Home LiteratureArticle Details
PMID: 22869738 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Oligomycin frames a common drug-binding site in the ATP synthase.

Symersky J, Osowski D, Walters DE, Mueller DM

Abstract

We report the high-resolution (1.9 Å) crystal structure of oligomycin bound to the subunit c(10) ring of the yeast mitochondrial ATP synthase. Oligomycin binds to the surface of the c(10) ring making contact with two neighboring molecules at a position that explains the inhibitory effect on ATP synthesis. The carboxyl side chain of Glu59, which is essential for proton translocation, forms an H-bond with oligomycin via a bridging water molecule but is otherwise shielded from the aqueous environment. The remaining contacts between oligomycin and subunit c are primarily hydrophobic. The amino acid residues that form the oligomycin-binding site are 100% conserved between human and yeast but are widely different from those in bacterial homologs, thus explaining the differential sensitivity to oligomycin. Prior genetics studies suggest that the oligomycin-binding site overlaps with the binding site of other antibiotics, including those effective against Mycobacterium tuberculosis, and thereby frames a common "drug-binding site." We anticipate that this drug-binding site will serve as an effective target for new antibiotics developed by rational design.

MeSH Terms
ATP Synthetase Complexes/chemistry,metabolism Animals Anti-Bacterial Agents/pharmacology Bacterial Proton-Translocating ATPases/chemistry,metabolism Binding Sites/drug effects Crystallography, X-Ray Drug Design Escherichia coli/enzymology Escherichia coli Proteins/chemistry,metabolism Humans Hydrogen Bonding/drug effects Mitochondria/drug effects,enzymology Mycobacterium tuberculosis/enzymology Oligomycins/pharmacology Protein Structure, Secondary Proton-Translocating ATPases/chemistry,metabolism Protons Saccharomyces cerevisiae/enzymology Saccharomyces cerevisiae Proteins/chemistry,metabolism Vacuolar Proton-Translocating ATPases/chemistry,metabolism
Chemicals
Anti-Bacterial Agents Escherichia coli Proteins Oligomycins Protons Saccharomyces cerevisiae Proteins ATP Synthetase Complexes ATP synthase subunit C, Mycobacterium tuberculosis ATP synthase subunit c, E coli Bacterial Proton-Translocating ATPases Vacuolar Proton-Translocating ATPases Proton-Translocating ATPases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Symersky Jindrich
Department of Biochemistry and Molecular Biology, Rosalind Franklin University of Medicine and Science, North Chicago, IL 60064, USA.
Osowski Daniel
Walters D Eric
Mueller David M
References (33)
33 references, click to expand
  1. Amino acid substitutions in mitochondrial ATPase subunit 6 of Saccharomyces cerevisiae leading to oligomycin resistance.
    FEBS Lett. 1986 Oct 20;207(1):79-83 PMID: 2876917
  2. Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis.
    J Biol Chem. 2008 Sep 12;283(37):25273-25280 PMID: 18625705
  3. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes.
    Acta Crystallogr D Biol Crystallogr. 2004 Aug;60(Pt 8):1355-63 PMID: 15272157
  4. Processing of X-ray diffraction data collected in oscillation mode.
    Methods Enzymol. 1997;276:307-26 PMID: 27754618
  5. RESTORATION OF OXIDATIVE PHOSPHORYLATION IN NON-PHOSPHORYLATING SUBMITOCHONDRIAL PARTICLES BY OLIGOMYCIN.
    Biochem Biophys Res Commun. 1965 Feb 17;18:523-9 PMID: 14301455
  6. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis.
    Science. 2005 Jan 14;307(5707):223-7 PMID: 15591164
  7. Amino acid substitutions in mitochondrial ATPase subunit 9 of Saccharomyces cerevisiae leading to oligomycin or venturicidin resistance.
    FEBS Lett. 1986 Jan 20;195(1-2):159-63 PMID: 2867935
  8. ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas.
    Microbiol Mol Biol Rev. 2008 Dec;72(4):590-641, Table of Contents PMID: 19052322
  9. Amino acid substitutions in mitochondrial ATP synthase subunit 9 of Saccharomyces cerevisiae leading to venturicidin or ossamycin resistance.
    FEBS Lett. 1989 Jun 5;249(2):333-6 PMID: 2661266
  10. Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria.
