Mitochondrial complex I and cell death: A semi-automatic shotgun model

Cell Death and Disease

Volumn 2, Issue 10, 2011, Pages

  Gonzalez Halphen, D ^a   Ghelli, A ^b   Iommarini, L ^b   Carelli, V ^b   Esposti, M D ^c  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Complex I; Mitochondria; Mitochondrial disease

Indexed keywords

QUINOL; QUINOLINE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

BACTERIAL CELL; BIOENERGY; BIOLOGICAL MODEL; CELL DEATH; CELL MEMBRANE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; SEMI AUTOMATIC SHOTGUN MODEL; STRUCTURE ANALYSIS; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

CELL DEATH; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIAL DISEASES;

EID: 80055007050     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.107     Document Type: Review

References (53)

1. Walker JE. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys 1992; 25: 253-324. (Pubitemid 23014370)
2. Degli Esposti M. Inhibitors of NADH-ubiquinone reductase: an overview. Biochim Biophys Acta 1998; 1364: 222-235.
3. Sharma LK, Lu J, Bai Y. Mitochondrial respiratory complex I: structure, function and implication in human diseases. Curr Med Chem 2009; 16: 1266-1277.
4. Efremov RG, Baradaran R, Sazanov LA. The architecture of respiratory complex I. Nature 2010; 465: 441-445.
5. Hunte C, Zickermann V, Brandt U. Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 2010; 329: 448-451.
6. Ohnishi T, Nakamaru-Ogiso E, Ohnishi ST. A new hypothesis on the simultaneous direct and indirect proton pump mechanisms in NADH-quinone oxidoreductase (complex I). FEBS Lett 2010; 584: 4131-4137.
7. Treberg JR, Brand MD. A model of the proton translocation mechanism of complex I. J Biol Chem 2011; 286: 17579-17584.
8. Degli Esposti M, Ghelli A. The mechanism of proton and electron transport in mitochondrial complex I. Biochim Biophys Acta 1994; 1187: 116-120. (Pubitemid 24267039)
9. Berry EA, Guergova-Kuras M, Huang LS, Crofts AR. Structure and function of cytochrome bc complexes. Annu Rev Biochem 2000; 69: 1005-1075.
10. Zickermann V, Kerscher S, Zwicker K, Tocilescu MA, Radermacher M, Brandt U. Architecture of complex I and its implications for electron transfer and proton pumping. Biochim Biophys Acta 2009; 1787: 574-583.
11. Janssen RJ, Nijtmans LG, van den Heuvel LP, Smeitink JA. Mitochondrial complex I: structure, function and pathology. J Inherit Metab Dis 2006; 29: 499-515. (Pubitemid 44193264)
12. Cardol P, Lapaille M, Minet P, Franck F, Matagne RF, Remacle C. ND3 and ND4L subunits of mitochondrial complex I, both nucleus encoded in Chlamydomonas reinhardtii, are required for activity and assembly of the enzyme. Eukaryot Cell 2006; 5: 1460-1467. (Pubitemid 44423644)
13. Pineau B, Mathieu C, Gérard-Hirne C, De Paepe R, Chétrit P. Targeting the NAD7 subunit to mitochondria restores a functional complex I and a wild type phenotype in the Nicotiana sylvestris CMS II mutant lacking nad7. J Biol Chem 2005; 280: 25994-26001. (Pubitemid 41022189)
14. Gasparre G, Porcelli AM, Bonora E, Pennisi LF, Toller M, Iommarini L et al. Disruptive mitochondrial DNA mutations in complex I subunits are markers of oncocytic phenotype in thyroid tumors. Proc Natl Acad Sci USA 2007; 104: 9001-9006. (Pubitemid 47175426)
15. Gasparre G, Iommarini L, Porcelli AM, Lang M, Ferri GG, Kurelac I et al. An inherited mitochondrial DNA disruptive mutation shifts to homoplasmy in oncocytic tumor cells. Hum Mutat 2009; 30: 391-396.
