The mitochondrial-encoded subunits of respiratory complex I (NADH:ubiquinone oxidoreductase): Identifying residues important in mechanism and disease

Biochemical Society Transactions

Volumn 39, Issue 3, 2011, Pages 799-806

  Bridges, Hannah R ^a   Birrell, James A ^a   Hirst, Judy ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Mitochondrial disease; Mitochondrial DNA mutation (mtDNA mutation); Mitochondrion; NADH:ubiquinone oxidoreductase (complex I); ND subunit

Indexed keywords

AMINO ACID; MEMBRANE PROTEIN; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINONE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ATAXIA; BACTERIUM; CARDIOMYOPATHY; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; CONFERENCE PAPER; CYTOPLASM; DEGENERATIVE DISEASE; DIABETES MELLITUS; DYSTONIA; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HYDROPHOBICITY; INSULIN DEPENDENT DIABETES MELLITUS; LEBER HEREDITARY OPTIC NEUROPATHY; LEIGH DISEASE; MAMMAL; MASS SPECTROMETRY; MELAS SYNDROME; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OPTIC NERVE DISEASE; OXIDATION REDUCTION STATE; PARACOCCUS DENITRIFICANS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; RHODOBACTER CAPSULATUS; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; DISEASE; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; NAD; OXIDATION-REDUCTION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA;

EID: 79957512037     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390799     Document Type: Conference Paper

References (46)

