Conserved amino acid residues of the NuoD segment important for structure and function of Escherichia coli NDH-1 (complex I)

Biochemistry

Volumn 54, Issue 3, 2015, Pages 753-764

  Sinha, Prem Kumar ^a,c   Castro Guerrero, Norma ^a,d   Patki, Gaurav ^a,e   Sato, Motoaki ^a,f   Torres Bacete, Jesus ^a,g   Sinha, Subhash ^a,h   Miyoshi, Hideto ^b   Matsuno Yagi, Akemi ^a   Yagi, Takao ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

^e UNIVERSITY OF HOUSTON   (United States)

^f NIPPON SODA CO LTD   (Japan)

^g CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^h ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI;

AMINO ACID RESIDUES; BINDING CAVITY; CONSERVED RESIDUES; DNA RECOMBINATION; HYDROPHILIC DOMAINS; MEMBRANE DOMAIN; OXIDOREDUCTASES; STRUCTURAL MODELING;

AMINO ACIDS;

AMINO ACID; ARGININE; CAPSAICIN; ESCHERICHIA COLI PROTEIN; GLYCINE; HISTONE; NUOA PROTEIN; NUOB PROTEIN; NUOC PROTEIN; NUOD PROTEIN; NUOH PROTEIN; PHENYLALANINE; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE); TYROSINE; UNCLASSIFIED DRUG; ENZYME INHIBITOR; MEMBRANE PROTEIN; MUTANT PROTEIN; NUOCD PROTEIN, E COLI; NUOH PROTEIN, E COLI; OXIDOREDUCTASE; PROTEIN SUBUNIT; PROTON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; DNA RECOMBINATION; ENZYME ACTIVITY; ESCHERICHIA COLI; IC50; MEMBRANE POTENTIAL; MEMBRANE VESICLE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; PROTON TRANSPORT; THERMUS THERMOPHILUS; CHEMISTRY; CONSERVED SEQUENCE; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; MUTATION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION;

ESCHERICHIA COLI;

AMINO ACID SEQUENCE; AMINO ACIDS; CONSERVED SEQUENCE; ELECTRON TRANSPORT COMPLEX I; ENZYME INHIBITORS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNOBLOTTING; INHIBITORY CONCENTRATION 50; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OXIDOREDUCTASES; PROTEIN SUBUNITS; PROTONS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84921860784     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501403t     Document Type: Article

References (63)

