Beyond the chemiosmotic theory: Analysis of key fundamental aspects of energy coupling in oxidative phosphorylation in the light of a torsional mechanism of energy transduction and ATP synthesis-invited review part 1

Journal of Bioenergetics and Biomembranes

Volumn 42, Issue 4, 2010, Pages 293-300

  Nath, Sunil ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

Author keywords

Bioenergetics; Chemiosmotic theory; Coupling; Electrogenic; Electroneutral; Energy transduction; F1FO ATP synthase; Membrane and ion transport; Mitochondria; Oxidative Phosphorylation; Photosynthesis and photophosphorylation; Torsional mechanism; Uncoupler; Unified theory of ATP synthesis and hydrolysis; Valinomycin

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANION; POTASSIUM ION; PROTON; VALINOMYCIN;

ELECTRON TRANSPORT; ENERGY TRANSFER; EQUILIBRIUM CONSTANT; MITOCHONDRION; OSMOSIS; OXIDATIVE PHOSPHORYLATION; PH; REVIEW; SYNTHESIS; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, BIOLOGICAL; OXIDATIVE PHOSPHORYLATION; PROTON-MOTIVE FORCE; THERMODYNAMICS;

EID: 77956057554     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-010-9296-5     Document Type: Review

References (65)

1. GF Azzone S Massari 1971 Thermodynamic and kinetic aspects of interconversion of chemical and osmotic energies in mitochondria Eur J Biochem 19 97 107 10.1111/j.1432-1033.1971.tb01292.x
2. 1-ATPase: Configuration of a critical intermediate in ATP synthesis/hydrolysis Proc Natl Acad Sci USA 95 11065 11070 10.1073/pnas.95.19.11065
3. PD Boyer 1993 The binding change mechanism for ATP synthase-some probabilities and possibilities Biochim Biophys Acta 1140 215 250 10.1016/0005-2728(93)90063-L
4. B Chance L Mela 1966 A hydrogen ion concentration gradient in a mitochondrial membrane Nature 212 369 372 10.1038/212369a0
5. i and ADP/ATP J Biol Chem 279 31761 31768 10.1074/jbc.M401353200
6. RE Davies HA Krebs 1952 The biochemical aspects of the transport of ions by nervous tissue Biochem Soc Symp 8 77 92
7. SJ Decker DR Lang 1978 Membrane bioenergetic parameters in uncoupler-resistant mutants of Bacillus megaterium J Biol Chem 253 6738 6743
8. C Deutsch M Erecinska R Werrlein IA Silver 1979 Cellular energy metabolism, trans-plasma and trans-mitochondrial membrane potentials, and pH gradients in mouse neuroblastoma Proc Natl Acad Sci USA 76 2175 2179 10.1073/pnas.76.5.2175
9. SJ Ferguson MC Sorgato 1982 Proton electrochemical gradients and energy-transduction processes Annu Rev Biochem 51 185 217 10.1146/annurev.bi.51. 070182.001153
10. DE Green 1981 A critique of the chemiosmotic model of energy coupling Proc Natl Acad Sci USA 78 2240 2243 10.1073/pnas.78.4.2240
11. Griffiths DE, Avner PR, Lancashire WE, Turner JR (1972) Study of energy-linked reactions: isolation and properties of mitochondrial oligomycin-resistant, trialkyl tin-resistant and uncoupler-resistant mutants of yeast. In: Azzone GF, Carafoli E, Lehninger AL, Quagliariello E, Siliprandi N (eds) Biochemistry and biophysics of mitochondrial membranes. Academic, New York, p 505
12. Griffiths DE, Houghton RL, Lancashire WE (1974) Mitochondrial genes and ATP-synthetase. In: Kroon AM, Saccone C (eds) The biogenesis of mitochondria. Academic, New York, p 215
13. AA Guffanti H Blumenfeld TA Krulwich 1981 ATP synthesis by an uncoupler-resistant mutant of Bacillus megaterium J Biol Chem 256 8416 8421
14. U Hansen D Gradmann D Sanders CL Slayman 1981 Interpretation of current-voltage relationships for "active" ion transport systems: I. Steady-state reaction-kinetic analysis of class-I mechanisms J Membr Biol 63 165 190 10.1007/BF01870979
15. WG Hanstein Y Hatefi 1974 Trinitrophenol: A membrane-impermeable uncoupler of oxidative phosphorylation Proc Natl Acad Sci USA 71 288 292 10.1073/pnas.71.2.288
