ATP synthesis’ bioenergetics model. OSF Preprints, https://doi.org/10.31219/osf.io/wamdy
  • Manoj, K. M., & Bazhin, N. M. (2021). Murburn precepts of aerobic respiration and homeostasis. Progress in Biophysics and Molecular Biology, 167, 104–120. https://doi.org/10.1016/j.pbiomolbio.2021.05.010
  • Manoj, K. M., & Soman, V. (2020). Classical and murburn explanations for acute toxicity of cyanide in aerobic respiration: A personal perspective. Toxicology, 432, 152369. https://doi.org/10.1016/j.tox.2020.152369
  • Manoj, K. M., & Tamagawa, H. (2022). Critical analysis of explanations for cellular homeostasis and electrophysiology from murburn perspective. Journal of Cellular Physiology, 237(1), 421–435. https://doi.org/10.1002/jcp.30578
  • Manoj, K. M., Bazhin, N. M., Jacob, V. D., Parashar, A., Gideon, D. A., & Manekkathodi, A. (2021a). Structure-function correlations and system dynamics in oxygenic photosynthesis: classical perspectives and murburn precepts. Journal of Biomolecular Structure and Dynamics, 1–27. https://doi.org/10.1080/07391102.2021.1953606
  • Manoj, K. M., Bazhin, N., & Tamagawa, H. (2021e). The murburn precepts for cellular ionic homeostasis and electrophysiology. Journal of Cellular Physiology, 237(1), 804–814. https://doi.org/10.1002/jcp.30547
  • Manoj, K. M., Gideon, D. A., & Jacob, V. D. (2018). Murburn scheme for mitochondrial thermogenesis. Biomedical Reviews, 29(0), 73–82. https://doi.org/10.14748/bmr.v29.5852
  • Manoj, K. M., Gideon, D. A., & Jaeken, L. (2021c). Why do cells need oxygen? Insights from mitochondrial composition and function. Cell Biology International, 46(3), 344–358. https://doi.org/10.1002/cbin.11746
  • Manoj, K. M., Gideon, D. A., Parashar, A., Nirusimhan, V., Annadurai, P., Jacob, V. D., & Manekkathodi, A. (2021b). Validating the predictions of murburn model for oxygenic photosynthesis: Analyses of ligand-binding to protein complexes and cross-system comparisons. Journal of Biomolecular Structure and Dynamics, 1–33. https://doi.org/10.1080/07391102.2021.1953607
  • Manoj, K. M., Nirusimhan, V., Parashar, A., Edward, J., & Gideon, D. A. (2021d). Murburn precepts for lactic-acidosis, Cori cycle, and Warburg effect: Interactive dynamics of dehydrogenases, protons, and oxygen. Journal of Cellular Physiology, 237(3), 1902–1922. https://doi.org/10.1002/jcp.30661
  • Manoj, K. M., Parashar, A., David Jacob, V., & Ramasamy, S. (2019a). Aerobic respiration: proof of concept for the oxygen-centric murburn perspective. Journal of Biomolecular Structure & Dynamics, 37(17), 4542–4556. https://doi.org/10.1080/07391102.2018.1552896
  • Manoj, K. M., Parashar, A., Gade, S. K., & Venkatachalam, A. (2016). Functioning of microsomal cytochrome P450s: Murburn concept explains the metabolism of xenobiotics in hepatocytes. Frontiers in Pharmacology, 7, 161. https://doi.org/10.3389/fphar.2016.00161
  • Manoj, K. M., Ramasamy, S., Parashar, A., Gideon, D. A., Soman, V., Jacob, V. D., & Pakshirajan, K. (2020). Acute toxicity of cyanide in aerobic respiration: Theoretical and experimental support for murburn explanation. Biomolecular Concepts, 11(1), 32–56. https://doi.org/10.1515/bmc-2020-0004
  • Manoj, K. M., Soman, V., Jacob, V. D., Parashar, A., Gideon, D. A., Kumar, M., Manekkathodi, A., Ramasamy, S., Pakshirajan, K., & Bazhin, N. M. (2019b). Chemiosmotic and murburn explanations for aerobic respiration: predictive capabilities, structure-function correlations and chemico-physical logic. Archives of Biochemistry and Biophysics, 676, 108128. https://doi.org/10.1016/j.abb.2019.108128
