Essentials for ATP synthesis by F1F0 ATP synthases

Annual Review of Biochemistry

Volumn 78, Issue , 2009, Pages 649-672

  Von Ballmoos, Christoph ^a   Wiedenmann, Alexander ^b   Dimroth, Peter ^c  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

ATP synthase assembly; Coupling ion coordination; Driving forces; Torque generation

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

CATALYSIS; CONFORMATIONAL TRANSITION; ENERGY METABOLISM; ENZYME ANALYSIS; HUMAN; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNTHESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTERIA; HUMANS; PROTON-TRANSLOCATING ATPASES;

EID: 67650738933     PISSN: 00664154     EISSN: 00664154     Source Type: Book Series    
DOI: 10.1146/annurev.biochem.78.081307.104803     Document Type: Review

References (101)

1. Saraste M. 1999. Oxidative phosphorylation at the fin de siecle. Science 283:1488-93
2. +-coupled ATP synthases operating at low electrochemical potential. Adv. Microb. Physiol. 49:175-218
3. Dimroth P, von Ballmoos C. 2008. ATP synthesis by decarboxylation phosphorylation. Results Probl. Cell Differ. 45:153-84
4. 1-ATPase from bovine heart mitochondria. Nature 370:621-28
5. Boyer PD. 1993. The binding change mechanism for ATP synthase - some probabilities and possibilities. Biochim. Biophys. Acta 1140:215-50
6. 1-ATPase. Nature 386:299-302
7. 1. FEBS Lett. 472:34-38
8. 0). Biochem. Soc. Trans. 23:767-70
9. 1-ATPase. Proc. Natl. Acad. Sci. USA 92:10964-68
10. 1 ATPase revealed by cryoelectron microscopy. Proc. Natl. Acad. Sci. USA 87:9585-89
11. 1-ATPase. Proc. Natl. Acad. Sci. USA 94:4401-5
12. Stock D, Leslie AG, Walker JE. 1999. Molecular architecture of the rotary motor in ATP synthase. Science 286:1700-5
13. 1 enzyme complexes during ATP synthesis or hydrolysis. FEBS Lett. 525:156-63
14. 1-ATP synthase. Nat. Struct. Mol. Biol. 11:135-41
15. 1-ATP synthase. Proc. Natl. Acad. Sci. USA 102:1333-38
16. 1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Mol. Biol. 11:142-48
17. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130:309-21
18. 1-ATPase single molecules. Nature 433:773-77
19. 1-ATPase. Nature 427:465-68
20. 0 ATP synthase. J. Biol. Chem. 273:16241-47
21. Vik SB, Ishmukhametov RR. 2005. Structure and function of subunit a of the ATP synthase of Escherichia coli. J. Bioenerg. Biomembr. 37:445-49
22. Dunn S, Revington M, Cipriano D, Shilton B. 2000. The b subunit of Escherichia coli ATP synthase. J. Bioenerg. Biomembr. 32:347-55
23. 0 complex from Escherichia coli ATP synthase. J. Bioenerg. Biomembr. 32:357-64
24. 0-ATP synthase. J. Biol. Chem. 279:11253-58
25. Weber J. 2007. ATP synthase-the structure of the stator stalk. Trends Biochem. Sci. 32:53-56
26. Dickson VK, Silvester JA, Fearnley IM, Leslie AG, Walker JE. 2006. On the structure of the stator of the mitochondrial ATP synthase. EMBO J. 25:2911-18
27. Ackerman SH, Tzagoloff A. 2005. Function, structure, and biogenesis of mitochondrial ATP synthase. Prog. Nucleic Acid Res. Mol. Biol. 80:95-133
28. von Meyenburg K, Jorgensen BB, Nielsen J, Hansen FG. 1982. Promoters of the atp operon coding for the membrane-bound ATP synthase of Escherichia coli mapped by Tn10 insertion mutations. Mol. Gen. Genet. 188:240-48
29. Gay NJ. 1984. Construction and characterization of an Escherichia coli strain with a uncI mutation. J. Bacteriol. 158:820-25
30. 0-ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc. Natl. Acad. Sci. USA 104:20776-81
31. 11 ring stoichiometry in the sodium F-ATP synthase. FEBS J. 272:5474-83
32. Kol S, Nouwen N, Driessen AJ. 2008. Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes. J. Biol. Chem. 283:31269-73
33. 1-ATP synthase in vitro. Biochem. Biophys. Res. Commun. 367:663-66
34. Pogoryelov D, Nikolaev Y, Schlattner U, Pervushin K, Dimroth P, Meier T. 2008. Probing the rotor subunit interface of the ATP synthase from Ilyobacter tartaricus. FEBS J. 275:4850-62
35. 0 in functionally assembled Escherichia coli ATP synthase. J. Biol. Chem. 280:33338-45
36. Meier T, Morgner N, Matthies D, Pogoryelov D, Keis S, et al. 2007. A tridecameric c ring of the adenosine triphosphate (ATP) synthase from the thermoalkaliphilic Bacillus sp. strain TA2.A1 facilitates ATP synthesis at low electrochemical proton potential. Mol. Microbiol. 65:1181-92
37. Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H, Müller DJ. 2000. Structural biology. Proton-powered turbine of a plant motor. Nature 405:418-19
38. 0-ATP synthase from thermoalkaliphilic Bacillus sp. strainTA2.A1. J. Bacteriol. 185:4442-49
39. von Ballmoos C, Cook GM, Dimroth P. 2008. Unique rotary ATP synthase and its biological diversity. Annu. Rev. Biophys. 37:43-64
40. Tomashek JJ, Brusilow WS. 2000. Stoichiometry of energy coupling by proton-translocating ATPases: a history of variability. J. Bioenerg. Biomembr. 32:493-500
41. Krebstakies T, Aldag I, Altendorf K, Greie JC, Deckers-Hebestreit G. 2008. The stoichiometry of subunit c of Escherichia coli ATP synthase is independent of its rate of synthesis. Biochemistry 47:6907-16
42. Meyer Zu,Tittingdorf JM, Rexroth S, Schäfer E, Schlichting R, Giersch C, et al. 2004. The stoichiometry of the chloroplast ATP synthase oligomer III in Chlamydomonas reinhardtii is not affected by the metabolic state. Biochim. Biophys. Acta 1659:92-99
43. Hinkle PC. 2005. P/O ratios of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 1706:1-11
44. +/ATP ratios of the H+-ATP synthases from chloroplasts and Escherichia coli. Proc. Natl. Acad. Sci. USA 105:3745-50
45. Toei M, Gerle C, Nakano M, Tani K, Gyobu N, et al. 2007. Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proc. Natl. Acad. Sci. USA 104:20256-61
46. +-ATPase from Ilyobacter tartaricus. Science 308:659-62
47. +-ATP synthase. J. Mol. Biol. 321:307-16
48. +-ATPase from Enterococcus hirae. Science 308:654-59
49. Oberfeld B, Brunner J, Dimroth P. 2006. Phospholipids occupy the internal lumen of the c ring of the ATP synthase of Escherichia coli. Biochemistry 45:1841-51
50. 0 ATP synthase. J. Biol. Chem. 277:3504-10
51. +-ATPase in Enterococcus hirae. J. Biol. Chem. 275:13415-19
52. Dimroth P, von Ballmoos C, Meier T. 2006. Catalytic and mechanical cycles in F-ATP synthases. Fourth in the Cycles Review Series. EMBO Rep. 7:276-82
53. Engelbrecht S, Junge W. 1997. ATP synthase: a tentative structural model. FEBS Lett. 414:485-91
54. 0 ATP synthases suggested by double mutants of the a subunit. J. Biol. Chem. 269:30364-69
55. Fillingame RH, Angevine CM, Dmitriev OY. 2003. Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 555:29-34
56. von Ballmoos C, Dimroth P. 2007. Two distinct proton binding sites in the ATP synthase family. Biochemistry 46:11800-9
57. Boyer PD. 1988. Bioenergetic coupling to protonmotive force: Should we be considering hydronium ion coordination and not group protonation? Trends Biochem. Sci. 13:5-7
58. Mellwig C, Böttcher B. 2003. A unique resting position of the ATP-synthase from chloroplasts. J. Biol. Chem. 278:18544-49
59. Rubinstein JL,Walker JE, Henderson R. 2003. Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J. 22:6182-92
60. +-translocating activity together with subunits a and c. Eur. J. Biochem. 271:3036-42
61. 0 complex of Escherichia coli ATP synthase by forming an ab2 subcomplex. J. Biol. Chem. 278:27068-71
62. 2-subunits as an anchor rail of a rotating c-ring. J. Biol. Chem. 279:33409-12
63. 0 ATPase of Escherichia coli. Mutagenic analysis of the a-subunit. J. Biol. Chem. 264:3292-300
64. 0 motor probed by mutational analyses of subunit a. J. Mol. Biol. 322:369-81
65. Elston T,Wang H, Oster G. 1998. Energy transduction in ATP synthase. Nature 391:510-13
66. 0 motor of the sodium ATPase. Biophys. J. 87:2148-63
67. 0-ATPase in Escherichia coli. J. Biol. Chem. 263:6606-12
68. Schwem BE, Fillingame RH. 2006. Cross-linking between helices within subunit a of Escherichia coli ATP synthase defines the transmembrane packing of a four-helix bundle. J. Biol. Chem. 281:37861-67
69. Angevine CM, Herold KA, Fillingame RH. 2003. Aqueous access pathways in subunit a of rotary ATP synthase extend to both sides of the membrane. Proc. Natl. Acad. Sci. USA 100:13179-83
70. Angevine CM, Fillingame RH. 2003. Aqueous access channels in subunit a of rotary ATP synthase. J. Biol. Chem. 278:6066-74
71. Meier T, Matthey U, von Ballmoos C, Vonck J, Krug von Nidda T, et al. 2003. Evidence for structural integrity in the undecameric c-rings isolated from sodium ATP synthases. J. Mol. Biol. 325:389-97