1. Hirst, J. (2010) Towards the molecular mechanism of respiratory complex I. Biochem. J. 425, 327-339
2. Efremov, R.G., Baradaran, R. and Sazanov, L.A. (2010) The architecture of respiratory complex I. Nature 465, 441-447
3. Hunte, C., Zickermann, V. and Brandt, U. (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329, 448-451
4. Sazanov, L.A. and Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311, 1430-1436 (Pubitemid 43376691)
5. 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
6. Hirst, J., Carroll, J., Fearnley, I.M., Shannon, R.J. and Walker, J.E. (2003) The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 1604, 135-150
7. Chomyn, A., Cleeter, M.W.J., Ragan, C.I., Riley, M., Doolittle, R.F. and Attardi, G. (1986) URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234, 614-618
8. Cardol, P., Lapaille, M., Minet, P., Franck, F., Matagne, R. and Remacle, C. (2006) ND3 and ND4L subunits of mitochondrial complex I, both nucleus encoded in Chlamydomonas reinhardtii, are required for activity and assembly of the enzyme. Eukaryotic Cell 5, 1460-1467 (Pubitemid 44423644)
9. Mathiesen, C. and Hägerhäll, C. (2002) Transmembrane topology of the NuoL, M and N subunits of NADH:ubiquinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters. Biochim. Biophys. Acta 1556, 121-132
10. Baranova, E.A., Morgan, D.J. and Sazanov, L.A. (2007) Single particle analysis confirms distal location of subunits NuoL and NuoM in Escherichia coli complex I. J. Struct. Biol. 159, 238-242
11. Birrell, J.A. and Hirst, J. (2010) Truncation of subunit ND2 disrupts the threefold symmetry of the antiporter-like subunits in complex I from higher metazoans. FEBS Lett. 584, 4247-4252
12. 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
13. Roth, R. and Hägerhäll, C. (2001) Transmembrane orientation and topology of the NADH:quinone oxidoreductase putative quinone binding subunit NuoH. Biochim. Biophys. Acta 1504, 352-362
14. 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
15. 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
16. Gingrich, J.R., Pelkey, K.A., Fam, S.R., Huang, Y., Petralia, R.S., Wenthold, R.J. and Salter, M.W. (2004) Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc. Natl. Acad. Sci. U.S.A. 101, 6237-6242
17. Torres-Bacete, J., Sinha, P.K., Castro-Guerrero, N., Matsuno-Yagi, A. and Yagi, T. (2009) Features of subunit NuoM(ND4) subunit in Escherichia coli NDH-1. J. Biol. Chem. 284, 33062-33069
18. +. J. Biol. Chem 278, 26817-16822
19. Di Bernardo, S., Yano, T. and Yagi, T. (2000) Exploring the membrane domain of the reduced nicotinamide adenine dinucleotide-quinone oxidoreductase of Paracoccus denitrificans: characterisation of the NQO7 subunit. Biochemistry 39, 9411-9418 (Pubitemid 30626331)
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:Q oxidoreductase from Escherichia coli. J. Biol. Chem 279, 32360-32366 (Pubitemid 39014689)
21. Kao, M.-C., Di Bernardo, S., Matsuno-Yagi, A. and Yagi, T. (2002) Characterisation of the membrane domain Nqo11 subunit of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. Biochemistry 41, 4377-4384 (Pubitemid 34259881)
22. Kervinen, M., Pätsi, J., Finel, M. and Hassinen, I. (2004) A pair of membrane embedded acidic residues in the NuoK subunit of Escherichia coli NDH-1, a counterpart of the ND4L subunit of complex I, are required for high ubiquinone reductase activity. Biochemistry 43, 773-781 (Pubitemid 38114065)
23. Kao, M.-C., Nakamaru-Ogiso, E., Matsuno-Yagi, A. and Yagi, T. (2005) Characterisation of the membrane domain NuoK (ND4L) NADH-quinone oxidoreductase of Escherichia coli. Biochemistry 44, 9545-9554 (Pubitemid 40962053)
24. Kao, M.-C., Di Bernardo, S., Matsuno-Yagi, A. and Yagi, T. (2003) Characterisation and topology of the membrane domain Nqo10 subunit of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. Biochemistry 42, 4534-4543 (Pubitemid 36457622)
25. Kao, M.-C., Di Bernardo, S., Nakamaru-Ogiso, E., Miyoshi, H., Matsuno-Yagi, A. and Yagi, T. (2005) Characterisation of the membrane domain NuoJ (ND6) NADH-quinone oxidoreductase of Escherichia coli by chromosomal DNA manipulation. Biochemistry 44, 3562-3571 (Pubitemid 40322025)
26. Carroll, J., Altman, M.C., Fearnely, I.M. and Walker, J.E. (2007) Identification of membrane proteins by tandem mass spectrometry of protein ions. Proc. Natl. Acad. Sci. U.S.A. 104, 14330-14335
27. Lang, B.F., Laforest, M.-J. and Burger, G. (2007) Mitochondrial introns: a critical view. Trends Genet. 23, 119-125
