Structure and Function of Subunit a of the ATP Synthase of Escherichia Coli

Overview

Journal J Bioenerg Biomembr

Publisher Springer

Specialties Biochemistry
Biology
Endocrinology

Date 2006 May 13

PMID 16691481

Citations 17

Authors

Steven B Vik

Robert R Ishmukhametov

Affiliations

Soon will be listed here.

Abstract

The structure of subunit a of the Escherichia coli ATP synthase has been probed by construction of more than one hundred monocysteine substitutions. Surface labeling with 3-N-maleimidyl-propionyl biocytin (MPB) has defined five transmembrane helices, the orientation of the protein in the membrane, and information about the relative exposure of the loops connecting these helices. Cross-linking studies using TFPAM-3 (N-(4-azido-2,3,5,6-tetrafluorobenzyl)-3-maleimido-propionamide) and benzophenone-4-maleimide have revealed which elements of subunit a are near subunits b and c. Use of a chemical protease reagent, 5-(-bromoacetamido)-1,10-phenanthroline-copper, has indicated that the periplasmic end of transmembrane helix 5 is near that of transmembrane helix 2.

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References

Girvin M, Rastogi V, Abildgaard F, Markley J, Fillingame R . Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry. 1998; 37(25):8817-24. DOI: 10.1021/bi980511m. View

Zhang W, Bogdanov M, Pi J, Pittard A, Dowhan W . Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. J Biol Chem. 2003; 278(50):50128-35. DOI: 10.1074/jbc.M309840200. View

Long J, DeLeon-Rangel J, Vik S . Characterization of the first cytoplasmic loop of subunit a of the Escherichia coli ATP synthase by surface labeling, cross-linking, and mutagenesis. J Biol Chem. 2002; 277(30):27288-93. DOI: 10.1074/jbc.M202118200. View

Valiyaveetil F, Fillingame R . Transmembrane topography of subunit a in the Escherichia coli F1F0 ATP synthase. J Biol Chem. 1998; 273(26):16241-7. DOI: 10.1074/jbc.273.26.16241. View

Elston T, Wang H, Oster G . Energy transduction in ATP synthase. Nature. 1998; 391(6666):510-3. DOI: 10.1038/35185. View

Aksimentiev A, Balabin I, Fillingame R, Schulten K . Insights into the molecular mechanism of rotation in the Fo sector of ATP synthase. Biophys J. 2004; 86(3):1332-44. PMC: 1303972. DOI: 10.1016/S0006-3495(04)74205-8. View

Vik S, Cain B, Chun K, Simoni R . Mutagenesis of the alpha subunit of the F1Fo-ATPase from Escherichia coli. Mutations at Glu-196, Pro-190, and Ser-199. J Biol Chem. 1988; 263(14):6599-605. View

Vik S, Patterson A, Antonio B . Insertion scanning mutagenesis of subunit a of the F1F0 ATP synthase near His245 and implications on gating of the proton channel. J Biol Chem. 1998; 273(26):16229-34. DOI: 10.1074/jbc.273.26.16229. View

Stock D, Leslie A, Walker J . Molecular architecture of the rotary motor in ATP synthase. Science. 1999; 286(5445):1700-5. DOI: 10.1126/science.286.5445.1700. View

10.

Ishmukhametov R, Galkin M, Vik S . Ultrafast purification and reconstitution of His-tagged cysteine-less Escherichia coli F1Fo ATP synthase. Biochim Biophys Acta. 2004; 1706(1-2):110-6. DOI: 10.1016/j.bbabio.2004.09.012. View

11.

Bragg P, Hou C . Subunit composition, function, and spatial arrangement in the Ca2+-and Mg2+-activated adenosine triphosphatases of Escherichia coli and Salmonella typhimurium. Arch Biochem Biophys. 1975; 167(1):311-21. DOI: 10.1016/0003-9861(75)90467-1. View

12.

Angevine C, Fillingame R . Aqueous access channels in subunit a of rotary ATP synthase. J Biol Chem. 2002; 278(8):6066-74. DOI: 10.1074/jbc.M210199200. View

13.

Cain B, Simoni R . Proton translocation by the F1F0ATPase of Escherichia coli. Mutagenic analysis of the a subunit. J Biol Chem. 1989; 264(6):3292-300. View

14.

Patterson A, Wada T, Vik S . His(15) of subunit a of the Escherichia coli ATP synthase is important for the structure or assembly of the membrane sector F(o). Arch Biochem Biophys. 1999; 368(1):193-7. DOI: 10.1006/abbi.1999.1306. View

15.

Zhang D, Vik S . Helix packing in subunit a of the Escherichia coli ATP synthase as determined by chemical labeling and proteolysis of the cysteine-substituted protein. Biochemistry. 2003; 42(2):331-7. DOI: 10.1021/bi026649t. View

16.

Foster D, Fillingame R . Stoichiometry of subunits in the H+-ATPase complex of Escherichia coli. J Biol Chem. 1982; 257(4):2009-15. View

17.

DeLeon-Rangel J, Zhang D, Vik S . The role of transmembrane span 2 in the structure and function of subunit a of the ATP synthase from Escherichia coli. Arch Biochem Biophys. 2003; 418(1):55-62. DOI: 10.1016/s0003-9861(03)00391-6. View

18.

Wada T, Long J, Zhang D, Vik S . A novel labeling approach supports the five-transmembrane model of subunit a of the Escherichia coli ATP synthase. J Biol Chem. 1999; 274(24):17353-7. DOI: 10.1074/jbc.274.24.17353. View

19.

Capaldi R, Aggeler R . Mechanism of the F(1)F(0)-type ATP synthase, a biological rotary motor. Trends Biochem Sci. 2002; 27(3):154-60. DOI: 10.1016/s0968-0004(01)02051-5. View

20.

Vik S, Lee D, Marshall P . Temperature-sensitive mutations at the carboxy terminus of the alpha subunit of the Escherichia coli F1F0 ATP synthase. J Bacteriol. 1991; 173(14):4544-8. PMC: 208122. DOI: 10.1128/jb.173.14.4544-4548.1991. View