1. Yagi, T. and Matsuno-Yagi, A. (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: The secret unlocked Biochemistry 42, 2266-2274
2. Brandt, U. (2006) Energy Converting NADH:Quinone Oxidoreductase (Complex I) Annu. Rev. Biochem. 75, 69-92
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. Balsa, E., Marco, R., Perales-Clemente, E., Szklarczyk, R., Calvo, E., Landazuri, M. O., and Enriquez, J. A. (2012) NDUFA4 Is a Subunit of Complex IV of the Mammalian Electron Transport Chain Cell Metab. 16, 378-386
5. Sinha, P. K., Castro-Guerrero, N., Matsuno-Yagi, A., Yagi, T., and Torres-Bacete, J. (2009) Bacterial complex I (NDH-1): Functional roles of the hydrophobic domain Curr. Topics Biochem. Res. 11, 79-90
6. Yagi, T., Di Bernardo, S., Nakamaru-Ogiso, E., Kao, M. C., Seo, B. B., and Matsuno-Yagi, A. (2004) NADH Dehydrogenase (NADH-Quinone Oxidoreductase). In Advances in Photosynthesis and Respiration; Respiration in Archaea and Bacteria (Zannoni, D., Ed.) Vol. 15, pp 15-40, Kluwer Academic Publishers, Dordrecht.
7. 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
8. Efremov, R. G. and Sazanov, L. A. (2011) Respiratory complex I: 'steam engine' of the cell? Curr. Opin. Struct. Biol. 21, 532-540
9. Matsuno-Yagi, A. and Yagi, T. (2001) Introduction: complex I - an L-shaped black box J. Bioenerg. Biomembr. 33, 155-157
10. Hinchliffe, P. and Sazanov, L. A. (2005) Organization of iron-sulfur clusters in respiratory complex I Science 309, 771-774
11. Sazanov, L. A. and Hinchliffe, P. (2006) Structure of the Hydrophilic Domain of Respiratory Complex I from Thermus thermophilus Science 311, 1430-1436
12. Friedrich, T. (2014) On the mechanism of respiratory complex I J. Bioenerg. Biomembr. 46, 255-268
13. 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
14. 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
15. 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
16. 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
17. 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
18. Sato, M., Sinha, P. K., Torres-Bacete, J., Matsuno-Yagi, A., and Yagi, T. (2013) Energy transducing roles of antiporter-like subunits in E. coli NDH-1 with main focus on subunit NuoN (ND2) J. Biol. Chem. 288, 24705-24716
19. Efremov, R. G. and Sazanov, L. A. (2011) Structure of the membrane domain of respiratory complex I Nature 476, 414-420
20. Efremov, R. G., Baradaran, R., and Sazanov, L. A. (2010) The architecture of respiratory complex I Nature 465, 441-445
21. Hunte, C., Zickermann, V., and Brandt, U. (2010) Functional Modules and Structural Basis of Conformational Coupling in Mitochondrial Complex I Science 329, 448-451
22. 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
23. Murai, M., Mashimo, Y., Hirst, J., and Miyoshi, H. (2011) Exploring Interactions between the 49 kDa and ND1 Subunits in Mitochondrial NADH-Ubiquinone Oxidoreductase (Complex I) by Photoaffinity Labeling Biochemistry 50, 6901-6908
24. Murai, M., Ishihara, A., Nishioka, T., Yagi, T., and Miyoshi, H. (2007) The ND1 Subunit Constructs the Inhibitor Binding Domain in Bovine Heart Mitochondrial Complex I Biochemistry 46, 6409-6416
25. Ohshima, M., Miyoshi, H., Sakamoto, K., Takegami, K., Iwata, J., Kuwabara, K., Iwamura, H., and Yagi, T. (1998) Characterization of the ubiquinone reduction site of mitochondrial complex I using bulky synthetic ubiquinones Biochemistry 37, 6436-6445
26. 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
27. Masuya, T., Murai, M., Ifuku, K., Morisaka, H., and Miyoshi, H. (2014) Site-specific chemical labeling of mitochondrial respiratory complex I through ligand-directed tosylate chemistry Biochemistry 53, 2307-2317
28. 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
29. Tocilescu, M. A., Fendel, U., Zwicker, K., Kerscher, S., and Brandt, U. (2007) Exploring the ubiquinone binding cavity of respiratory complex I J. Biol. Chem. 282, 29514-29520
30. Tocilescu, M. A., Zickermann, V., Zwicker, K., and Brandt, U. (2010) Quinone binding and reduction by respiratory complex I Biochim. Biophys. Acta 1797, 1883-1890
31. Zickermann, V., Kerscher, S., Zwicker, K., Tocilescu, M. A., Radermacher, M., and Brandt, U. (2009) Architecture of complex I and its implications for electron transfer and proton pumping Biochim. Biophys. Acta 1787, 574-583
32. 3H]dihydrorotenone FEBS Lett. 219, 108-113
