A new model for mitochondrial membrane potential production and storage

Medical Hypotheses

Volumn 83, Issue 2, 2014, Pages 175-181

  Bagkos, Georgios ^a   Koufopoulos, Kostas ^a   Piperi, Christina ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CYTOCHROME C OXIDASE; HYDROGEN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); WATER; ADENOSINE TRIPHOSPHATE; MULTIENZYME COMPLEX; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; BIOENERGY; BIOLOGICAL ACTIVITY; CELL FUNCTION; CELL VIABILITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRIC CURRENT; ELECTRICAL POTENTIAL PARAMETERS; ELECTRICITY; ELECTRON TRANSPORT; ENERGY CONSERVATION; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PROTEIN HYDROLYSIS; PROTON TRANSPORT; RESPIRATORY CHAIN; BIOLOGICAL MODEL; BIOSYNTHESIS; ENERGY METABOLISM; HYDROLYSIS; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; HUMANS; HYDROLYSIS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MODELS, BIOLOGICAL; PROTON-TRANSLOCATING ATPASES;

EID: 84902765798     PISSN: 03069877     EISSN: 15322777     Source Type: Journal    
DOI: 10.1016/j.mehy.2014.05.001     Document Type: Article

References (96)

1. Kadenbach B., Ramzan R., Vogt S. Degenerative diseases, oxidative stress and cytochrome c oxidase function. Trends Mol Med 2009, 15(4):139-147.
2. Komi Y., Ohno O., Suzuki Y., et al. Inhibition of tumor angiogenesis by targeting endothelial surface ATP synthase with sangivamycin. Japn J Clin Oncol 2007, 37(11):867-873.
3. Gonzalez O., Gronau S., Pfeiffer F., Mendoza E., Zimmer R., Oesterhelt D. Systems analysis of bioenergetics and growth of the extreme halophile Halobacterium salinarum. PLoS Comput Biol 2009, 5(4):e1000332.
4. Cardona T., Battchikova N., Zhang P., Stensjö K., Aro E.-M., Lindblad P., et al. Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim Biophys Acta 2009, 1787:252-263.
5. Vantourout P., Radojkovic C., Lichtenstein L., Pons V., Champagne E., Martinez L.O. Ecto-F1-ATPase: a moonlighting protein complex and an unexpected apoA-I receptor. World J Gastroenterol 2010, 16(47):5925-5935.
6. Nishikawa T., Araki E. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 2007, 9(3):343-353.
7. Rask-Madsen C., King G.L. Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab 2013, 17(1):20-33.
8. Seddon M., Looi Y.H., Shah A.M. Oxidative stress and redox signalling in cardiac hypertrophy and heart failure. Heart 2007, 93:903-907.
9. Camara A.K.S., Bienengraeber M., Stowe D.F. Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol 2011, 2:13.
10. Hedskog L., Zhang S., Ankarcrona M. Strategic role for mitochondria in Alzheimer's disease and cancer. Antioxid Redox Signal 2012, 16(12):1476-1489.
11. Ralpha S.J., Rodriguez-Enriquez S., Neuzil J., Moreno-Sanchez R. Bioenergetic pathways in tumor mitochondria as targets for cancer therapy and the importance of the ROS-induced apoptotic trigger. Mol Aspects Med 2010, 31:29-59.
12. Whitaker-Menezes D., Martinez-Outschoorn U.E., Flomenberg N., et al. Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ. Cell Cycle 2011, 10(23):4047-4064.
13. Lyon A.R., Jourdey P.J., Jin D., et al. Optical imaging of mitochondrial function uncovers actively propagating waves of mitochondrial membrane potential collapse across intact heart. J Mol Cell Cardiol 2010, 49:565-575.
14. Camara A.K.S., Lesnefsky E.J., Stowe D.F. Potential therapeutic benefits of strategies directed to mitochondria. Antioxid Redox Signal 2010, 13(3):279-347.
