Obstruction of transmembrane helical movements in subunit a blocks proton pumping by F1Fo ATP synthase

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25535-25541

  Moore, Kyle J ^a   Fillingame, Robert H ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP SYNTHASE; ATP SYNTHESIS; BOND FORMATION; PROTON-PUMPING; TRANSMEMBRANE HELICES; TRANSMEMBRANES;

BIOCHEMISTRY;

BIOLOGY;

ASPARTIC ACID; CYSTEINE; F1FO ATP SYNTHASE; GLYCINE; HISTIDINE; ISOLEUCINE; LEUCINE; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ALPHA CHAIN; ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE TRANSPORT; CHANNEL GATING; CHEMICAL MODIFICATION; CONTROLLED STUDY; CYTOPLASM; ENZYME CONFORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTON PUMPING; PROTON TRANSPORT; ROTATION;

ATP SYNTHASE; ATPASES; CYSTEINE-MEDIATED CROSS-LINKING; F1FO ATPASE; PROTON TRANSPORT; SUBUNIT A; TRANSMEMBRANE HELICES;

AMINO ACID SUBSTITUTION; BACTERIAL PROTON-TRANSLOCATING ATPASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84883397875     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.496794     Document Type: Article

References (37)

1. Yoshida, M., Muneyuki, E., and Hisabori, T. (2001) ATP synthase-a marvelous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2, 669-677
2. Nakamoto, R. K., Baylis Scanlon, J. A., and Al-Shawi, M. K. (2008) The rotary mechanism of the ATP synthase. Arch. Biochem. Biophys. 476, 43-50
3. von Ballmoos, C., Wiedenmann, A., and Dimroth, P. (2009) Essentials for ATP synthesis by F1-FO ATP synthases. Annu. Rev. Biochem. 78, 649-672
4. Senior, A. E. (1988) ATP synthesis by oxidative phosphorylation. Physiol. Rev. 68, 177-231
5. Jiang, W., Hermolin, J., and Fillingame, R. H. (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is ten. Proc. Natl. Acad. Sci. U.S.A. 98, 4966-4971
6. Mitome, N., Suzuki, T., Hayashi, S., and Yoshida, M. (2004) Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H+/ ATP ratio and permissive elastic coupling. Proc. Natl. Acad. Sci. U.S.A. 101, 12159-12164
7. Meier, T., Polzer, P., Diederichs, K., Welte, W., and Dimroth, P. (2005) Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science 308, 659-662
8. Pogoryelov, D., Yildiz, O., Faraldo-Gómez, J.D., Meier, T. (2009) Highresolution structure of the rotor ring of a proton-dependent ATP synthase. Nat. Struct. Mol. Biol. 16, 1068-1073
9. Jones, P. C., Jiang, W., and Fillingame, R. H. (1998) Arrangement of the multicopyH+-translocating subunit c in the membrane sector of the Escherichia coli F1Fo ATP synthase. J. Biol. Chem. 273, 17178-17185
10. Dmitriev, O.Y., Jones, P.C., and Fillingame, R. H. (1999) Structure of the subunit c oligomer in the F1Fo ATP synthase: Model derived from solution structure of the monomer and cross-linking in the native enzyme. Proc. Natl. Acad. Sci. U.S.A. 96, 7785-7790
11. Meier, T., Krah, A., Bond P.J., Pogoryelov D., Diederichs, K., Faraldo-Gómez, J. D. (2009) Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J. Mol. Biol. 391, 498-507
12. Krah, A., Pogoryelov, D., Langer J.D., Bond, P. J., Meier, T., and Faraldo-Gomez, J. D. (2010) Structural and energetic basis for H+ versus Na+ binding selectivity in ATP synthase Fo rotors. Biochim. Biophys. Acta 1797, 763-772
13. Valiyaveetil, F. I., and Fillingame, R. H. (1998) Transmembrane topography of subunit a in the Escherichia coli F1Fo ATP synthase. J. Biol. Chem. 273, 16241-16247
14. Long, J. C., Wang, S., and Vik, S. B. (1998) Membrane topology of subunit a of the F1Fo ATP synthase as determined by labeling of unique cycteine residues. J. Biol. Chem. 273, 16235-16240
15. Wada, T., Long, J. C., Zhang, D., and Vik, S. B. (1999) A novel labeling approach supports the five-transmembrane model of subunit a of the Escherichia coli ATP synthase. J. Biol. Chem. 274, 17353-17357
16. Fillingame, R. H., Angevine, C. M., and Dmitriev, O. Y. (2003) Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 555, 29-34
