LHON/MELAS overlap mutation in ND1 subunit of mitochondrial complex i affects ubiquinone binding as revealed by modeling in Escherichia coli NDH-1

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 2, 2012, Pages 312-318

  Pätsi, Jukka ^a   Maliniemi, Pilvi ^a   Pakanen, Salla ^a,b   Hinttala, Reetta ^a,b   Uusimaa, Johanna ^a,b   Majamaa, Kari ^a,b   Nyström, Thomas ^c   Kervinen, Marko ^a,b   Hassinen, Ilmo E ^a  

^a UNIVERSITY OF OULU   (Finland)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Escherichia coli; Leber hereditary optic neuropathy; MELAS; Mitochondria; NADH ubiquinone oxidoreductase; Ubiquinone

Indexed keywords

ESCHERICHIA COLI PROTEIN; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINONE;

ARTICLE; DISEASE ASSOCIATION; DNA DETERMINATION; ENZYME ACTIVITY; ESCHERICHIA COLI; LEBER HEREDITARY OPTIC NEUROPATHY; MELAS SYNDROME; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SUBUNIT; SITE DIRECTED MUTAGENESIS; SUBSTITUTION REACTION;

AMINO ACID SEQUENCE; ANIMALS; ELECTRON TRANSPORT COMPLEX I; ESCHERICHIA COLI PROTEINS; HUMANS; MELAS SYNDROME; MEMBRANE PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NADH DEHYDROGENASE; OPTIC ATROPHY, HEREDITARY, LEBER; PROTEIN BINDING; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUINONE;

ESCHERICHIA COLI;

EID: 84655167298     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.10.014     Document Type: Article

References (58)

