Energy transducing roles of antiporter-like subunits in Escherichia coli NDH-1 with main focus on subunit NuoN (ND2)

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24705-24716

  Sato, Motoaki ^a,b   Sinha, Prem Kumar ^a   Torres Bacete, Jesus ^a,c   Matsuno Yagi, Akemi ^a   Yagi, Takao ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NIPPON SODA CO LTD   (Japan)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE MUTANTS; GLUTAMIC ACID; INTERACTION POINTS; LYSINE RESIDUES; MEMBRANE DOMAIN; OXIDOREDUCTASES; PROTON TRANSLOCATION; TRANSMEMBRANE HELICES;

AMINO ACIDS; ESCHERICHIA COLI;

PROTONS;

ANTIPORTER; PROTEIN NUOL; PROTEIN NUOM; PROTEIN NUON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; STRUCTURE ACTIVITY RELATION;

BIOENERGETICS; ELECTRON TRANSPORT SYSTEM (ETS); MEMBRANE ENERGETICS; MEMBRANE ENZYMES; NADH DEHYDROGENASE; SITE-DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION TRANSPORT; MEMBRANE PROTEINS; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTONS;

EID: 84883180274     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.482968     Document Type: Article

References (54)

1. Brandt, U. (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75, 69-92
2. Wikström, M., and Hummer, G. (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc. Natl. Acad. Sci. U.S.A. 109, 4431-4436
3. 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
4. Sharma, L. K., Lu, J., and Bai, Y. (2009) Mitochondrial respiratory complex I. Structure, function and implication in human diseases. Curr. Med. Chem. 16, 1266-1277
5. 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
6. Yagi, T., and Matsuno-Yagi, A. (2003) The proton-translocating NADHquinone oxidoreductase in the respiratory chain. The secret unlocked. Biochemistry 42, 2266-2274
7. Efremov, R. G., Baradaran, R., and Sazanov, L. A. (2010) The architecture of respiratory complex I. Nature 465, 441-445
8. Yagi, T., and Dinh, T. M. (1990) Identification of the NADH-binding subunit of NADH-ubiquinone oxidoreductase of Paracoccus denitrificans. Biochemistry 29, 5515-5520
9. +-translocating NADH-quinone oxidoreductase (NDH-1) of Paracoccus denitrificans. Studies on topology and stoichiometry of the peripheral subunits. J. Biol. Chem. 274, 28606-28611
10. Berrisford, J. M., and Sazanov, L. A. (2009) Structural basis for the mechanism of respiratory complex I. J. Biol. Chem. 284, 29773-29783
11. Hinchliffe, P., and Sazanov, L. A. (2005) Organization of iron-sulfur clusters in respiratory complex I. Science 309, 771-774
12. Yakovlev, G., Reda, T., and Hirst, J. (2007) Reevaluating the relationship between EPR spectra and enzyme structure for the iron sulfur clusters in NADH:quinone oxidoreductase. Proc. Natl. Acad. Sci. U.S.A. 104, 12720-12725
13. Ohnishi, T., and Nakamaru-Ogiso, E. (2008) Were there any "misassignments" among iron-sulfur clusters N4, N5 and N6b in NADH-quinone oxidoreductase (complex I)? Biochim. Biophys. Acta 1777, 703-710
14. Sazanov, L. A. (2007) Respiratory complex I. Mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Bio-chemistry 46, 2275-2288
15. Sinha, P. K., Nakamaru-Ogiso, E., Torres-Bacete, J., Sato, M., Castro-Guerrero, N., Ohnishi, T., Matsuno-Yagi, A., and Yagi, T. (2012) Electron transfer in subunit NuoI (TYKY) of Escherichia coli NDH-1 (NADH:quinone oxidoreductase). J. Biol. Chem. 287, 17363-17373
16. Shiraishi, Y., Murai, M., Sakiyama, N., Ifuku, K., and Miyoshi, H. (2012) Fenpyroximate binds to the interface between PSST and 49 kDa subunits in mitochondrial NADH-ubiquinone oxidoreductase. Biochemistry 51, 1953-1963
17. Efremov, R. G., and Sazanov, L. A. (2011) Structure of the membrane domain of respiratory complex I. Nature 476, 414-420
18. Hunte, C., Zickermann, V., and Brandt, U. (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329, 448-451
19. Baradaran, R., Berrisford, J. M., Minhas, G. S., and Sazanov, L. A. (2013) Crystal structure of the entire respiratory complex I. Nature 494, 443-448
20. Mathiesen, C., and Hägerhäll, C. (2002) Transmembrane topology of the Nuo L, M and N subunits of NADH:quinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters. Biochim. Biophys. Acta 1556, 121-132
21. Kajiyama, Y., Otagiri, M., Sekiguchi, J., Kudo, T., and Kosono, S. (2009) The MrpA, MrpB, and MrpD subunits of the Mrp antiporter complex in Bacillus subtilis contain membrane-embedded and essential acidic residues. Microbiology 155, 2137-2147
22. Hedderich, R. (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles. Ancestors of complex I. J. Bioenerg. Biomembr. 36, 65-75
