The ND2 subunit is labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor

FEBS Letters

Volumn 584, Issue 5, 2010, Pages 883-888

  Nakamaru Ogiso, Eiko ^a,b   Han, Hongna ^a   Matsuno Yagi, Akemi ^a   Keinan, Ehud ^a   Sinha, Subhash C ^a   Yagi, Takao ^a   Ohnishi, Tomoko ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Asimicin; Bovine heart mitochondria; Complex I; ND2; Photoaffinity labeling; Quinone binding

Indexed keywords

ASIMICIN; BENZOPHENONE ASIMICIN; ROTENONE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ISOLATION; ENZYME SUBUNIT; HEART MITOCHONDRION; NONHUMAN; PHOTOAFFINITY LABELING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING;

ANIMALS; BENZOPHENONES; CATTLE; ELECTRON TRANSPORT COMPLEX I; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; ENZYME INHIBITORS; FURANS; IMMUNOBLOTTING; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; PROTEIN SUBUNITS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

BOVINAE;

EID: 76749117977     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.01.004     Document Type: Article

References (35)

1. Yagi T., and Matsuno-Yagi A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42 (2003) 2266-2274
2. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75 (2006) 69-92
3. Carroll J., Fearnley I.M., Skehel J.M., Shannon R.J., Hirst J., and Walker J.E. Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 281 (2006) 32724-32727
4. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
5. Ohnishi T. Iron-sulfur clusters/semiquinones in complex I. Biochim. Biophys. Acta 1364 (1998) 186-206
6. +-sensitive ubisemiquinone species (SQ(Nf)) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44 (2005) 1744-1754
7. Ohnishi T., and Salerno J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 579 (2005) 4555-4561
8. Ohnishi T., Johnson Jr. J.E., Yano T., Lobrutto R., and Widger W.R. Thermodynamic and EPR studies of slowly relaxing ubisemiquinone species in the isolated bovine heart complex I. FEBS Lett. 579 (2005) 500-506
9. Degli Esposti M. Inhibitors of NADH-ubiquinone reductase: an overview. Biochim. Biophys. Acta 1364 (1998) 222-235
10. Earley F.G., Patel S.D., Ragan I., and Attardi G. Photolabelling of a mitochondrially encoded subunit of NADH dehydrogenase with [3H]dihydrorotenone. FEBS Lett. 219 (1987) 108-112
11. Murai M., Ishihara A., Nishioka T., Yagi T., and Miyoshi H. The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I. Biochemistry 46 (2007) 6409-6416
12. Schuler F., and Casida J.E. Functional coupling of PSST and ND1 subunits in NADH:ubiquinone oxidoreductase established by photoaffinity labeling. Biochim. Biophys. Acta 1506 (2001) 79-87
13. Yagi T., and Hatefi Y. Identification of the dicyclohexylcarbodiimide-binding subunit of NADH-ubiquinone oxidoreductase (complex I). J. Biol. Chem. 263 (1988) 16150-16155
14. Gong X., Xie T., Yu L., Hesterberg M., Scheide D., Friedrich T., and Yu C.A. The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli. J. Biol. Chem. 278 (2003) 25731-25737
15. Matsumoto Y., Murai M., Fujita D., Sakamoto K., Miyoshi H., Yoshida M., and Mogi T. Mass spectrometric analysis of the ubiquinol-binding site in cytochrome bd from Escherichia coli. J. Biol. Chem. 281 (2006) 1905-1912
16. Nakamaru-Ogiso E., Sakamoto K., Matsuno-Yagi A., Miyoshi H., and Yagi T. The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry 42 (2003) 746-754
17. Murai M., Sekiguchi K., Nishioka T., and Miyoshi H. Characterization of the inhibitor binding site in mitochondrial NADH-ubiquinone oxidoreductase by photoaffinity labeling using a quinazoline-type inhibitor. Biochemistry 48 (2009) 688-698
18. Sekiguchi K., Murai M., and Miyoshi H. Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I. Biochim. Biophys. Acta 1787 (2009) 1106-1111
19. Okun J.G., Lummen P., and Brandt U. Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH:ubiquinone oxidoreductase). J. Biol. Chem. 274 (1999) 2625-2630
20. Rupprecht J.K., Hui Y.H., and McLaughlin J.L. Annonaceous acetogenins: a review. J. Nat. Prod. 53 (1990) 237-278
21. Dorman G., and Prestwich G.D. Benzophenone photophores in biochemistry. Biochemistry 33 (1994) 5661-5673
22. Matsuno-Yagi A., and Hatefi Y. Studies on the mechanism of oxidative phosphorylation. Catalytic site cooperativity in ATP synthesis. J. Biol. Chem. 260 (1985) 11424-11427
23. Han H., Sinha M.K., D'Souza L.J., Keinan E., and Sinha S.C. Total synthesis of 34-hydroxyasimicin and its photoactive derivative for affinity labeling of the mitochondrial complex I. Chemistry 10 (2004) 2149-2158
24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
25. Schägger H. Tricine-SDS-PAGE. Nat. Protoc. 1 (2006) 16-22
26. Wittig I., Braun H.P., and Schägger H. Blue native PAGE. Nat. Protoc. 1 (2006) 418-428
27. Rais I., Karas M., and Schägger H. Two-dimensional electrophoresis for the isolation of integral membrane proteins and mass spectrometric identification. Proteomics 4 (2004) 2567-2571
28. Fleischer S., Rouser G., Fleischer B., Casu A., and Kritchevsky G. Lipid composition of mitochondria from bovine heart, liver, and kidney. J. Lipid Res. 8 (1967) 170-180
29. Burre J., Beckhaus T., Schägger H., Corvey C., Hofmann S., Karas M., Zimmermann H., and Volknandt W. Analysis of the synaptic vesicle proteome using three gel-based protein separation techniques. Proteomics 6 (2006) 6250-6262
30. Galkin A., Meyer B., Wittig I., Karas M., Schagger H., Vinogradov A., and Brandt U. Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I. J. Biol. Chem. 283 (2008) 20907-20913
31. Kawamura A., Hindi S., Mihai D.M., James L., and Aminova O. Binding is not enough: flexibility is needed for photocrosslinking of Lck kinase by benzophenone photoligands. Bioorg. Med. Chem. 16 (2008) 8824-8829
32. Shimada H., Grutzner J.B., Kozlowski J.F., and McLaughlin J.L. Membrane conformations and their relation to cytotoxicity of asimicin and its analogues. Biochemistry 37 (1998) 854-866
33. Amarneh B., and Vik S.B. Mutagenesis of subunit N of the Escherichia coli complex I. Identification of the initiation codon and the sensitivity of mutants to decylubiquinone. Biochemistry 42 (2003) 4800-4808
34. Fisher N., and Rich P.R. A motif for quinone binding sites in respiratory and photosynthetic systems. J. Mol. Biol. 296 (2000) 1153-1162
35. Magnitsky S., et al. EPR characterization of ubisemiquinones and iron-sulfur cluster N2, central components of the energy coupling in the NADH-ubiquinone oxidoreductase (complex I) in situ. J. Bioenerg. Biomembr. 34 (2002) 193-208