16. WG Hanstein Y Hatefi 1974 Characterization and localization of mitochondrial uncoupler binding sites with an uncoupler capable of photoaffinity labeling J Biol Chem 249 1356 1362
17. S Jain S Nath 2000 Kinetic model of ATP synthase: pH dependence of the rate of ATP synthesis FEBS Lett 476 113 117 10.1016/S0014-5793(00)01716-6
18. S Jain S Nath 2001 Catalysis by ATP synthase: Mechanistic, kinetic and thermodynamic characteristics Thermochim Acta 378 35 44 10.1016/S0040-6031(01) 00628-1
19. S Jain R Murugavel LD Hansen 2004 ATP synthase and the torsional mechanism: Resolving a 50-year-old mystery Curr Sci 87 16 19
20. 1-ATPase Nature 459 364 370 10.1038/nature08145
21. DB Kell 1979 On the functional proton current pathway of electron transport phosphorylation: An electrodic view Biochim Biophys Acta 549 55 79
22. Lehninger AL (1964) The mitochondrion. Benjamin, New York
23. F Lipmann 1941 Metabolic generation and utilization of phosphate bond energy Adv Enzymol 1 99 162
24. + fluxes Eur J Biochem 12 301 309 10.1111/j.1432-1033.1970.tb00851.x
25. 2+ and tetrapropylammonium in steady-state mitochondria Arch Biochem Biophys 173 332 340 10.1016/0003-9861(76)90267-8
26. S Massari E Balboni GF Azzone 1972 Distribution of permeant cations in rat liver mitochondria under steady state conditions Biochim Biophys Acta 283 16 22 10.1016/0005-2728(72)90093-X
27. 1-ATPase with nucleotide bound to all three catalytic sites: Implications for the mechanism of rotary catalysis Cell 106 331 341 10.1016/S0092-8674(01)00452-4
28. P Mitchell 1961 Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 144 148 10.1038/191144a0
29. P Mitchell 1966 Chemiosmotic coupling in oxidative and photosynthetic phosphorylation Biol Rev 41 445 502 10.1111/j.1469-185X.1966.tb01501.x
30. P Mitchell 1979 Keilin's respiratory chain concept and its chemiosmotic consequences Science 206 1148 1159 10.1126/science.388618
31. P Mitchell J Moyle 1969 Estimation of membrane potential and pH difference across the cristae membrane of rat liver mitochondria Eur J Biochem 7 471 484 10.1111/j.1432-1033.1969.tb19633.x
32. HJ Morowitz 1978 Proton semiconductors and energy transduction in biological systems Am J Physiol 235 R99 R114
33. Nath S (1994) A fundamental thermodynamic principle for coupling in oxidative phosphorylation. In Proceedings of the Sixteenth International Congress of Biochemistry and Molecular Biology, New Delhi, Vol. II, p 390
34. Nath S (1997) A thermodynamic principle for the coupled nonequilibrium processes of ATP synthesis. In Proceedings of the ISBC X, The International Society for Biological Calorimetry, Monte Verità, p i9
35. S Nath 1998 A thermodynamic principle for the coupled bioenergetic processes of ATP synthesis Pure Appl Chem 70 639 644 10.1351/pac199870030639
36. S Nath 1999 Surface tension of nonideal binary liquid mixtures as a function of composition J Coll Interface Sc 209 116 122 10.1006/jcis.1998.5873
37. 0-ATP synthase: A scrutiny of the major possibilities Adv Biochem Eng Biotechnol 74 65 98
38. S Nath 2003 Molecular mechanisms of energy transduction in cells: Engineering applications and biological implications Adv Biochem Eng Biotechnol 85 125 180
39. S Nath 2004 The torsional mechanism of energy transduction and ATP synthesis as a breakthrough in our understanding of the mechanistic, kinetic and thermodynamic details Thermochim Acta 422 5 17 10.1016/j.tca.2004.08.004
40. S Nath 2006 A novel systems biology/engineering approach solves fundamental molecular mechanistic problems in bioenergetics and motility Process Biochem 41 2218 2235 10.1016/j.procbio.2006.07.003