  • Matthies, D., Haberstock, S., Joos, F., Dötsch, V., Vonck, J., Bernhard, F., & Meier, T. (2011). Cell-free expression and assembly of ATP synthase. Journal of Molecular Biology, 413(3), 593–603. https://doi.org/10.1016/j.jmb.2011.08.055
  • Mayer, F., & Müller, V. (2014). Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiology Reviews, 38(3), 449–472. https://doi.org/10.1111/1574-6976.12043
  • Mazhab-Jafari, M. T., & Rubinstein, J. L. (2016). Cryo-EM studies of the structure and dynamics of vacuolar-type ATPases. Science Advances, 2(7), e1600725. https://doi.org/10.1126/sciadv.1600725
  • Miranda‐Astudillo, H., Zarco‐Zavala, M., García‐Trejo, J. J., & González‐Halphen, D. (2021). Regulation of bacterial ATP synthase activity: A gear‐shifting or a pawl–ratchet mechanism? The FEBS Journal, 288(10), 3159–3163. https://doi.org/10.1111/febs.15671
  • Mitchell, P. (1985). Molecular mechanics of protonmotive F0F1 ATPases: Rolling well and turnstile hypothesis. FEBS Letters, 182(1), 1–7. https://doi.org/10.1016/0014-5793(85)81142-X
  • Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
  • Mukherjee, S., & Warshel, A. (2017). The FOF1 ATP synthase: from atomistic three-dimensional structure to the rotary-chemical function. Photosynthesis Research, 134(1), 1–15. https://doi.org/10.1007/s11120-017-0411-x
  • Murphy, B. J., Klusch, N., Langer, J., Mills, D. J., Yildiz, Ö., & Kühlbrandt, W. (2019). Rotary substates of mitochondrial ATP synthase reveal the basis of flexible F1-Fo coupling. Science, 364(6446), eaaw9128. https://doi.org/10.1126/science.aaw9128
  • Murphy, M. P. (2009). How mitochondria produce reactive oxygen species. The Biochemical Journal, 417(1), 1–13. https://doi.org/10.1042/BJ20081386
  • Musier, K. M., & Hammes, G. G. (1987). Rotation of nucleotide sites is not required for the enzymatic activity of chloroplast coupling factor 1. Biochemistry, 26(19), 5982–5988. https://doi.org/10.1021/bi00393a006
  • Nath, S. (2017). Two-ion theory of energy coupling in ATP synthesis rectifies a fundamental flaw in the governing equations of the chemiosmotic theory. Biophysical Chemistry, 230, 45–52. https://doi.org/10.1016/j.bpc.2017.08.005
  • Nicholls, D. G. (2004). Mitochondrial membrane potential and aging. Aging Cell, 3(1), 35–40. https://doi.org/10.1111/j.1474-9728.2003.00079.x
  • Noji, H., Yasuda, R., Yoshida, M., & Kinosita, K. (1997). Direct observation of the rotation of F 1-ATPase. Nature, 386(6622), 299–302. https://doi.org/10.1038/386299a0
  • O'Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: An open chemical toolbox. Journal of Cheminformatics, 3(1), 33–14. https://doi.org/10.1186/1758-2946-3-33
  • Parashar, A., & Manoj, K. M. (2021). Murburn precepts for cytochrome P450 mediated drug/xenobiotic metabolism and homeostasis. Current Drug Metabolism, 22(4), 315–326. https://doi.org/10.2174/1389200222666210118102230
  • Parashar, A., Jacob, V. D., Gideon, D. A., & Manoj, K. M. (2021). Hemoglobin catalyzes ATP-synthesis in human erythrocytes: a murburn model. Journal of Biomolecular Structure and Dynamics, 1–13. https://doi.org/10.1080/07391102.2021.1925592
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • Pogoryelov, D., Reichen, C., Klyszejko, A. L., Brunisholz, R., Muller, D. J., Dimroth, P., & Meier, T. (2007). The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. Journal of Bacteriology, 189(16), 5895–5902. https://doi.org/10.1128/JB.00581-07
  • Pollack, G. H. (2013). The fourth phase of water. Ebner & Sons Publishers.
