Engineering rotor ring stoichiometries in the ATP synthase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 25, 2012, Pages

  Pogoryelov, Denys ^a   Klyszejko, Adriana L ^a,b   Krasnoselska, Ganna O ^a   Heller, Eva Maria ^a   Leone, Vanessa ^a   Langer, Julian D ^a   Vonck, Janet ^a   Müller, Daniel J ^c   Faraldo Gómez, José D ^a   Meier, Thomas ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c ETH ZURICH   (Switzerland)

Author keywords

Alpha helix packing; Bioenergetics; F 1F o ATP synthase; Membrane protein; Rotary motor stoichiometry

Indexed keywords

GLYCINE; ION; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; BACTERIAL CELL; BIOCHEMISTRY; BIOENERGY; CHEMICAL ENGINEERING; CHEMICAL INTERACTION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENERGY TRANSFER; ENZYME ENGINEERING; ENZYME STRUCTURE; ENZYME SYNTHESIS; FORCE; GEOMETRY; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROPIONIGENIUM MODESTUM; QUANTITATIVE ANALYSIS; SITE DIRECTED MUTAGENESIS; SPECTROSCOPY; STOICHIOMETRY; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; SYNECHOCOCCUS ELONGATUS;

ADENOSINE TRIPHOSPHATE; ATP SYNTHETASE COMPLEXES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEOLIPIDS; SURFACE PLASMON RESONANCE;

EID: 84862583909     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120027109     Document Type: Article

References (61)

1. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621-628.
2. 0ATP synthases. Annu Rev Biochem 78:649-672.
3. 1-ATPase. Nature 459:364-370.
4. 1-ATPase. Nature 386:299-302.
5. Iino R, Rondelez Y, Yoshida M, Noji H (2005) Chemomechanical coupling in single-molecule F-type ATP synthase. J Bioenerg Biomembr 37:451-454.
6. Boyer PD (1997) The ATP synthase - a splendid molecular machine. Annu Rev Biochem 66:717-749.
7. Stock D, Leslie AGW, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286:1700-1705.
8. 0 ATP synthase. Biochemistry 37:8817-8824.
9. Watt IN, Montgomery MG, Runswick MJ, Leslie AGW, Walker JE (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci USA 107:16823-16827.
10. osymmetry mismatch is not obligatory. EMBO Rep 6:1040-1044.
11. +- dependent F-ATP synthases. J Mol Biol 391:498-507.
12. Pogoryelov D, Yildiz Ö, Faraldo-Gómez JD, Meier T (2009) High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16:1068-1073.
13. o complex of ATP synthases. Nat Chem Biol 6:891-899.
14. Ferguson SJ (2010) ATP synthase: From sequence to ring size to the P/O ratio. Proc Natl Acad Sci USA 107:16755-16756.
15. MacKenzie KR, Prestegard JH, Engelman DM (1997) A transmembrane helix dimer: Structure and implications. Science 276:131-133.
16. +-ATP synthase. J Mol Biol 321:307-316.
17. +-ATPase from Ilyobacter tartaricus. Science 308:659-662.
18. o-ATP synthase rotor ring. PLoS Biol 8:e000443.
19. Liu J, Fujisawa M, Hicks DB, Krulwich TA (2009) Characterization of the functionally critical AXAXAXA and PXXEXXP motifs of the ATP synthase c-subunit from an alkaliphilic Bacillus. J Biol Chem 284:8714-8725.
20. 13 ring from a thermoalkaliphilic ATP synthase reveals an extended diameter due to a special structural region. J Mol Biol 388:611-618.
21. Fleming KG, Ackerman AL, Engelman DM (1997) The effect of point mutations on the free energy of transmembrane α-helix dimerization. J Mol Biol 272:266-275.
22. Pogoryelov D, et al. (2007) The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. J Bacteriol 189:5895-5902.
23. 11 ring stoichiometry in the sodium F-ATP synthase. FEBS J 272:5474-5483.
24. 0 ATP synthases. EMBO Rep 3: 1094-1098.
25. Müller DJ, et al. (2001) ATP synthase: Constrained stoichiometry of the transmembrane rotor. FEBS Lett 504:219-222.
26. +-ATP synthase has an undecameric rotor. EMBO Rep 2:229-233.
27. Meier T, Matthey U, Henzen F, Dimroth P, Müller DJ (2001) The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids. FEBS Lett 505:353-356.
28. o rotors. Biochim Biophys Acta 1797:763-772.
29. Pogoryelov D, et al. (2008) Probing the rotor subunit interface of the ATP synthase from Ilyobacter tartaricus. FEBS J 275:4850-4862.
30. Vorburger T, et al. (2008) Arginine-induced conformational change in the c-ring/a-subunit interface of ATP synthase. FEBS J 275:2137-2150.
31. o ATP synthase from Ilyobacter tartaricus and identification of the encoded subunits. Biochim Biophys Acta 1625:221-226.
32. Klionsky DJ, Brusilow WSA, Simoni RD (1984) In vivo evidence for the role of the εsubunit as an inhibitor of the proton-translocating ATPase of Escherichia coli. J Bacteriol 160:1055-1060.
33. 0 ATPase of Ilyobacter tartaricus, a sodium ion pump. J Bacteriol 180:3312-3316.
34. + translocation. Proc Natl Acad Sci USA 109:947-952.
35. Gemperli AC, Dimroth P, Steuber J (2003) Sodium ion cycling mediates energy coupling between complex I and ATP synthase. Proc Natl Acad Sci USA 100:839-844.
36. omotor in bacterial ATP synthases. Mol Microbiol 72:479-490.
37. Kaim G, Dimroth P (1999) ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18:4118-4127.
38. Senes A, Ubarretxena-Belandia I, Engelman DM (2001) The Calpha - H. . .O hydrogen bond: A determinant of stability and specificity in transmembrane helix interactions. Proc Natl Acad Sci USA 98:9056-9061.
39. 0 of Propionigenium modestum is a functional sodium ion pump. Biochemistry 29:5458-5463.
40. o-ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc Natl Acad Sci USA 104:20776-20781.
41. +/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proc Natl Acad Sci USA 104: 20256-20261.
42. +- ATP synthases from chloroplasts and Escherichia coli. Proc Natl Acad Sci USA 105: 3745-3750.
43. 0 ATPase of Escherichia coli. Arch Biochem Biophys 323:423-428.
44. 0 ATPase of Escherichia coli. J Bacteriol 180:3205-3208.
45. +- transporting ATP synthase. Functional dimers and trimers and determination of stoichiometry by cross-linking analysis. J Biol Chem 273:29701-29705.
46. Jiang W, Hermolin J, Fillingame RH (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc Natl Acad Sci USA 98:4966-4971.
47. +/ATP ratio and permissive elastic coupling. Proc Natl Acad Sci USA 101:12159-12164.
48. Meier T, 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 65:1181-1192.
49. o ATP synthase. FEBS J 275:1999-2007.
50. 10 ring stoichiometry in the Escherichia coli ATP synthase analyzed by cross-linking. J Bacteriol 191:2400-2404.
51. 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 47:6907-6916.
52. Arechaga I, Butler PJ, Walker JE (2002) Self-assembly of ATP synthase subunit c rings. FEBS Lett 515:189-193.
53. Crowther RA, Henderson R, Smith JM (1996) MRC image processing programs. J Struct Biol 116:9-16.
54. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763.
55. Müller DJ, Engel A (2007) Atomic force microscopy and spectroscopy of native membrane proteins. Nat Protoc 2:2191-2197.
56. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82-97.
57. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116:17-24.
58. Staritzbichler R, Anselmi C, Forrest LR, Faraldo-Gómez JD (2011) GRIFFIN: A versatile methodology for optimization of protein-lipid interfaces for membrane-protein simulations. J Chem Theory Comput 7:1167-1176.
59. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
60. MacKerell AD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of Proteins. J Phys Chem B 102:3586-3616.
61. Mackerell AD, Jr., Feig M, Brooks CL, 3rd (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25:1400-1415.