Pivotal roles of three conserved carboxyl residues of the NuoC (30k) segment in the structural integrity of proton-translocating NADH-quinone oxidoreductase from escherichia coli

Biochemistry

Volumn 49, Issue 47, 2010, Pages 10072-10080

  Castro Guerrero, Norma ^a   Sinha, Prem Kumar ^a   Torres Bacete, Jesus ^a   Matsuno Yagi, Akemi ^a   Yagi, Takao ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COFACTORS; COMPLEX I; CONSERVED RESIDUES; ENZYMATIC ASSAY; GEL ANALYSIS; GENE MANIPULATION; HYDROPHOBIC SUBUNITS; L-SHAPED; MEMBRANE-BOUND ENZYMES; OXIDOREDUCTASES; STRUCTURAL STABILITIES; TRANSDUCING; TWO DOMAINS;

ESCHERICHIA COLI; PROTONS; STABILITY;

ENZYMES;

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE);

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ASPARTIC ACID; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUTAMIC ACID; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTONS; QUINONE REDUCTASES; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 78649504798     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100885v     Document Type: Article

References (50)

1. Walker, J. E. (1992) The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains Q. Rev. Biophys. 25, 253-324
2. Yagi, T. and Matsuno-Yagi, A. (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: The secret unlocked Biochemistry 42, 2266-2274
3. Brandt, U. (2006) Energy Converting NADH:Quinone Oxidoreductase (Complex I) Annu. Rev. Biochem. 75, 69-92
4. Carroll, J., Fearnley, I. M., Skehel, J. M., Shannon, R. J., Hirst, J., and Walker, J. E. (2006) Bovine complex I is a complex of forty-five different subunits J. Biol. Chem. 281, 32724-32727
5. Yagi, T., Yano, T., and Matsuno-Yagi, A. (1993) Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches J. Bioenerg. Biomembr. 25, 339-345
6. Yagi, T., Yano, T., Di Bernardo, S., and Matsuno-Yagi, A. (1998) Procaryotic complex I (NDH-1), an overview Biochim. Biophys. Acta 1364, 125-133
7. Guénebaut, V., Schlitt, A., Weiss, H., Leonard, K., and Friedrich, T. (1998) Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Mol. Biol. 276, 105-112
8. Ohnishi, T. (1998) Iron-sulfur clusters semiquinones in Complex I Biochim. Biophys. Acta 1364, 186-206
9. Hinchliffe, P. and Sazanov, L. A. (2005) Organization of iron-sulfur clusters in respiratory complex I Science 309, 771-774
10. Sazanov, L. A. and Hinchliffe, P. (2006) Structure of the Hydrophilic Domain of Respiratory Complex I from Thermus thermophilus Science 311, 1430-1436
11. Berrisford, J. M. and Sazanov, L. A. (2009) Structural basis for the mechanism of respiratory complex I J. Biol. Chem. 284, 29773-29783
12. Nakamaru-Ogiso, E., Yano, T., Yagi, T., and Ohnishi, T. (2005) Characterization of the iron-sulfur cluster N7(N1c) in the subunit NuoG of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli J. Biol. Chem. 280, 301-307 (Pubitemid 40164993)
13. Nakamaru-Ogiso, E., Matsuno-Yagi, A., Yoshikawa, S., Yagi, T., and Ohnishi, T. (2008) Iron-sulfur cluster N5 is coordinated by a HXXXCXXCXXXXXC motif in the nuog subunit of E. coli NADH:Quinone oxidoreductase (complex I) J. Biol. Chem. 283, 25979-25987
14. Friedrich, T. (1998) The NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli Biochim. Biophys. Acta 1364, 134-146
15. Dupuis, A., Chevallet, M., Darrouzet, E., Duborjal, H., Lunardi, J., and Issartel, J. P. (1998) The Complex I from Rhodobacter capsulatus Biochim. Biophys. Acta 1364, 147-165
16. Yano, T., Chu, S. S., Sled, V. D., Ohnishi, T., and Yagi, T. (1997) The proton-translocating NADH-quinone oxidoreductase (NDH-1) of thermophilic bacterium Thermus thermophilus HB-8: Complete DNA sequence of the gene cluster and thermostable properties of the expressed NQO2 subunit J. Biol. Chem. 272, 4201-4211
17. Darrouzet, E., Issartel, J. P., Lunardi, J., and Dupuis, A. (1998) The 49-kDa subunit of NADH-ubiquinone oxidoreductase (Complex I) is involved in the binding of piericidin and rotenone, two quinone-related inhibitors FEBS Lett. 431, 34-38
18. Prieur, I., Lunardi, J., and Dupuis, A. (2001) Evidence for a quinone binding site close to the interface between NUOD and NUOB subunits of Complex I Biochim. Biophys. Acta 1504, 173-178
19. Kashani-Poor, N., Zwicker, K., Kerscher, S., and Brandt, U. (2001) A central functional role for the 49 kDa subunit within the catalytic core of mitochondrial complex I J. Biol. Chem. 276, 24082-24087
20. Kao, M. C., Di Bernardo, S., Perego, M., Nakamaru-Ogiso, E., Matsuno-Yagi, A., and Yagi, T. (2004) Functional roles of four conserved charged residues in the membrane domain subunit NuoA of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli J. Biol. Chem. 279, 32360-32366
21. Kao, M. C., Di Bernardo, S., Nakamaru-Ogiso, E., Miyoshi, H., Matsuno-Yagi, A., and Yagi, T. (2005) Characterization of the membrane domain subunit NuoJ (ND6) of the NADH-quinone oxidoreductase from Escherichia coli by chromosomal DNA manipulation Biochemistry 44, 3562-3571 (Pubitemid 40322025)