23. Mathiesen, C., and Hägerhäll, C. (2003) The "antiporter module" of respiratory chain Complex I includes the MrpC/NuoK subunit. A revision of the modular evolution scheme. FEBS Lett. 549, 7-13
24. 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. 285, 39070-39078
25. 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
26. 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
27. 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
28. Torres-Bacete, J., Sinha, P. K., Castro-Guerrero, N., Matsuno-Yagi, A., and Yagi, T. (2009) Features of subunit NuoM (ND4) Escherichia coli NDH-1. Topology and implication of conserved Glu-144 for coupling site 1. J. Biol. Chem. 284, 33062-33069
29. Torres-Bacete, J., Sinha, P. K., Matsuno-Yagi, A., and Yagi, T. (2011) Structural contribution of C-terminal segments of NuoL (ND5) and NuoM (ND4) subunits of complex I from Escherichia coli. J. Biol. Chem. 286, 34007-34014
30. 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
31. Torres-Bacete, J., Sinha, P. K., Sato, M., Patki, G., Kao, M. C., Matsuno-Yagi, A., and Yagi, T. (2012) Roles of subunit NuoK (ND4L) in the energy transducing mechanism of E. coli NDH-1 (NADH:quinone oxidoreductase). J. Biol. Chem. 287, 42763-42772
32. -) stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett. 451, 157-161
33. Steimle, S., Bajzath, C., Dörner, K., Schulte, M., Bothe, V., and Friedrich, T. (2011) The role of subunit NuoL for proton translocation by the respiratory complex I. Biochemistry 50, 3386-3393
34. Dröse, S., Krack, S., Sokolova, L., Zwicker, K., Barth, H. D., Morgner, N., Heide, H., Steger, M., Nübel, E., Zickermann, V., Kerscher, S., Brutschy, B., Radermacher, M., and Brandt, U. (2011) Functional dissection of the proton pumping modules of mitochondrial complex I. PLoS Biol. 9, e1001128
35. 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
36. Euro, L., Belevich, G., Verkhovsky, M. I., Wikström, M., and Verkhovskaya, M. (2008) Conserved lysine residues of the membrane subunit NuoM are involved in energy conversion by the proton-pumping NADH:ubiquinone oxidoreductase (complex I). Biochim. Biophys. Acta 1777, 1166-1172
37. 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
38. Takano, S., Yano, T., and Yagi, T. (1996) Structural studies of the protontranslocating NADH-quinone oxidoreductase (NDH-1) of Paracoccus denitrificans. Identity, property, and stoichiometry of the peripheral subunits. Biochemistry 35, 9120-9127
39. Castro-Guerrero, N., Sinha, P. K., Torres-Bacete, J., Matsuno-Yagi, A., and Yagi, T. (2010) 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 49, 10072-10080
40. 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
41. 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
42. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
43. Schägger, H., and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231
44. Yagi, T. (1986) Purification and characterization of NADHdehydrogenase complex from Paracoccus denitrificans. Arch. Biochem. Biophys. 250, 302-311
45. Matsushita, K., Ohnishi, T., and Kaback, H. R. (1987) NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry 26, 7732-7737
46. Yano, T., Sled', V. D., Ohnishi, T., and Yagi, T. (1996) Expression and characterization of the flavoprotein subcomplex composed of 50-kDa (NQO1) and 25-kDa (NQO2) subunits of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. J. Biol. Chem. 271, 5907-5913
47. Screpanti, E., and Hunte, C. (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261-267
48. Ohnishi, T. (2010) Structural biology. Piston drives a proton pump. Nature 465, 428-429
49. Belevich, G., Knuuti, J., Verkhovsky, M. I., Wikström, M., and Verkhovskaya, M. (2011) Probing the mechanistic role of the longα-helix in subunit L of respiratory Complex I from Escherichia coli by site-directed mutagenesis. Mol. Microbiol. 82, 1086-1095
50. Yagi, T. (1990) Inhibition by capsaicin of NADH-quinone oxidoreductases is correlated with the presence of energy-coupling site 1 in various organisms. Arch. Biochem. Biophys. 281, 305-311
51. Satoh, T., Miyoshi, H., Sakamoto, K., and Iwamura, H. (1996) Comparison of the inhibitory action of synthetic capsaicin analogues with var-ious NADH-ubiquinone oxidoreductases. Biochim. Biophys. Acta 1273, 21-30
52. Michel, J., DeLeon-Rangel, J., Zhu, S., Van Ree, K., and Vik, S. B. (2011) Mutagenesis of the L, M, and N subunits of complex I from Escherichia coli indicates a common role in function. PLoS ONE 6, e17420
53. Verkhovskaya, M., and Bloch, D. A. (2013) Energy-converting respiratory Complex I. On the way to the molecular mechanism of the proton pump. Int. J. Biochem. Cell Biol. 45, 491-511
54. 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