41. S Nath 2008 The new unified theory of ATP synthesis/hydrolysis and muscle contraction, its manifold fundamental consequences and mechanistic implications and its applications in health and disease Int J Mol Sci 9 1784 1840 10.3390/ijms9091784
42. S Nath S Jain 2000 Kinetic modeling of ATP synthesis by ATP synthase and its mechanistic implications Biochem Biophys Res Commun 272 629 633 10.1006/bbrc.2000.2774
43. 0 portion of ATP synthase reveals a non-chemiosmotic mode of energy coupling Thermochim Acta 394 89 98 10.1016/S0040-6031(02)00242-3
44. SS Nath S Nath 2009 Energy transfer from adenosine triphosphate: Quantitative analysis and mechanistic implications J Phys Chem B 113 1533 1537 10.1021/jp809678n
45. S Nath V Shishodia 1993 Surface tension of nonelectrolyte solutions J Coll Interface Sc 156 498 503 10.1006/jcis.1993.1143
46. S Nath H Rohatgi A Saha 1999 The torsional mechanism of energy transfer in ATP synthase Curr Sci 77 167 169
47. S Nath H Rohatgi A Saha 2000 The catalytic cycle of ATP synthesis by means of a torsional mechanism Curr Sci 78 23 27
48. J Prebble 2002 Peter Mitchell and the ox phos wars Trends Biochem Sci 27 209 212 10.1016/S0968-0004(02)02059-5
49. BC Pressman EJ Harris WS Jagger JH Johnson 1967 Antibiotic-mediated transport of alkali ions across lipid barriers Proc Natl Acad Sci USA 58 1949 1956 10.1073/pnas.58.5.1949
50. ME Pullman HS Penefsky A Datta E Racker 1960 Partial resolution of the enzymes catalyzing oxidative phosphorylation. I. Purification and properties of soluble dinitrophenol-stimulated adenosine triphosphatase J Biol Chem 235 3322 3329
51. B Reynafarje A Alexandre P Davies AL Lehninger 1982 Proton translocation stoichiometry of cytochrome oxidase: Use of a fast-responding oxygen electrode Proc Natl Acad Sci USA 79 7218 7222 10.1073/pnas.79.23.7218
52. H Rohatgi A Saha S Nath 1998 Mechanism of ATP synthesis by protonmotive force Curr Sci 75 716 718
53. H Rottenberg AK Solomon 1969 The osmotic nature of the ion-induced swelling of rat-liver mitochondria Biochim Biophys Acta 193 48 57 10.1016/0005-2736(69)90057-1
54. 0-ATP synthase Biochim Biophys Acta 1553 188 211 10.1016/S0005-2728(02)00185-8
55. EC Slater 1953 Mechanism of phosphorylation in the respiratory chain Nature 172 975 978 10.1038/172975a0
56. EC Slater 1987 The mechanism of the conservation of energy of biological oxidations Eur J Biochem 166 489 504 10.1111/j.1432-1033.1987.tb13542.x
57. EC Slater J Rosing A Mol 1973 The phosphorylation potential generated by respiring mitochondria Biochim Biophys Acta 292 534 553 10.1016/0005-2728(73) 90003-0
58. D Stock AGW Leslie JE Walker 1999 Molecular architecture of the rotary motor in ATP synthase Science 286 1700 1705 10.1126/science.286.5445.1700
59. H Tedeschi 2005 Old and new data, new issues: The mitochondrial ΔΨ Biochim Biophys Acta 1709 195 202 10.1016/j.bbabio.2005.07.008
60. JT Tupper H Tedeschi 1969 Mitochondrial membrane potentials measured with microelectrodes: Probable ionic basis Science 166 1539 1540 10.1126/science.166.3912.1539
61. HV Westerhoff BA Melandri G Venturoli GF Azzone DB Kell 1984 A minimal hypothesis for membrane-linked free-energy transduction: The role of independent, small coupling units Biochim Biophys Acta 768 257 292
62. RJP Williams 1961 Possible functions of chains of catalysts J Theor Biol 1 1 17 10.1016/0022-5193(61)90023-6
63. RJP Williams 1962 Possible functions of chains of catalysts II J Theor Biol 3 209 229 10.1016/S0022-5193(62)80015-0
64. RJP Williams 1979 Some unrealistic assumptions in the theory of chemi-osmosis and their consequences FEBS Lett 102 126 132 10.1016/0014-5793(79) 80943-6
65. DF Wilson HP Ting MS Koppelman 1971 Mechanism of action of uncouplers of oxidative phosphorylation Biochemistry 10 2897 2902 10.1021/bi00791a016