15. Bashan N., Kovsan J., Kachko I., Ovadia H., Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009, 89:27-71.
16. Ristow M., Zarse K. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 2010, 45:410-418.
17. Kuznetsov A.V., Margreiter R. Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int J Mol Sci 2009, 10:1911-1929.
18. Geissler A., Krimmer T., Bomer U., Guiard B., Rassow J., Pfanner N. Membrane potential-driven protein import into mitochondria. Mol Biol Cell 2000, 11:3977-3991.
19. Quarato G., Piccoli C., Scrima R., Capitanio N. Functional imaging of membrane potential at the single mitochondrion level: possible application for diagnosis of human diseases. Mitochondrion 2011, 11:764-773.
20. Butow R.A., Avadhani N.G. Mitochondrial signaling: the retrograde response. Mol Cell 2004, 14:1-15.
21. Strahl H., Hamoen L.W. Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 2010, 107(27):12281-12286.
22. Miceli M.V., Jiang J.C., Tiwari A., Rodriguez-Quiñones J.F., Jazwinski S.M. Loss of mitochondrial membrane potential triggers the retrograde response extending yeast replicative lifespan. Front Genet 2012, 2:1-11.
23. Hawkins B.J., Levin M.D., Doonan P.J., et al. Mitochondrial complex II prevents hypoxic but not calcium- and proapoptotic Bcl-2 protein-induced mitochondrial membrane potential loss. J Biol Chem 2010, 285(34):26494-26505.
24. Chinopoulos C., Gerencser A.A., Mandi M., et al. Forward operation of adenine nucleotide translocase during F0F1-ATPase reversal: critical role of matrix substrate-level phosphorylation. FASEB J 2010, 24:2405-2416.
25. ° cells. J Biol Chem 1998, 273(36):22983-22989.
26. Brown S.V., Hosking P., Li J., Williams N. ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryot Cell 2006, 5(1):45-53.
27. Tupper J.T., Tedeschi H. Microelectrode studies on the membrane properties of isolated mitochondria. Proc Natl Acad Sci USA 1969, 63:370-377.
28. Lemasters J.J., Ramshesh V.K. Imaging of mitochondrial polarization and depolarization with cationic fluorophores. Methods Cell Biol 2007, 80:283-295.
29. Tyner K.M., Kopelman R., Philbert M.A. Nanosized voltmeter" enables cellular-wide electric field mapping. Biophys J 2007, 93:1163-1174.
30. Gerencser A.A., Chinopoulos C., Birket M.J., et al. Quantitative measurement of mitochondrial membrane potential in cultured cells: calcium-induced de- and hyperpolarization of neuronal mitochondria. J Physiol 2012, 590(12):2845-2871.
31. Nicholls D.G. Mitochondrial membrane potential and aging. Aging Cell 2004, 1:35-40.
32. Alberts B.D., Bray D., Lewis J., Raff M., Roberts K., Watson J.D. Molecular biology of the cell 1994, Garland Publishing, New York, NY. 3rd ed.
33. Petita C., Pietri-Rouxela F., Lesneb A., et al. Oxygen consumption by cultured human cells is impaired by a nucleoside analogue cocktail that inhibits mitochondrial DNA synthesis. Mitochondrion 2005, 5:154-161.
34. Arvier M., Lagoutte L., Johnson G., et al. Adenine nucleotide translocator promotes oxidative phosphorylation and mild uncoupling in mitochondria after dexamethasone treatment. Am J Physiol - Endocrinol Metab 2007, 293:E1320-E1324.
35. Hayakawa Y., Nemoto T., Iino M., Kasai H. Rapid Ca2+-dependent increase in oxygen consumption by mitochondria in single mammalian central neurons. Cell Calcium 2005, 37:359-370.
36. Fabbri F., Carloni S., Brigliadori G., Zoli W., Lapalombella R., Marini M. Sequential events of apoptosis involving docetaxel, a microtubule-interfering agent: a cytometric study. BMC Cell Biol 2006, 7:6.
37. Olsen L.F., Andersen A.Z., Lunding A., Brasen J.C., Poulsen A.K. Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases. Biophys J 2009, 96:3850-3861.
38. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997, 416(1):15-18.