  • Pu, J., & Karplus, M. (2008). How subunit coupling produces the gamma-subunit rotary motion in F1-ATPase. Proceedings of the National Academy of Sciences of the United States of America, 105(4), 1192–1197. https://doi.org/10.1073/pnas.0708746105
  • Rees, D. M., Leslie, A. G., & Walker, J. E. (2009). The structure of the membrane extrinsic region of bovine ATP synthase. Proceedings of the National Academy of Sciences of the United States of America, 106(51), 21597–21601. https://doi.org/10.1073/pnas.0910365106
  • Sanner, M. F. (1999). Python: a programming language for software integration and development. Journal of Molecular Graphics & Modelling, 17(1), 57–61.
  • Schep, D. G., Zhao, J., & Rubinstein, J. L. (2016). Models for the a subunits of the Thermus thermophilus V/A-ATPase and Saccharomyces cerevisiae V-ATPase enzymes by cryo-EM and evolutionary covariance. Proceedings of the National Academy of Sciences of the United States of America, 113(12), 3245–3250. https://doi.org/10.1073/pnas.1521990113
  • Shibata, C., Ehara, T., Tomura, K., Igarashi, K., & Kobayashi, H. (1992). Gene structure of Enterococcus hirae (Streptococcus faecalis) F1F0-ATPase, which functions as a regulator of cytoplasmic pH. Journal of Bacteriology, 174(19), 6117–6124. https://doi.org/10.1128/jb.174.19.6117-6124.1992
  • Stewart, A. G., Lee, L. K., Donohoe, M., Chaston, J. J., & Stock, D. (2012). The dynamic stator stalk of rotary ATPases. Nature Communications, 3(1), 1–8. https://doi.org/10.1038/ncomms1693
  • Stewart, A. G., Sobti, M., Harvey, R. P., & Stock, D. (2013). Rotary ATPases: models, machine elements and technical specifications. Bioarchitecture, 3(1), 2–12. https://doi.org/10.4161/bioa.23301
  • Stock, D., Leslie, A. G., & Walker, J. E. (1999). Molecular architecture of the rotary motor in ATP synthase. Science (New York, NY), 286(5445), 1700–1705.
  • Stroud, R. M., Savage, D., Miercke, L. J., Lee, J. K., Khademi, S., & Harries, W. (2003). Selectivity and conductance among the glycerol and water conducting aquaporin family of channels. FEBS Letters, 555(1), 79–84. https://doi.org/10.1016/S0014-5793(03)01195-5
  • Tsong, T. Y., & Astumian, R. D. (1988). Electroconformational coupling: how membrane-bound ATPase transduces energy from dynamic electric fields. Annual Review of Physiology, 50(1), 273–290. https://doi.org/10.1146/annurev.ph.50.030188.001421
  • Uchihashi, T., Iino, R., Ando, T., & Noji, H. (2011). High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science (New York, NY), 333(6043), 755–758.
  • Volkán-Kacsó, S., & Marcus, R. A. (2017). Theory of long binding events in single-molecule-controlled rotation experiments on F1-ATPase. Proceedings of the National Academy of Sciences of the United States of America, 114(28), 7272–7277. https://doi.org/10.1073/pnas.1705960114
  • von Ballmoos, C., Cook, G. M., & Dimroth, P. (2008). Unique rotary ATP synthase and its biological diversity. Annual Review of Biophysics, 37, 43–64. https://doi.org/10.1146/annurev.biophys.37.032807.130018
  • Watt, IN., Montgomery, M. G., Runswick, M. J., Leslie, A. G., & Walker, J. E. (2010). Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 107(39), 16823–16827. https://doi.org/10.1073/pnas.1011099107

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