DOI: 10.1073/pnas.0910365106. The structure of the membrane extrinsic region of bovine ATP synthase

The structure of the membrane extrinsic region of bovine ATP synthase

10.1073/pnas.0910365106

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The structure of the complex between bovine mitochondrial F 1 -ATPase and a stator subcomplex has been determined at a resolution of 3.2 Å. The resolved region of the stator contains residues 122–207 of subunit b; residues 5–25 and 35–57 of F 6 ; 3 segments of subunit d from residues 30–40, 65–74, and 85–91; and residues 1–146 and 169–189 of the oligomycin sensitivity conferral protein (OSCP). The stator subcomplex represents its membrane distal part, and its structure has been augmented with an earlier structure of a subcomplex containing residues 79–183, 3–123, and 5–70 of subunits b, d, and F 6 , respectively, which extends to the surface of the inner membrane of the mitochondrion. The N-terminal domain of the OSCP links the stator with F 1 -ATPase via α-helical interactions with the N-terminal region of subunit α E . Its C-terminal domain makes extensive helix–helix interactions with the C-terminal α-helix of subunit b from residues 190–207. Subunit b extends as a continuous 160-Å long α-helix from residue 188 back to residue 79 near to the surface of the inner mitochondrial membrane. This helix appears to be stiffened by other α-helices in subunits d and F 6 , but the structure can bend inward toward the F 1 domain around residue 146 of subunit b. The linker region between the 2 domains of the OSCP also appears to be flexible, enabling the stator to adjust its shape as it passes over the changing profile of the F 1 domain during a catalytic cycle. The structure of the membrane extrinsic part of bovine ATP synthase is now complete.

Bibliography

Rees, D. M., Leslie, A. G. W., & Walker, J. E. (2009). The structure of the membrane extrinsic region of bovine ATP synthase. Proceedings of the National Academy of Sciences, 106(51), 21597â21601.

Authors 3

David M. Rees (first)
Andrew G. W. Leslie (additional)
John E. Walker (additional)

References 33 Referenced 147

10.1093/emboj/cdg608
10.1074/jbc.M700203200
10.1042/BST0340989
10.1038/sj.emboj.7601410
10.1126/science.286.5445.1700
IR Collinson, et al., In vitro assembly of a stalk complex in the presence of F1-ATPase and in its absence. J Mol Biol 242, 408–421 (1994). (10.1016/S0022-2836(84)71591-9) / J Mol Biol / In vitro assembly of a stalk complex in the presence of F1-ATPase and in its absence by Collinson IR (1994)
10.1016/j.jmb.2007.02.059
10.1038/sj.emboj.7601177
10.1016/j.bbabio.2006.01.001
10.1021/bi981120a
10.1074/jbc.M201047200
10.1021/bi0510678
10.1021/bi00324a029
10.1021/bi9704109
10.1016/S0022-2836(02)00671-X
10.1021/bi0510678
10.1074/jbc.273.24.15162
10.1074/jbc.273.15.8646
10.1074/jbc.M000375200
10.1038/nature02212
10.1038/sj.emboj.7600682
10.1074/jbc.M212852200
10.1016/S0005-2728(00)00086-4
10.1074/jbc.M404993200
10.1073/pnas.0807683105
AGW Leslie, Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallography, pp. 26 (1992). / Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallography / Recent changes to the MOSFLM package for processing film and image plate data by Leslie AGW (1992)
10.1107/S0907444905036693
10.1107/S0567739478001114
10.1107/S0907444905001617
10.1107/S0907444904019158
10.1107/S0907444996012255
PV Afonine, RW Grosse-Kunstleve, PD Adams, The Phenix refinement framework. CCP4 Newsletter on Protein Crystallography, pp. 42, contribution 8. (2005). / CCP4 Newsletter on Protein Crystallography / The Phenix refinement framework by Afonine PV (2005)
WL DeLano The PyMol Molecular Graphics System (DeLano Scientific, San Carlos, CA, 2002). / The PyMol Molecular Graphics System by DeLano WL (2002)

Dates

Type	When
Created	15 years, 8 months ago (Dec. 8, 2009, 12:32 a.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 6:58 p.m.)
Indexed	2 weeks, 1 day ago (Aug. 7, 2025, 4:48 p.m.)
Issued	15 years, 8 months ago (Dec. 22, 2009)
Published	15 years, 8 months ago (Dec. 22, 2009)
Published Online	15 years, 8 months ago (Dec. 22, 2009)
Published Print	15 years, 8 months ago (Dec. 22, 2009)

Funders 0

None

BibTeX

@article{Rees_2009, title={The structure of the membrane extrinsic region of bovine ATP synthase}, volume={106}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0910365106}, DOI={10.1073/pnas.0910365106}, number={51}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Rees, David M. and Leslie, Andrew G. W. and Walker, John E.}, year={2009}, month=dec, pages={21597–21601} }

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  "abstract": "<jats:p>\n            The structure of the complex between bovine mitochondrial F\n            <jats:sub>1</jats:sub>\n            -ATPase and a stator subcomplex has been determined at a resolution of 3.2 \u212b. The resolved region of the stator contains residues 122\u2013207 of subunit b; residues 5\u201325 and 35\u201357 of F\n            <jats:sub>6</jats:sub>\n            ; 3 segments of subunit d from residues 30\u201340, 65\u201374, and 85\u201391; and residues 1\u2013146 and 169\u2013189 of the oligomycin sensitivity conferral protein (OSCP). The stator subcomplex represents its membrane distal part, and its structure has been augmented with an earlier structure of a subcomplex containing residues 79\u2013183, 3\u2013123, and 5\u201370 of subunits b, d, and F\n            <jats:sub>6</jats:sub>\n            , respectively, which extends to the surface of the inner membrane of the mitochondrion. The N-terminal domain of the OSCP links the stator with F\n            <jats:sub>1</jats:sub>\n            -ATPase via \u03b1-helical interactions with the N-terminal region of subunit \u03b1\n            <jats:sub>E</jats:sub>\n            . Its C-terminal domain makes extensive helix\u2013helix interactions with the C-terminal \u03b1-helix of subunit b from residues 190\u2013207. Subunit b extends as a continuous 160-\u212b long \u03b1-helix from residue 188 back to residue 79 near to the surface of the inner mitochondrial membrane. This helix appears to be stiffened by other \u03b1-helices in subunits d and F\n            <jats:sub>6</jats:sub>\n            , but the structure can bend inward toward the F\n            <jats:sub>1</jats:sub>\n            domain around residue 146 of subunit b. The linker region between the 2 domains of the OSCP also appears to be flexible, enabling the stator to adjust its shape as it passes over the changing profile of the F\n            <jats:sub>1</jats:sub>\n            domain during a catalytic cycle. The structure of the membrane extrinsic part of bovine ATP synthase is now complete.\n          </jats:p>",
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