39. Labajova A., Vojtiskova A., Krivakova P., Kofranek J., Drahota Z., Houstek J. Evaluation of mitochondrial membrane potential using a computerized device with a tetraphenylphosphonium-selective electrode. Anal Biochem 2006, 353:37-42.
40. Heerdt B.G., Houston M.A., Augenlicht L.H. Growth properties of colonic tumor cells are a function of the intrinsic mitochondrial membrane potential. Cancer Res 2006, 66(3):1591-1596.
41. Houston M.A., Augenlicht L.H., Heerdt B.G. Stable differences in intrinsic mitochondrial membrane potential of tumor cell subpopulations reflect phenotypic heterogeneity. Int J Cell Biol 2011, 2011:978583.
42. Kurz F.T., Aon M.A., O'Rourke B., Armoundas A.A. Wavelet analysis reveals heterogeneous time-dependent oscillations of individual mitochondria. Am J Physiol - Heart Circ Physiol 2010, 299:H1736-H1740.
43. Smith T.A.D., Blaylock M.G. Treatment of breast tumor cells in vitro with the mitochondrial membrane potential dissipater valinomycin increases 18F-FDG incorporation. J Nucl Med 2007, 48(8):1308-1312.
44. Crider B.P., Carper S.W., Lancaster J.R. Electron transfer-driven ATP synthesis in Methanococcus voltae is not dependent on a proton electrochemical gradient. Proc Natl Acad Sci USA 1985, 82:6793-6796.
45. Lemeshko V.V., Anishkin A.G. Mathematical simulation of energy coupling in mitochondria within the framework of the proton-chemical hypothesis. Biophysics 1998, 43(2):285-291.
46. Dimroth P., Kaim G., Matthey U. Crucial role of the membrane potential for ATP synthesis by F1F0 ATP synthases. J Exp Biol 2000, 203:51-59.
47. Papa S. Role of cooperative H+/e- linkage (Redox Bohr Effect) at Heme a/CuA and Heme a3/CuB in the proton pump of cytochrome c oxidase. Biochemistry (Moscow) 2005, 70(2):178-186.
48. Richter O.-M.H., Ludwig B. Electron transfer and energy transduction in the terminal part of the respiratory chain - lessons from bacterial model systems. Biochim Biophys Acta 2009, 1787:626-634.
49. Vojtísková A., Jesina P., Kalous M., et al. Mitochondrial membrane potential and ATP production in primary disorders of ATP synthase. Toxicol Mech Methods 2004, 14(1-2):7-21.
50. Galati D., Srinivasan S., Raza H., et al. Role of nuclear-encoded subunit Vb in the assembly and stability of cytochrome c oxidase complex: implications in mitochondrial dysfunction and ROS production. Biochem J 2009, 420:439-449.
51. Yu M.A., Egawa T., Shinzawa-Itoh K., et al. Radical formation in cytochrome c oxidase. Biochim Biophys Acta 2011, 1807:1295-1304.
52. Moyler J., Mitchell P. Cytochrome c oxidase is not a proton pump. FEBS Lett 1978, 88(2):268-272.
53. Wilson D.F., Fairs K. Evidence for a structural interaction between ATP synthetase and cytochrome c oxidase in mitochondria. Arch Biochem Biophys 1974, 163:491-497.
54. Qiu Z.-H., Yu L., Yu C.-A. Spin-label electron paramagnetic resonance and differential scanning calorimetry studies of the interaction between mitochondrial cytochrome oxidase and adenosine triphosphate synthase complex. Biochemistry 1992, 31:3297-3302.
55. Liu X., Gong X., Hicks D.B., Krulwich T.A., Yu L., Yu C.-A. Interaction between cytochrome caa3 and F1F0-ATP synthase of alkaliphilic Bacillus pseudofirmus OF4 is demonstrated by saturation transfer electron paramagnetic resonance and differential scanning calorimetry assays. Biochemistry 2007, 46:306-313.
56. Mulkidjanian A.Y. Proton in the well and through the desolvation barrier. Biochim Biophys Acta 2006, 1757:415-427.
57. Newman J. Electric current and cell membranes. Physics of the life sciences 2008, Springer Science.
58. Neukirch S., Goriely A., Hausrath A.C. Elastic coiled-coils act as energy buffers in the ATP synthase. Int J Non-Linear Mech 2008, 43:1064-1073.