17. Cain, B. D. (2000) Mutagenic analysis of the FO stator subunits. J. Bioenerg. Biomembr. 32, 365-371
18. Hatch, L. P., Cox, G. B., and Howitt, S. M. (1995) The essential arginine residue at position 210 in the a subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity. J. Biol. Chem. 270, 29407-29412
19. Valiyaveetil, F. I., and Fillingame, R. H. (1997) On the role of Arg210 and Glu219 of subunit a in proton translocation by the Escherichia coli FoF1 ATP synthase. J. Biol. Chem. 272, 32635-32641
20. Eya, S., Maeda, M., and Futai, M. (1991) Role of the carboxyl terminal region of H+-ATPase (FOF1) a subunit from Escherichia coli. Arch. Biochem. Biophys. 284, 71-77
21. Schwem, B. E., and Fillingame, R. H. (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, 37861-37867
22. Hakulinen, J. K., Klyszejko, A. L., Hoffmann, J., Eckhardt-Strelau, L., Brutschy, B., Vonck, J., and Meier, T. (2012) Structural study on the architecture of the bacterial ATP synthase Fo motor. Proc. Natl. Acad. Sci. U.S.A. 109, E2050-E2056
23. Jiang, W., and Fillingame, R. H. (1998) Interacting helical faces of subunits a and c in the F1Fo ATP synthase of Escherichia coli defined by disulfide cross-linking. Proc. Natl. Acad. Sci. U.S.A. 95, 6607-6612
24. Moore, K. J., and Fillingame, R. H. (2008) Structural interactions between transmembrane helices 4 and 5 of subunit a and the subunit c ring of Escherichia coli ATP synthase. J. Biol. Chem. 283, 31726-31735
25. Ishmukhametov, R. R., Pond, J. B., Al-Huqail, A., Galkin, M. A., and Vik, S. B. (2008) ATP synthesis without R210 of subunit a in the Escherichia coli ATP synthase. Biochim. Biophys. Acta 1777, 32-38
26. Angevine, C. M., and Fillingame, R. H. (2003) Aqueous access channels in subunit a of rotary ATP synthase. J. Biol. Chem. 278, 6066-6074
27. Angevine, C. M., Herold, K. A., and Fillingame, R. H. (2003) Aqueous access pathways in subunit a of rotary ATP synthase extend to both sides of the membrane. Proc. Natl. Acad. Sci. U.S.A. 100, 13179-13183
28. Angevine, C. M., Herold, K. A., Vincent, O. D., and Fillingame, R. H. (2007) Aqueous access pathways in ATP synthase of subunit a: reactivity of cysteine substituted into transmembrane helices 1, 3 and 5. J. Biol. Chem. 282, 9001-9007
29. Dong, H, and Fillingame, R. H. (2010) Chemical reactivities of cysteine substitutions in subunit a of ATP synthase define residues gating H+- transport from each side of the membrane. J. Biol. Chem. 285, 39811-39818
30. Steed, P. R., and Fillingame, R. H. (2008) Subunit a facilitates aqueous access to a membrane-embedded region of subunit c in Escherichia coli ATP synthase. J. Biol. Chem. 283, 12365-12372
31. Steed, P. R., and Fillingame, R. H. (2009) Aqueous accessibility to the transmembrane regions of subunit c of the Escherichia coli F1F0 ATP synthase. J. Biol. Chem. 284, 23243-23250
32. Gohlke, H., Schlieper, D., and Groth, G. (2012) Resolving the negative potential (n-side) water-accessible proton pathway of F-type ATP synthase by molecular dynamics simulations. J. Biol. Chem. 287, 36536-36543
33. Moore, K. J., Angevine, C. M., Vincent, O. D., Schwem, B. E., and Fillingame, R. H. (2008) The cytoplasmic loops of subunit a of Escherichia coli ATP synthase may participate in the proton translocating mechanism. J. Biol. Chem. 283, 13044-13052
34. Kuo, P. H., Ketchum, C. J., and Nakamoto, R. K. (1998) Stability and functionality of cysteine-less FOF1 ATP synthase from Escherichia coli. FEBS Lett. 426, 217-220
35. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
36. Jones, P. C., and Fillingame, R. H. (1998) Genetic fusions of subunit c in the Fo sector ofH+-transportingATPsynthase: functional dimers and trimers and determination of stoichiometry by cross-linking analysis. J. Biol. Chem. 273, 29701-29705
37. Loo, T. W., and Clarke, D. M. (2001) Determining the dimensions of the drug-binding domain of human P-glycoprotein using thiol cross-linking compounds as molecular rulers. J. Biol. Chem. 276, 36877-36880