16. Valentino ML, Barboni P, Ghelli A, Bucchi L, Rengo C, Achilli A et al. The ND1 gene of complex I is a mutational hot spot for Leber's hereditary optic neuropathy. Ann Neurol 2004; 56: 631-641. (Pubitemid 39540743)
17. Bridges HR, Birrell JA, Hirst J. The mitochondrial-encoded subunits of respiratory complex I (NADH:ubiquinone oxidoreductase): identifying residues important in mechanism and disease. Biochem Soc Trans 2011; 39: 799-806.
18. Chinnery PF, Brown DT, Andrews RM, Singh-Kler R, Riordan-Eva P, Lindley J et al. The mitochondrial ND6 gene is a hot spot for mutations that cause Leber's hereditary optic neuropathy. Brain 2001; 124: 209-218. (Pubitemid 32056000)
19. Patsi J, Kervinen M, Finel M, Hassinen IE. 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 2008; 409: 129-137.
20. Carelli V, Ghelli A, Ratta M, Bacchilega E, Sangiorgi S, Mancini R et al. Leber's hereditary optic neuropathy: biochemical effect of 11778/ND4 and 3460/ND1 mutations and correlation with the mitochondrial genotype. Neurology 1997; 48: 1623-1632.
21. Carelli V, Ghelli A, Bucchi L, Montagna P, De Negri A, Leuzzi V et al. Biochemical features of mtDNA 14484 (ND6/M64V) point mutation associated with Leber's hereditary optic neuropathy. Ann Neurol 1999; 45: 320-328. (Pubitemid 29120036)
22. Ruiz-Pesini E, Lott MT, Procaccio V, Poole J, Brandon MC, Mishmar D et al. An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Res 2007; 35: D823-D828. (Pubitemid 46056316)
23. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P et al. A method and server for predicting damaging missense mutations. Nat Methods 2010; 7: 248-249.
24. Michel J, DeLeon-Rangel J, Zhu S, Van Ree K, Vik SB. Mutagenesis of the L, M, and N subunits of complex I from Escherichia coli indicates a common role in function. PLoS One 2011; 6: e17420.
25. Birrell JA, Hirst J. Truncation of subunit ND2 disrupts the threefold symmetry of the antiporter-like subunits in complex I from higher metazoans. FEBS Lett 2010; 584: 4247-4252.
26. Carr CM, Kim PS. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 1993; 73: 823-832. (Pubitemid 23159019)
27. Gruenke JA, Armstrong RT, Newcomb WW, Brown JC, White JM. New insights into the spring-loaded conformational change of influenza virus hemagglutinin. J Virol 2002; 76: 4456-4466. (Pubitemid 34309582)
28. Battchikova N, Eisenhut M, Aro EM. Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 2011; 1807: 935-944.
29. Gingrich JR, Pelkey KA, Fam SR, Huang Y, Petralia RS, Wenthold RJ et al. Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc Natl Acad Sci USA 2004; 101: 6237-6242. (Pubitemid 38520558)
30. Lunardi J, Darrouzet E, Dupuis A, Issartel JP. 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 1998; 1407: 114-124. (Pubitemid 28345161)
31. Jewess PJ. Insecticides and acaricides which act at the rotenone-binding site of mitochondrial NADH:ubiquinone oxidoreductase; competitive displacement studies using a 3H-labelled rotenone analogue. Biochem Soc Trans 1994; 22: 247-251. (Pubitemid 24072430)
32. Murai M, Ishihara A, Nishioka T, Yagi T, Miyoshi H. The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I. Biochemistry 2007; 46: 6409-6416. (Pubitemid 46842884)
33. Nakamaru-Ogiso E, Sakamoto K, Matsuno-Yagi A, Miyoshi H, Yagi T. The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry 2003; 42: 746-754. (Pubitemid 36133299)
34. Schuler F, Casida JE. Functional coupling of PSST and ND1 subunits in NADH:ubiquinone oxidoreductase established by photoaffinity labeling. Biochim Biophys Acta 2001; 1506: 79-87. (Pubitemid 32545423)
35. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 2006; 75: 69-92. (Pubitemid 44118026)
36. Esposti MD, Ghelli A. Ubiquinone and inhibitor sites in complex I: one, two or three? Biochem Soc Trans 1999; 27: 606-609. (Pubitemid 29412498)
37. Kakutani N, Murai M, Sakiyama N, Miyoshi H. Exploring the binding site of delta (lac)-acetogenin in bovine heart mitochondrial NADH-ubiquinone oxidoreductase. Biochemistry 2010; 49: 4794-4803.
38. Nakamaru-Ogiso E, Han H, Matsuno-Yagi A, Keinan E, Sinha SC, Yagi T et al. The ND2 subunit is labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor. FEBS Lett 2010; 584: 883-888.
39. Brandt U, Kerscher S, Drose S, Zwicker K, Zickermann V. Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 2003; 545: 9-17. (Pubitemid 36629630)
40. Gondal JA, Anderson WM. The molecular morphology of bovine heart mitochondrial NADH-ubiquinone reductase. Native disulfide-linked subunits and rotenone-induced conformational changes. J Biol Chem 1985; 260: 12690-12694. (Pubitemid 16230555)
41. Berrisford JM, Sazanov LA. Structural basis for the mechanism of respiratory complex I. J Biol Chem 2009; 284: 29773-29783.
42. Friedrich T, Hellwig P. Redox-induced conformational changes within the Escherichia coli NADH ubiquinone oxidoreductase (complex I): an analysis by mutagenesis and FT-IR spectroscopy. Biochim Biophys Acta 2010; 1797: 659-663.
43. Yagi T, Matsuno-Yagi A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 2003; 42: 2266-2274. (Pubitemid 36255200)
44. Degli Esposti M, Ngo A, McMullen GL, Ghelli A, Sparla F, Benelli B et al. The specificity of mitochondrial complex I for ubiquinones. Biochem J 1996; 313: 327-334. (Pubitemid 26013462)
45. Helfenbaum L, Ngo A, Ghelli A, Linnane AW, Degli Esposti M. Proton pumping of mitochondrial complex I: differential activation by analogs of ubiquinone. J Bioenerg Biomembr 1997; 29: 71-80. (Pubitemid 27114079)
46. King MS, Sharpley MS, Hirst J. Reduction of hydrophilic ubiquinones by the flavin in mitochondrial NADH:ubiquinone oxidoreductase (Complex I) and production of reactive oxygen species. Biochemistry 2009; 48: 2053-2062.
47. Ghelli A, Benelli B, Esposti MD. Measurement of the membrane potential generated by complex I in submitochondrial particles. J Biochem 1997; 121: 746-755. (Pubitemid 27170860)
48. Brandt U. A two-state stabilization-change mechanism for proton-pumping complex I. Biochim Biophys Acta 2011; 1807: 1364-1369.
49. Otero-Cruz JD, Báez-Pagán CA, Caraballo-González IM, Lasalde-Dominicci JA. Tryptophan-scanning mutagenesis in the alphaM3 transmembrane domain of the muscle-type acetylcholine receptor. A spring model revealed. J Biol Chem 2007; 282: 9162-9171. (Pubitemid 47093517)
50. Earley FG, Ragan CI. Photoaffinity labelling of mitochondrial NADH dehydrogenase with arylazidoamorphigenin, an analogue of rotenone. Biochem J 1984; 224: 525-534.
51. Spruijt RB, Wolfs CJ, Hemminga MA. Membrane assembly of M13 major coat protein: evidence for a structural adaptation in the hinge region and a tilted transmembrane domain. Biochemistry 2004; 43: 13972-13980. (Pubitemid 39482747)
52. Verkhovskaya ML, Belevich N, Euro L, Wikstrom M, Verkhovsky MI. Real-time electron transfer in respiratory complex I. Proc Natl Acad Sci USA 2008; 105: 3763-3767. (Pubitemid 351723472)
53. Kervinen M, Hinttala R, Helander HM, Kurki S, Uusimaa J, Finel M et al. 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 2006; 15: 2543-2552. (Pubitemid 44288684)