59. Efremov R.G., Sazanov L.A. The coupling mechanism of respiratory complex I - a structural and evolutionary perspective. Biochim Biophys Acta 2012, 1817:1785-1795.
60. Egawa T., Yeh S.R., Rousseau D.L. Redox-controlled proton gating in bovine cytochrome c oxidase. PLoS One 2013, 8(5):e63669.
61. Maréchal A., Rich P.R. Water molecule reorganization in cytochrome c oxidase revealed by FTIR spectroscopy. Proc Natl Acad Sci USA 2011, 108:8634-8638.
62. Wikstrom M.K.F. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature 1977, 266:271-273.
63. Allchin D. Cellular and theoretical chimeras: piecing together how cells process energy. Stud Hist Philos Sci 1996, 27(1):31-41.
64. Yoshikawa S., Muramoto K., Shinzawa-Itoh K. Proton-pumping mechanism of cytochrome c oxidase. Annu Rev Biophys 2011, 40:205-223.
65. Grinius L.L., Jasaitis A.A., Kadziauskas Y.P., et al. Conversion of biomembrane-produced energy into electric form. Biochim Biophys Acta 1970, 216:1-12.
66. Appleby R.D., Porteous W.K., Hughes G., et al. Quantitation and origin of the mitochondrial membrane potential in human cells lacking mitochondrial DNA. Eur J Biochem 1999, 262:108-116.
67. Baracca A., Barogi S., Carelli V., Lenaz G., Solaini G. Catalytic activities of mitochondrial ATP synthase in patients with mitochondrial DNA T8993G mutation in the ATPase 6 gene encoding subunit a. J Biol Chem 2000, 275(6):4177-4182.
68. Allemann N., Schneider A. ATP production in isolated mitochondria of procyclic Trypanosoma brucei. Mol Biochem Parasitol 2000, 111:87-94.
69. Almeida A., Almeida J., Bolanos J.P., Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA 2001, 98(26):15294-15299.
70. Wigdal S.S., Kirkland R.A., Franklin J.L., Haak-Frendscho M. Cytochrome c release precedes mitochondrial membrane potential loss in cerebellar granule neuron apoptosis: lack of mitochondrial swelling. J Neurochem 2002, 82:1029-1038.
71. Abramov A.Y., Smulders-Srinivasan T.K., Kirby D.M., et al. Mechanism of neurodegeneration of neurons with mitochondrial DNA mutations. Brain 2010, 133:797-807.
72. Huber H.J., Dussmann H., Kilbride S.M., Rehm M., Prehn J.H.M. Glucose metabolism determines resistance of cancer cells to bioenergetic crisis after cytochrome-c release. Mol Syst Biol 2011, 7:470.
73. Hirata H., Ohno K., Sone N., Kagawa Y., Hamamoto T. Direct measurement of the electrogenicity of the H+-ATPase from thermophilic bacterium PS3 reconstituted in planar phospholipid bilayers. J Biol Chem 1986, 261(21):9839-9843.
74. Christensen B., Cutweiler M., Grell E., et al. Pump and displacement currents of reconstituted ATP synthase on black lipid membranes. J Membr Biol 1988, 104:179-191.
75. Tadini-Buoninsegni F., Bartolommei G., Moncelli M.R., Pilankatta R., Lewis D., Inesi G. ATP dependent charge movement in ATP7B Cu+-ATPase is demonstrated by pre-steady state electrical measurements. FEBS Lett 2010, 584:4619-4622.
76. Okuno D., Iino R., Noji H. Rotation and structure of FoF1-ATP synthase. J Biochem 2011, 149(6):655-664.
77. Mnatsakanyan N., Hook J.A., Quisenberry L., Weber J. ATP synthase with its γ subunit reduced to the N-terminal helix can still catalyze ATP synthesis. J Biol Chem 2009, 284(39):26519-26525.
78. Wei Meng H. Single molecule characterisation of ATP synthase [Ph.D. thesis]. St Cross College, Oxford University; 2010.