    Proc Natl Acad Sci U S A. 2010 Sep 28;107(39):16823-7 PMID: 20847295
  11. EVIDENCE FOR ENERGY-COUPLING IN NON-PHOSPHORYLATING ELECTRON TRANSPORT PARTICLES FROM BEEF-HEART MITOCHONDRIA.
    Nature. 1964 Jan 11;201:152-5 PMID: 14118261
  12. Molecular architecture of the rotary motor in ATP synthase.
    Science. 1999 Nov 26;286(5445):1700-5 PMID: 10576729
  13. Studies on energy-linked reactions: modified mitochondrial ATPase of oligomycin-resistant mutants of Saccharomyces cerevisiae.
    Eur J Biochem. 1974 Jul 1;46(1):157-67 PMID: 4277672
  14. Structure of the c(10) ring of the yeast mitochondrial ATP synthase in the open conformation.
    Nat Struct Mol Biol. 2012 Apr 15;19(5):485-91, S1 PMID: 22504883
  15. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases.
    J Exp Biol. 1997 Jan;200(Pt 1):1-8 PMID: 9023991
  16. DNA sequence analysis of the oli1 gene reveals amino acid changes in mitochondrial ATPase subunit 9 from oligomycin-resistant mutants of Saccharomyces cerevisiae.
    Eur J Biochem. 1985 Nov 4;152(3):709-14 PMID: 2932333
  17. Molecular replacement with MOLREP.
    Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):22-5 PMID: 20057045
  18. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  19. A reconstituted system of oxidative phosphorylation.
    Biochem Biophys Res Commun. 1964;14:75-8 PMID: 5836560
  20. Inhibition of Escherichia coli H+-ATPase by venturicidin, oligomycin and ossamycin.
    Biochim Biophys Acta. 1985 May 31;807(3):238-44 PMID: 2859888
  21. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XI. Stimulation of oxidative phosphorylation by coupling factors and oligomycin; inhibition by an antibody against coupling factor 1.
    J Biol Chem. 1966 May 25;241(10):2483-9 PMID: 4287858
  22. A mitochondrial factor conferring oligomycin sensitivity on soluble mitochondrial ATPase.
    Biochem Biophys Res Commun. 1963 Mar 25;10:435-9 PMID: 13972927
  23. Refinement of macromolecular structures by the maximum-likelihood method.
    Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55 PMID: 15299926
  24. Genetic basis for natural and acquired resistance to the diarylquinoline R207910 in mycobacteria.
    Antimicrob Agents Chemother. 2006 Aug;50(8):2853-6 PMID: 16870785
  25. Microscopic rotary mechanism of ion translocation in the F(o) complex of ATP synthases.
    Nat Chem Biol. 2010 Dec;6(12):891-9 PMID: 20972431
  26. The Cambridge Structural Database: a quarter of a million crystal structures and rising.
    Acta Crystallogr B. 2002 Jun;58(Pt 3 Pt 1):380-8 PMID: 12037359
  27. Localization on mitochondrial DNA of mutations leading to a loss of rutamycin-sensitive adenosine triphosphatase.
    Eur J Biochem. 1976 Sep;68(1):113-9 PMID: 134892
  28. Partial resolution of the enzymes catalyzing oxidative phosphorylation. 8. Properties of a factor conferring oligomycin sensitivity on mitochondrial adenosine triphosphatase.
    J Biol Chem. 1966 May 25;241(10):2461-6 PMID: 4223640
  29. Coot: model-building tools for molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32 PMID: 15572765
  30. Molecular surface area and hydrophobic effect.
    Protein Eng. 1992 Dec;5(8):715-6 PMID: 1287651
  31. Antibiotics as tools for metabolic studies. I. A survey of toxic antibiotics in respiratory, phosphorylative and glycolytic systems.
    Arch Biochem Biophys. 1958 Dec;78(2):587-97 PMID: 13618041
  32. Identification of amino acid substitutions in the dicyclohexylcarbodiimide-binding subunit of the mitochondrial ATPase complex from oligomycin-resistant mutants of Saccharomyces cerevisiae.
    Eur J Biochem. 1979 Oct 15;100(2):599-607 PMID: 159820
  33. The hydrophobic effect and the organization of living matter.
    Science. 1978 Jun 2;200(4345):1012-8 PMID: 653353
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-08-28
Epub
2012-00-06
Pages
13961-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3435195
Subset
IM
Grants
NIGMS NIH HHS · R01 GM066223 · United States
NIGMS NIH HHS · R01GM66223 · United States
Databases
PDB
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com