28. Zickermann, V., Barquera, B., Wikström, M. and Finel, M. (1998) Analysis of the pathogenic human mitochondrial mutation ND1/3460, and mutations of strictly conserved residues in its vicinity, using the bacterium Paracoccus denitrificans. Biochemistry 37, 11792-11796 (Pubitemid 28400050)
29. Kervinen, M., Hinttala, R., Helander, H.M., Kurki, S., Uusimaa, J., Finel, M., Majamaa, K. and Hassinen, I. (2006) The MELAS mutations 3946 and 3949 perturb the critical structure in a conserved loop of the ND1 subunit of mitochondrial complex I. Hum. Mol. Genet. 15, 2543-2552
30. Torres-Bacete, J., Nakamaru-Ogiso, E., Matsuno-Yagi, A. and Yagi, T. (2007) Characterisation of the NuoM(ND4) subunit in Escherichia coli NDH-1. J. Biol. Chem. 282, 36914-36922
31. 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
32. Nakamura-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 Escherichia coli complex I. J. Biol. Chem. 285, 39070-39078
33. Pätsi, J., Kervinen, M., Finel, M. and Hassinen, I.E. (2008) Leber hereditary optic neuropathy mutations in the ND6 subunit of mitochondrial complex I affect ubiquinone reduction kinetics in a bacterial model of the enzyme. Biochem. J. 409, 129-137
34. Yadava, N., Potluri, P., Smith, E.N., Bisevac, A. and Scheffler, I.E. (2002) Species specific and mutant MWFE proteins. J. Biol. Chem. 277, 21221-21230
35. Mitchell, A.L., Elson, J.L., Howell, N., Taylor, R.W. and Turnbull, D.M. (2006) Sequence variation in mitochondrial complex I genes: mutation or polymorphism? J. Med. Genet. 43, 175-179
36. Brandon, M.C., Lott, M.T., Nguyen, K.C., Spolim, S., Navathe, S.B., Baldi, P. and Wallace, D.C. (2005) MITOMAP: a human mitochondrial genome database - 2004 update. Nucleic Acids Res. 33, D611-D613 (Pubitemid 40207946)
37. Lunardi, J., Darrouzet, E., Dupuis, A. and Issartel, J.-P. (1998) The nuoM arg368his mutation in NADH:ubiquinone oxidoreductase from Rhodobacter capsulatus: a model for the human nd4-11778 mtDNA mutation associated with Leber's hereditary optic neuropathy. Biochim. Biophys. Acta 1407, 114-124
38. Chen, J., Hattori, Y., Nakajima, K., Eizawa, T., Ehara, T., Koyama, T., Hirai, T., Fukuda, Y., Kinoshita, M., Sugiyama, A. et al. (2006) Mitochondrial complex I activity is significantly decreased in a patient with maternally inherited type 2 diabetes mellitus and hypertrophic cardiomyopathy associated with mitochondrial DNA C3310T mutation: a cybrid study. Diabetes Res. Clin. Pract. 74, 148-153
39. Jaksch, M., Hofmann, S., Kaufhold, P., Obermaier-Kusser, B., Zierz, S. and Gerbitz, K.-D. (1996) A novel combination of mitochondria1 tRNA and ND1 gene mutations in a syndrome with MELAS, cardiomyopathy, and diabetes mellitus. Hum. Mutat. 7, 358-360
40. Malfatti, E., Bugiani, M., Invernizzi, F., Fischinger-Moura de Souza, C., Farina, L., Carrara, F., Lamantea, E., Antozzi, C., Confalonieri, P., Sanseverino, M.T. et al. (2007) Novel mutations of ND genes in complex I deficiency associated with mitochondrial encephalopathy. Brain 130, 1894-1904 (Pubitemid 47343808)
41. Ugalde, C., Hinttala, R., Timal, S., Smeets, R., Rodenburg, R.J.T., Uusimaa, J., van Heuvel, L.P., Nijtmans, L.G.J., Majamaa, K. and Smeitink, J.A.M. (2007) Mutated ND2 impairs mitochondrial complex I assembly and leads to Leigh syndrome. Mol. Genet. Metab. 90, 10-14
42. Ohkubo, E., Aida, K., Chen, J., Hayashi, J.-I., Isobe, K., Tawata, M. and Onaya, T. (2000) A patient with type 2 diabetes mellitus associated with mutations in calcium sensing receptor gene and mitochondrial DNA. Biochem. Biophys. Res. Commun. 278, 808-813
43. Sarzi, E., Brown, M.D., Lebon, S., Chretien, D., Munnich, A., Rotig, A. and Procaccio, V. (2007) A novel recurrent mitochondrial DNA mutation in ND3 gene is associated with isolated complex I deficiency causing Leigh syndrome and dystonia. Am. J. Med. Genet. Part A 143, 33-41
44. Shanske, S., Coku, J., Lu, J., Ganesh, J., Krishna, S., Tanji, K., Bonilla, E., Naini, A.B., Hirano, M. and DiMauro, S. (2008) The G13513A mutation in the ND5 gene of mitochondrial DNA as a common cause of MELAS or Leigh syndrome: evidence from 12 cases. Arch. Neurol. 65, 368-372
45. Valente, L., Piga, D., Lamantea, E., Carrara, F., Uziel, G., Cudia, P., Zani, A., Farina, L., Morandi, L., Mora, M. et al. (2009) Identification of novel mutations in five patients with mitochondrial encephalomyopathy. Biochim. Biophys. Acta 1787, 491-501
46. Tawata, M., Hayashi, J.-I., Isobe, K., Ohkubo, E., Ohtaka, M., Chen, J., Aida, K. and Onaya, T. (2000) A new mitochondrial DNA mutation at 14577 T/C is probably a major pathogenic mutation for maternally inherited type 2 diabetes. Diabetes 49, 1269-1272 (Pubitemid 30439105)