22. Kao, M. C., Nakamaru-Ogiso, E., Matsuno-Yagi, A., and Yagi, T. (2005) Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli Biochemistry 44, 9545-9554
23. Torres-Bacete, J., Nakamaru-Ogiso, E., Matsuno-Yagi, A., and Yagi, T. (2007) Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1: Conserved charged residues essential for energy-coupled activities J. Biol. Chem. 282, 36914-36922
24. Sinha, P. K., Torres-Bacete, J., Nakamaru-Ogiso, E., Castro-Guerrero, N., Matsuno-Yagi, A., and Yagi, T. (2009) Critical roles of subunit NuoH (ND1) in the assembly of peripheral subunits with the membrane domain of Escherichia coli NDH-1 J. Biol. Chem. 284, 9814-9823
25. Nakamaru-Ogiso, E., Kao, M. C., Chen, H., Sinha, S. C., Yagi, T., and Ohnishi, T. (2010) The membrane subunit NuoL(ND5) is involved in the indirect proton pumping mechanism of E. coli complex I J. Biol. Chem. (in press)
26. Finel, M. (1998) Organization and evolution of structural elements within complex I Biochim. Biophys. Acta 1364, 112-121
27. Satoh, T., Miyoshi, H., Sakamoto, K., and Iwamura, H. (1996) Comparison of the inhibitory action of synthetic capsaicin analogues with various NADH-ubiquinone oxidoreductases Biochim. Biophys. Acta 1273, 21-30
28. Torres-Bacete, J., Sinha, P. K., Castro-Guerrero, N., Matsuno-Yagi, A., and Yagi, T. (2009) Features of subunit NuoM (ND4) in Escherichia coli NDH-1: Topology and implication of conserved Glu144 for coupling site 1 J. Biol. Chem. 284, 33062-33069
29. Link, A. J., Phillips, D., and Church, G. M. (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: Application to open reading frame characterization J. Bacteriol. 179, 6228-6237
30. Amarneh, B. and Vik, S. B. (2003) Mutagenesis of Subunit N of the Escherichia coli Complex I. Identification of the Initiation Codon and the Sensitivity of Mutants to Decylubiquinone Biochemistry 42, 4800-4808
31. Schagger, H. and Von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal. Biochem. 199, 223-231
32. Sali, A. and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234, 779-815
33. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948
34. DeLano, W. L. (2008) The PyMOL Molecular Graphics System, DeLano Scientific LLC, Palo Alto, CA.
35. Matsushita, K., Ohnishi, T., and Kaback, H. R. (1987) NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain Biochemistry 26, 7732-7737
36. Hedderich, R. (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: Ancestors of complex I J. Bioenerg. Biomembr. 36, 65-75
37. Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R., and Metcalf, W. W. (2002) Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation Proc. Natl. Acad. Sci. U.S.A. 99, 5632-5637
38. Andrews, S. C., Berks, B. C., McClay, J., Ambler, A., Quail, M. A., Golby, P., and Guest, J. R. (1997) A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system Microbiology 143 (Part 11) 3633-3647
39. Friedrich, T. (2001) Complex I: A chimaera of a redox and conformation-driven proton pump? J. Bioenerg. Biomembr. 33, 169-177
40. Grgic, L., Zwicker, K., Kashani-Poor, N., Kerscher, S., and Brandt, U. (2004) Functional significance of conserved histidines and arginines in the 49 kDa subunit of mitochondrial complex I J. Biol. Chem. 279, 21193-21199 (Pubitemid 38656523)
41. 3H]dihydrorotenone FEBS Lett. 219, 108-113
42. Earley, F. G. and Ragan, C. I. (1984) Photoaffinity labelling of mitochondrial NADH dehydrogenase with arylazidoamorphigenin, an analogue of rotenone Biochem. J. 224, 525-534
43. Yagi, T. and Hatefi, Y. (1988) Identification of the DCCD-binding subunit of NADH-ubiquinone oxidoreductase (complex I) J. Biol. Chem. 263, 16150-16155
44. Schuler, F. and Casida, J. E. (2001) Functional coupling of PSST and ND1 subunits in NADH:ubiquinone oxidoreductase established by photoaffinity labeling Biochim. Biophys. Acta 1506, 79-87
45. Sekiguchi, K., Murai, M., and Miyoshi, H. (2009) Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I Biochim. Biophys. Acta 1787, 1106-1111
46. Kakutani, N., Murai, M., Sakiyama, N., and Miyoshi, H. (2010) Exploring the Binding Site of Δlac-Acetogenin in Bovine Heart Mitochondrial NADH-Ubiquinone Oxidoreductase Biochemistry 49, 4794-4803
47. Kurki, S., Zickermann, V., Kervinen, M., Hassinen, I., and Finel, M. (2000) Mutagenesis of Three Conserved Glu Residues in a Bacterial Homologue of the ND1 Subunit of Complex I Affects Ubiquinone Reduction Kinetics but Not Inhibition by Dicyclohexylcarbodiimide Biochemistry 39, 13496-13502
48. Efremov, R. G., Baradaran, R., and Sazanov, L. A. (2010) The architecture of respiratory complex I Nature 465, 441-445
49. Perales-Clemente, E., Fernandez-Vizarra, E., Acin-Perez, R., Movilla, N., Bayona-Bafaluy, M. P., Moreno-Loshuertos, R., Perez-Martos, A., Fernandez-Silva, P., and Enriquez, J. A. (2010) Five Entry Points of the Mitochondrially Encoded Subunits in Mammalian Complex I Assembly Mol. Cell. Biol. 30, 3038-3047
50. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680-685