72. 0 ATP synthases. Eur. J. Biochem. 269:5581-89
73. 0 ATP synthase of Escherichia coli defined by disulfide cross-linking. Proc. Natl. Acad. Sci. USA 95:6607-12
74. Rastogi VK, Girvin ME. 1999. Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402:263-68
75. +-translocation. J. Mol. Biol. 358:132-44
76. Vincent OD, Schwem BE, Steed PR, JiangW,Fillingame RH. 2007. Fluidity of structure and swiveling of helices in the subunit c ring of Escherichia coli ATP synthase as revealed by cysteine-cysteine cross-linking. J. Biol. Chem. 282:33788-94
77. Vorburger T, Zingg Ebneter J, Wiedenmann A, Morger D, Weber G, et al. 2008. Arginine-induced conformational change in the c-ring/a-subunit interface of ATP synthase. FEBS J. 275:2137-50
78. + concentration: probing the binding site for the coupling ions. Biochemistry 32:10378-86
79. Hoppe J, Schairer HU, Sebald W. 1980. Identification of amino-acid substitutions in the proteolipid subunit of the ATP synthase from dicyclohexylcarbodiimide-resistant mutants of Escherichia coli. Eur. J. Biochem. 112:17-24
80. 0 complex. J. Biol. Chem. 264:3896-903
81. de Jonge MR, Koymans LH, Guillemont JE, Koul A, Andries K. 2007. A computational model of the inhibition of Mycobacterium tuberculosis ATPase by a new drug candidate R207910. Proteins 67:971-80
82. Partis MD, Bertoli E, Griffiths DE, Azzi A. 1980. Interaction of the dibutylchloromethyltin chloride binding site with the carbodiimide binding site in mitochondria. Biochem. Biophys. Res. Commun. 96: 1103-8
83. von Ballmoos C, Brunner J, Dimroth P. 2004. The ion channel of F-ATP synthase is the target of toxic organotin compounds. Proc. Natl. Acad. Sci. USA 101:11239-44
84. 0 complexes of ATP synthases. Biochim. Biophys. Acta 1777:1301-10
85. Mitchell P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144-48
86. Jagendorf AT, Uribe E. 1966. ATP formation caused by acid-base transition of spinach chloroplasts. Proc. Natl. Acad. Sci. USA 55:170-77
87. Kaim G, Dimroth P. 1999. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J. 18:4118-27
88. Mitchell P. 1966. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. Camb. Philos. Soc. 41:445-502
89. Cockrell RS, Harris EJ, Pressman BC. 1967. Synthesis of ATP driven by a potassium gradient in mitochondria. Nature 215:1487-88
90. Maloney PC, Wilson TH. 1975. ATP synthesis driven by a protonmotive force in Streptococcus lactis. J. Membr. Biol. 25:285-310
91. Sone N, Yoshida M, Hirata H, Kagawa Y. 1977. Adenosine triphosphate synthesis by electrochemical proton gradient in vesicles reconstituted from purified adenosine triphosphatase and phospholipids of thermophilic bacterium. J. Biol. Chem. 252:2956-60
92. +-ATPases from Escherichia coli or chloroplasts reconstituted into liposomes. FEBS Lett. 457:327-32
93. Bokranz M, Morschel E, Kröger A. 1985. Phosphorylation and phosphate-ATP exchange catalyzed by the ATP synthase isolated from Wolinella succinogenes. Biochim. Biophys. Acta 810:332-39
94. Laubinger W, Dimroth P. 1988. Characterization of the ATP synthase of Propionigenium modestum as a primary sodium pump. Biochemistry 27:7531-37
95. Feniouk BA, Kozlova MA, Knorre DA, Cherepanov DA, Mulkidjanian AY, Junge W. 2004. The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating. Biophys. J. 86:4094-109
96. 0 ATPase from Propionigenium modestum: discovery of a membrane potential dependent step. Biochemistry 31:12665-72
97. Guffanti AA, Fuchs RT, Schneier M, Chiu E, Krulwich TA. 1984. A transmembrane electrical potential generated by respiration is not equivalent to a diffusion potential of the same magnitude forATP synthesis by Bacillus firmus RAB. J. Biol. Chem. 259:2971-75
98. Michel H, Oesterhelt D. 1980. Electrochemical proton gradient across the cell membrane of Halobacterium halobium: comparison of the light-induced increase with the increase of intracellular adenosine triphosphate under steady-state illumination. Biochemistry 19:4615-19
99. 1-ATP synthase. Results Probl. Cell Differ. 45:279-308
100. Bowler MW, Montgomery MG, Leslie AG,Walker JE. 2006. How azide inhibits ATP hydrolysis by the F-ATPases. Proc. Natl. Acad. Sci. USA 103:8646-49
101. 0 motor in bacterial ATP synthases. Mol. Microbiol. doi: 10.1111/j.1365-2958.2009.06658.x