1. J. Carroll, I.M. Fearnley, J.M. Skehel, R.J. Shannon, J. Hirst, and J.E. Walker Bovine complex I is a complex of 45 different subunits J. Biol. Chem. 281 2006 32724 32727 (Pubitemid 46036828)
2. U. Brandt Energy converting NADH:quinone oxidoreductase (complex I) Annu. Rev. Biochem. 75 2006 69 92 (Pubitemid 44118026)
3. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436 (Pubitemid 43376691)
4. R.G. Efremov, and L.A. Sazanov Structure of the membrane domain of respiratory complex I Nature 476 2011 414 420
5. C. Hunte, V. Zickermann, and U. Brandt Functional modules and structural basis of conformational coupling in mitochondrial complex I Science 329 2010 448 451
6. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
7. N. Kashani-Poor, K. Zwicker, S. Kerscher, and U. Brandt A central functional role for the 49-kDa subunit within the catalytic core of mitochondrial complex I J. Biol. Chem. 276 2001 24082 24087
8. M.A. Tocilescu, U. Fendel, K. Zwicker, S. Kerscher, and U. Brandt Exploring the ubiquinone binding cavity of respiratory complex I J. Biol. Chem. 282 2007 29514 29520 (Pubitemid 350043352)
9. M.A. Tocilescu, U. Fendel, K. Zwicker, S. Drose, S. Kerscher, and U. Brandt The role of a conserved tyrosine in the 49-kDa subunit of complex I for ubiquinone binding and reduction Biochim. Biophys. Acta 1797 2010 625 632
10. U. Fendel, M.A. Tocilescu, S. Kerscher, and U. Brandt Exploring the inhibitor binding pocket of respiratory complex I Biochim. Biophys. Acta 1777 2008 660 665
11. P.M. Ahlers, K. Zwicker, S. Kerscher, and U. Brandt Function of conserved acidic residues in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica J. Biol. Chem. 275 2000 23577 23582 (Pubitemid 30624640)
12. T. Friedrich, P. van Heek, H. Leif, T. Ohnishi, E. Forche, B. Kunze, R. Jansen, W. Trowitzsch-Kienast, G. Hofle, and H. Reichenbach Two binding sites of inhibitors in NADH: ubiquinone oxidoreductase (complex I). Relationship of one site with the ubiquinone-binding site of bacterial glucose:ubiquinone oxidoreductase Eur. J. Biochem. 219 1994 691 698 (Pubitemid 24053688)
13. J.G. Okun, P. Lümmen, and U. Brandt Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH:ubiquinone oxidoreductase) J. Biol. Chem. 274 1999 2625 2630 (Pubitemid 29075339)
14. P.K. Sinha, J. Torres-Bacete, E. Nakamaru-Ogiso, N. Castro-Guerrero, A. Matsuno-Yagi, and T. Yagi 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 2009 9814 9823
15. E.A. Baranova, P.J. Holt, and L.A. Sazanov Projection structure of the membrane domain of Escherichia coli respiratory complex I at 8 A resolution J. Mol. Biol. 366 2007 140 154 (Pubitemid 46123333)
16. (Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies Nature 348 1990 651 653 (Pubitemid 120015131)
17. Y. Kirino, T. Yasukawa, S. Ohta, S. Akira, K. Ishihara, K. Watanabe, and T. Suzuki Codon-specific translational defect caused by a wobble modification deficiency in mutant tRNA from a human mitochondrial disease Proc. Natl. Acad. Sci. U. S. A. 101 2004 15070 15075 (Pubitemid 39391720)
18. D.R. Dunbar, P.A. Moonie, M. Zeviani, and I.J. Holt Complex I deficiency is associated with 3243G:C mitochondrial DNA in osteosarcoma cell cybrids Hum. Mol. Genet. 5 1996 123 129 (Pubitemid 26018283)
19. M. Kervinen, R. Hinttala, H.M. Helander, S. Kurki, J. Uusimaa, M. Finel, K. Majamaa, and I.E. Hassinen 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 2006 2543 2552 (Pubitemid 44288684)
20. D.M. Kirby, R. McFarland, A. Ohtake, C. Dunning, M.T. Ryan, C. Wilson, D. Ketteridge, D.M. Turnbull, D.R. Thorburn, and R.W. Taylor Mutations of the mitochondrial ND1 gene as a cause of MELAS J. Med. Genet. 41 2004 784 789 (Pubitemid 39389297)
21. E. Malfatti, M. Bugiani, F. Invernizzi, C.F. de Souza, L. Farina, F. Carrara, E. Lamantea, C. Antozzi, P. Confalonieri, M.T. Sanseverino, R. Giugliani, G. Uziel, and M. Zeviani Novel mutations of ND genes in complex I deficiency associated with mitochondrial encephalopathy Brain 130 2007 1894 1904 (Pubitemid 47343808)
22. G. Lenaz, A. Baracca, V. Carelli, M. D'Aurelio, G. Sgarbi, and G. Solaini Bioenergetics of mitochondrial diseases associated with mtDNA mutations Biochim. Biophys. Acta 1658 2004 89 94 (Pubitemid 39013238)
23. E.L. Blakely, R. de Silva, A. King, V. Schwarzer, T. Harrower, G. Dawidek, D.M. Turnbull, and R.W. Taylor LHON/MELAS overlap syndrome associated with a mitochondrial MTND1 gene mutation Eur. J. Hum. Genet. 13 2005 623 627 (Pubitemid 40691403)
24. J. Montoya, E. Lopez-Gallardo, C. Diez-Sanchez, M.J. Lopez-Perez, and E. Ruiz-Pesini 20 years of human mtDNA pathologic point mutations: carefully reading the pathogenicity criteria Biochim. Biophys. Acta 1787 2009 470 483
25. J. Pätsi, M. Kervinen, M. Finel, and I.E. Hassinen 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 2008 129 137
26. V. Zickermann, B. Barquera, M. Wikström, and M. Finel 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 1998 11792 11796 (Pubitemid 28400050)
27. J. Lunardi, E. Darrouzet, A. Dupuis, and J.P. Issartel 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 1998 114 124 (Pubitemid 28345161)
28. P. Maliniemi, M. Kervinen, and I.E. Hassinen Modeling of human pathogenic mutations in Escherichia coli complex I reveals a sensitive region in the fourth inside loop of NuoH Mitochondrion 9 2009 394 401
29. M. Kervinen, J. Pätsi, M. Finel, and I.E. Hassinen A pair of membrane-embedded acidic residues in the NuoK subunit of Escherichia coli NDH-1, a counterpart of the ND4L subunit of the mitochondrial complex I, are required for high ubiquinone reductase activity Biochemistry 43 2004 773 781 (Pubitemid 38114065)
30. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K.A. Datsenko, M. Tomita, B.L. Wanner, and H. Mori Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection Mol. Syst. Biol. 2 2006 10.1038/msb4100050 (2006.0008) (Pubitemid 43948152)
31. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. U. S. A. 97 2000 6640 6645 (Pubitemid 30412767)
32. T. Pohl, M. Uhlmann, M. Kaufenstein, and T. Friedrich Lambda Red-mediated mutagenesis and efficient large scale affinity purification of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) Biochemistry 46 2007 10694 10702 (Pubitemid 47417261)
33. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
34. K. Bjorklof, V. Zickermann, and M. Finel Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues FEBS Lett. 467 2000 105 110 (Pubitemid 30069552)
35. A. Cortes, M. Cascante, M.L. Cardenas, and A. Cornish-Bowden Relationships between inhibition constants, inhibitor concentrations for 50% inhibition and types of inhibition: new ways of analysing data Biochem. J. 357 2001 263 268 (Pubitemid 32642925)
36. L. Gerencsér, L. Rinyu, L. Kálmán, E. Takahashi, C.A. Wraight, and P. Maróti Competitive binding of quinone and antibiotic stigmatellin to reaction centers of photosynthetic bacteria Acta Biol. Szeged. 48 2004 25 33 (Pubitemid 40514472)
37. J. Torres-Bacete, E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1: conserved charged residues essential for energy-coupled activities J. Biol. Chem. 282 2007 36914 36922
38. H. Schägger Native electrophoresis for isolation of mitochondrial oxidative phosphorylation protein complexes Methods Enzymol. 260 1995 190 202
39. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680 (Pubitemid 24354800)
40. A. Krogh, B. Larsson, G. von Heijne, and E.L. Sonnhammer Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 305 2001 567 580 (Pubitemid 33032862)
41. A. Majander, M. Finel, M.L. Savontaus, E. Nikoskelainen, and M. Wikström Catalytic activity of complex I in cell lines that possess replacement mutations in the ND genes in Leber's hereditary optic neuropathy Eur. J. Biochem. 239 1996 201 207 (Pubitemid 26228161)
42. L. Sinegina, M. Wikström, M.I. Verkhovsky, and M.L. Verkhovskaya Activation of isolated NADH:ubiquinone reductase I (complex I) from Escherichia coli by detergent and phospholipids. Recovery of ubiquinone reductase activity and changes in EPR signals of iron-sulfur clusters Biochemistry 44 2005 8500 8506 (Pubitemid 40799931)
43. L.J. Wong Pathogenic mitochondrial DNA mutations in protein-coding genes Muscle Nerve 36 2007 279 293
44. R. Hinttala, M. Kervinen, J. Uusimaa, P. Maliniemi, S. Finnila, H. Rantala, A.M. Remes, I.E. Hassinen, and K. Majamaa Analysis of functional consequences of haplogroup J polymorphisms m.4216T>C and m.3866T>C in human MT-ND1: mutagenesis of homologous positions in Escherichia coli Mitochondrion 10 2010 358 361
45. S. Kurki, V. Zickermann, M. Kervinen, I. Hassinen, and M. Finel 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 2000 13496 13502
46. M.S. Sharpley, R.J. Shannon, F. Draghi, and J. Hirst Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria Biochemistry 45 2006 241 248 (Pubitemid 43054102)
47. L.A. Sazanov, J. Carroll, P. Holt, L. Toime, and I.M. Fearnley A role for native lipids in the stabilization and two-dimensional crystallization of the Escherichia coli NADH-ubiquinone oxidoreductase (complex I) J. Biol. Chem. 278 2003 19483 19491 (Pubitemid 36799345)
48. M.S. King, M.S. Sharpley, and J. Hirst Reduction of hydrophilic ubiquinones by the flavin in mitochondrial NADH:ubiquinone oxidoreductase (Complex I) and production of reactive oxygen species Biochemistry 48 2009 2053 2062
49. A. Ghelli, M. Degli Esposti, V. Carelli, and G. Lenaz Changes in mitochondrial complex I activity and coenzyme Q binding site in Leber's hereditary optic neuropathy (LHON) Mol. Aspects Med. 18 Suppl 1997 S263 S267
50. N. Kakutani, M. Murai, N. Sakiyama, and H. Miyoshi Exploring the binding site of delta(lac)-acetogenin in bovine heart mitochondrial NADH-ubiquinone oxidoreductase Biochemistry 49 2010 4794 4803
51. M.A. Grönlund, A.K. Honarvar, S. Andersson, A.R. Moslemi, A. Oldfors, E. Holme, M. Tulinius, and N. Darin Ophthalmological findings in children and young adults with genetically verified mitochondrial disease Br. J. Ophthalmol. 94 2010 121 127
52. P. Yu-Wai-Man, P.G. Griffiths, and P.F. Chinnery Mitochondrial optic neuropathies - disease mechanisms and therapeutic strategies Prog. Retin. Eye Res. 30 2011 81 114
53. R. Horvath, R. Reilmann, E. Holinski-Feder, E.B. Ringelstein, and T. Klopstock The role of complex I genes in MELAS: a novel heteroplasmic mutation 3380G>A in ND1 of mtDNA Neuromuscul. Disord. 18 2008 553 556
54. M. Liang, M. Guan, F. Zhao, X. Zhou, M. Yuan, Y. Tong, L. Yang, Q.P. Wei, Y.H. Sun, F. Lu, J. Qu, and M.X. Guan Leber's hereditary optic neuropathy is associated with mitochondrial ND1 T3394C mutation Biochem. Biophys. Res. Commun. 383 2009 286 292
55. R. Matsuoka, M. Furutani, J. Hayashi, K. Isobe, K. Akimoto, T. Shibata, S. Imamura, M. Tatsuguchi, Y. Furutani, A. Takao, S. Ohnishi, H. Kasanuki, and K. Momma A mitochondrial DNA mutation cosegregates with the pathophysiological U wave Biochem. Biophys. Res. Commun. 257 1999 228 233 (Pubitemid 29300645)
56. M.D. Brown, J.M. Shoffner, Y.L. Kim, A.S. Jun, B.H. Graham, M.F. Cabell, D.S. Gurley, and D.C. Wallace Mitochondrial DNA sequence analysis of four Alzheimer's and Parkinson's disease patients Am. J. Med. Genet. 61 1996 283 289
57. K. Huoponen, J. Vilkki, P. Aula, E.K. Nikoskelainen, and M.L. Savontaus A new mtDNA mutation associated with Leber hereditary optic neuroretinopathy Am. J. Hum. Genet. 48 1991 1147 1153
58. A.R. Moslemi, N. Darin, M. Tulinius, L.M. Wiklund, E. Holme, and A. Oldfors Progressive encephalopathy and complex I deficiency associated with mutations in MTND1 Neuropediatrics 39 2008 24 28 (Pubitemid 351828313)