79. Fillingame R.H., Jiang W., Dmitriev O.Y. The oligomeric subunit c rotor in the Fo sector of ATP synthase: unresolved questions in our understanding of function. J Bioenerg Biomembr 2000, 32:433-439.
80. Urachev L.A., Jasaitis A.A., Mikelsaar H., et al. Reconstitution of Biological molecular generators of electric current H+-ATPase. J Biol Chem 1976, 251(22):7077-7082.
81. Sundaresan V.B., Sarles S.A., Leo D.J. Stack of biocells converting ATP to electrical power and possible applications. MRS Proc 2006, 950. 0950-D01-03. 10.1557/PROC-0950-D01-03.
82. Liua X., Cuib Y., Chenc C., Laib B., Yueb J., Zhang Z. Preliminary estimation of rotary torque produced by proton-motive force in fully functional F0F1-ATPase. Protein Pept Lett 2007, 14:45-50.
83. Vollmar M. Crystallisation and structure solution of the c-ring of F0F1 ATP synthase from spinach chloroplasts [Ph.D. thesis]. Heinrich-Heine-Universität Düsseldorf; 2009.
84. Rappaport F., Finazzi G., Pierre Y., Bennoun P. A new electrochemical gradient generator in thylakoid membranes of green algae. Biochemistry 1999, 38:2040-2047.
85. Burzik C., Kaim G., Dimroth P., Bamberg E., Fendler K. Charge displacements during ATP-hydrolysis and synthesis of the Na+-transporting F0F1-ATPase of Ilyobacter tartaricus. Biophys J 2003, 85:2044-2054.
86. Brustovetsky N., Becker A., Klingenberg M., Bamberg E. Electrical currents associated with nucleotide transport by the reconstituted mitochondrial ADP/ATP carrier. Proc Natl Acad Sci USA 1996, 93:664-668.
87. Watzke N., Diekert K., Obrdlik P. Electrophysiology of respiratory chain complexes and the ADP-ATP exchanger in native mitochondrial membranes. Biochemistry 2010, 49:10308-10318.
88. Falchi A.M., Isola R., Diana A., Putzolu M., Diaz G. Characterization of depolarization and repolarization phases of mitochondrial membrane potential fluctuations induced by tetramethylrhodamine methyl ester photoactivation. FEBS J 2005, 272:1649-1659.
89. Aon M.A., Cortassa S., O'Rourke B. Redox-optimized ROS balance: a unifying hypothesis. Biochim Biophys Acta 2010, 1797:865-877.
90. Esteve-Núñez A., Sosnik J., Visconti P., Lovley D.R. Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ Microbiol 2008, 10(2):497-505.
91. Schrotta G.D., Bonannia P.S., Robuschia L., Esteve-Nunez A., Busalmena J.P. Electrochemical insight into the mechanism of electron transport in biofilms of Geobacter sulfurreducens. Electrochim Acta 2011, 56:10791-10795.
92. Uría N., Berbel X.M., Sanchez O., Munoz F.X., Mas J. Transient storage of electrical charge in biofilms of Shewanella oneidensis MR-1 growing in a microbial fuel cell. Environ Sci Technol 2011, 45:10250-10256.
93. Haltia T., Saraste M., Wikstrom M. Subunit III of cytochrome c oxidase is not involved in proton translocation: a site-directed mutagenesis study. EMBO J 1991, 10(8):2015-2021.
94. Horváth R., Scharfe C., Hoeltzenbein M., et al. Childhood onset mitochondrial myopathy and lactic acidosis caused by a stop mutation in the mitochondrial cytochrome c oxidase III gene. J Med Genet 2002, 39:812-816.
95. Bornhövd C., Vogel F., Neupert W., Reichert A.S. Mitochondrial membrane potential is dependent on the oligomeric state of F1F0-ATP synthase supracomplexes. J Biol Chem 2006, 281:13990-13998.
96. Seelert H., Dencher N.A. ATP synthase superassemblies in animals and plants: two or more are better. Biochim Biophys Acta 2011, 1807:1185-1197.