33. Ichimaru, N., Murai, M., Kakutani, N., Kako, J., Ishihara, A., Nakagawa, Y., Nishioka, T., Yagi, T., and Miyoshi, H. (2008) Synthesis and Characterization of New Piperazine-Type Inhibitors for Mitochondrial NADH-Ubiquinone Oxidoreductase (Complex I) Biochemistry 47, 10816-10826
34. 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
35. 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
36. Sato, M., Torres-Bacete, J., Sinha, P. K., Matsuno-Yagi, A., and Yagi, T. (2014) Essential regions in the membrane domain of bacterial complex I (NDH-1): the machinery for proton translocation J. Bioenerg. Biomembr. 46, 279-287
37. Yagi, T., Torres-Bacete, J., Sinha, P. K., Castro-Guerrero, N., and Matsuno-Yagi, A. (2012) in A Structural Perspective on Respiratory Complex I (Sazanov, L., Ed.) pp 147-169, Springer, Chambersburg.
38. 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
39. Sinha, S. C., Sinha, S. C., and Keinan, E. (1999) Total Synthesis of Squamotacin J. Org. Chem. 64, 7067-7073
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. 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
42. Ghelli, A., Benelli, B., and Degli Esposti, M. (1997) Measurement of the membrane potential generated by complex I in submitochondrial particles J. Biochem. (Tokyo) 121, 746-755
43. 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
44. 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
45. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., and Schwede, T. (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Nucleic Acids Res. 42, W252-W258
46. 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
47. Belevich, G., Euro, L., Wikstrom, M., and Verkhovskaya, M. (2007) Role of the Conserved Arginine 274 and Histidine 224 and 228 Residues in the NuoCD Subunit of Complex I from Escherichia coli Biochemistry 46, 526-533
48. Flemming, D., Hellwig, P., and Friedrich, T. (2003) Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase J. Biol. Chem. 278, 3055-3062
49. Matsushita, K., Ohnishi, T., and Kaback, H. R. (1987) NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain Biochemistry 26, 7732-7737
50. Tocilescu, M. A., Fendel, U., Zwicker, K., Drose, S., Kerscher, S., and Brandt, U. (2010) The role of a conserved tyrosine in the 49-kDa subunit of complex I for ubiquinone binding and reduction Biochim. Biophys. Acta 1797, 625-632
51. Marin, S. E., Mesterman, R., Robinson, B., Rodenburg, R. J., Smeitink, J., and Tarnopolsky, M. (2013) Leigh Syndrome Associated with Mitochondrial Complex I Deficiency Due to Novel Mutations In NDUFV1 and NDUFS2 Gene 516, 162-167
52. Murai, M., Sekiguchi, K., Nishioka, T., and Miyoshi, H. (2009) Characterization of the Inhibitor Binding Site in Mitochondrial NADH-Ubiquinone Oxidoreductase by Photoaffinity Labeling Using a Quinazoline-Type Inhibitor (dagger) Biochemistry 48, 688-698
53. Nakanishi, S., Abe, M., Yamamoto, S., Murai, M., and Miyoshi, H. (2011) Bis-THF motif of acetogenin binds to the third matrix-side loop of ND1 subunit in mitochondrial NADH-ubiquinone oxidoreductase Biochim. Biophys. Acta 1807, 1170-1176
54. 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
55. Nakamaru-Ogiso, E., Han, H., Matsuno-Yagi, A., Keinan, E., Sinha, S. C., Yagi, T., and Ohnishi, T. (2010) The ND2 subunit was labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor FEBS Lett. 584, 883-888
56. Murai, M. and Miyoshi, H. (2014) Chemical modifications of respiratory complex I for structural and functional studies J. Bioenerg. Biomembr. 46, 313-321
57. Sazanov, L. A. (2014) The mechanism of coupling between electron transfer and proton translocation in respiratory complex I J. Bioenerg. Biomembr. 46, 247-253
58. Rossman, M. G., Moras, D., and Olsen, K. W. (1974) Chemical and biological evolution of a nucleotide-binding protein Nature 250, 194-199
59. 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
60. Patsi, J., Maliniemi, P., Pakanen, S., Hinttala, R., Uusimaa, J., Majamaa, K., Nystrom, T., Kervinen, M., and Hassinen, I. E. (2012) LHON/MELAS overlap mutation in ND1 subunit of mitochondrial complex I affects ubiquinone binding as revealed by modeling in Escherichia coli NDH-1 Biochim. Biophys. Acta 1817, 312-318
61. Berrisford, J. M. and Sazanov, L. A. (2009) Structural basis for the mechanism of respiratory complex I J. Biol. Chem. 284, 29773-29783
62. 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
63. DeLano, W. L. (2008) The PyMOL Molecular Graphics System, DeLano Scientific LLC, Palo Alto, CA, USA, http://www.pymol.org.