Skip to main content

Characterization of Bacterial Complex I (NDH-1) by a Genetic Engineering Approach

  • Chapter
  • First Online:
A Structural Perspective on Respiratory Complex I

Abstract

Genetic engineering has been widely adopted in many different fields of research and study on complex I is no exception. Because of current limitations in the technology when studying eukaryotes, most work has been performed using bacterial complex I (NDH-1). The bacterial system has been proven to be an excellent model in which to investigate the structure and mechanism of complex I. Sequence information, from the early days, and the availability of 3D structures, in more recent years, of NDH-1 have significantly boosted the importance of the gene engineering approach. Mutational approach has helped in identifying a number of amino acid residues that are essential not only for structural integrity but also for cofactor ligation, substrate binding and electron transfer. More recently, this approach determined residues essential for proton translocation coupled to the electron transfer from NADH to quinone. Understanding the roles of these residues, together with structural information, should lead to the elucidation of the reaction mechanism of NDH-1/complex I. This chapter is concerned with that knowledge of NDH-1 which has been advanced by a genetic engineering approach and possible applications that may extend the research to mitochondrial complex I.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albracht SP (2010a) The reaction of NADPH with bovine mitochondrial NADH:ubiquinone oxidoreductase revisited: I. Proposed consequences for electron transfer in the enzyme. J Bioenerg Biomembr 42:261–278

    Article  PubMed  CAS  Google Scholar 

  • Albracht SP (2010b) The reaction of NADPH with bovine mitochondrial NADH:ubiquinone oxidoreductase revisited: II. Comparison of the proposed working hypothesis with literature data. J Bioenerg Biomembr 42:279–292

    Article  PubMed  CAS  Google Scholar 

  • Amarneh B, Vik SB (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

    Article  PubMed  CAS  Google Scholar 

  • Au HC, Seo BB, Matsuno-Yagi A, Yagi T, Scheffler IE (1999) The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria. Proc Natl Acad Sci USA 96:4354–4359

    Article  PubMed  CAS  Google Scholar 

  • Berrisford JM, Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. J Biol Chem 284:29773–29783

    Article  PubMed  CAS  Google Scholar 

  • Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69–92

    Article  PubMed  CAS  Google Scholar 

  • Cardol P, Lapaille M, Minet P, Franck F, Matagne RF, 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. Eukaryot Cell 5:1460–1467

    Article  PubMed  CAS  Google Scholar 

  • Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, Walker JE (2006) Bovine complex I is a complex of forty-five different subunits. J Biol Chem 281:32724–32727

    Article  PubMed  CAS  Google Scholar 

  • Castro-Guerrero N, Sinha PK, Torres-Bacete J, Matsuno-Yagi A, Yagi T (2010) Pivotal roles of three conserved carboxyl residues of the NuoC (30 k) segment in the structural integrity of proton-translocating NADH-quinone oxidoreductase from Escherichia coli. Biochemistry 49:10072–10080

    Article  PubMed  CAS  Google Scholar 

  • Chevallet M, Dupuis A, Lunardi J, Van Belzen R, Albracht SPJ, Issartel JP (1997) The NuoI subunit of the Rhodobacter capsulatus respiratory complex I (equivalent to the bovine TYKY subunit) is required for proper assembly of the membraneous and peripheral domains of the enzyme. Eur J Biochem 250:451–458

    Article  PubMed  CAS  Google Scholar 

  • Darrouzet E, Dupuis A (1997) Genetic evidence for the existence of two quinone related inhibitor binding sites in NADH-CoQ reductase. Biochim Biophys Acta 1319:1–4

    Article  PubMed  CAS  Google Scholar 

  • Di Bernardo S, Yagi T (2001) Direct interaction between a membrane domain subunit and a connector subunit in the H+-translocating NADH-quinone oxidoreductase. FEBS Lett 508:385–388

    Article  PubMed  Google Scholar 

  • Di Bernardo S, Yano T, Yagi T (2000) Exploring the membrane domain of the reduced nicotinamide adenine dinucleotide-quinone oxidoreductase of Paracoccus denitrificans: characterization of the NQO7 subunit. Biochemistry 39:9411–9418

    Article  PubMed  CAS  Google Scholar 

  • Dupuis A, Peinnequin A, Chevallet M, Lunardi J, Darrouzet E, Pierrard B, Procaccio V, Issartel JP (1995) Identification of five Rhodobacter capsulatus genes encoding the equivalent of ND subunits of the mitochondrial NADH- ubiquinone oxidoreductase. Gene 167:99–104

    Article  PubMed  CAS  Google Scholar 

  • Dupuis A, Peinnequin A, Darrouzet E, Lunardi J (1997) Genetic disruption of the respiratory NADH-ubiquinone reductase of Rhodobacter capsulatus leads to an unexpected photosynthesis- negative phenotype. FEMS Microbiol Lett 148:107–114

    Article  CAS  Google Scholar 

  • Dupuis A, Chevallet M, Darrouzet E, Duborjal H, Lunardi J, Issartel JP (1998) The complex I from Rhodobacter capsulatus. Biochim Biophys Acta 1364:147–165

    Article  PubMed  CAS  Google Scholar 

  • Dupuis A, Prieur I, Lunardi J (2001) Toward a characterization of the connecting module of complex I. J Bioenerg Biomembr 33:159–168

    Article  PubMed  CAS  Google Scholar 

  • Dutton PL, Moser CC, Sled VD, Daldal F, Ohnishi T (1998) A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364:245–257

    Article  PubMed  CAS  Google Scholar 

  • Earley FGP, Patel SD, Ragan CI, Attardi G (1987) Photolabelling of a mitochondrially encoded subunit of NADH dehydrogenase with [3  H]dihydrorotenone. FEBS Lett 219:108–113

    Article  PubMed  CAS  Google Scholar 

  • Efremov RG, Sazanov LA (2011) Structure of the membrane domain of respiratory complex I. Nature 476:414–420

    Article  PubMed  CAS  Google Scholar 

  • Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465:441–445

    Article  PubMed  CAS  Google Scholar 

  • Euro L, Belevich G, Verkhovsky MI, Wikstrom M, Verkhovskaya M (2008a) 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

    Article  PubMed  CAS  Google Scholar 

  • Euro L, Bloch DA, Wikstrom M, Verkhovsky MI, Verkhovskaya M (2008b) Electrostatic interactions between FeS clusters in NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. Biochemistry 47:3185–3193

    Article  PubMed  CAS  Google Scholar 

  • Euro L, Belevich G, Bloch DA, Verkhovsky MI, Wikstrom M, Verkhovskaya M (2009) The role of the invariant glutamate 95 in the catalytic site of complex I from Escherichia coli. Biochim Biophys Acta 1787:68–73

    Article  PubMed  CAS  Google Scholar 

  • Falk-Krzesinski H, Wolfe AJ (1998) Genetic analysis of the nuo locus, which encodes the proton-translocating NADH dehydrogenase in Escherichia coli. J Bacteriol 180:1174–1184

    PubMed  CAS  Google Scholar 

  • Fearnley IM, Carroll J, Shannon RJ, Runswick MJ, Walker JE, Hirst J (2001) GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 276:38345–38348

    Article  PubMed  CAS  Google Scholar 

  • Flemming D, Hellwig P, Friedrich T (2002) 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

    Article  PubMed  CAS  Google Scholar 

  • Flemming D, Schlitt A, Spehr V, Bischof T, Friedrich T (2003) Iron-sulfur cluster N2 of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is located on subunit NuoB. J Biol Chem 278:47602–47609

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T (2001) Complex I: a chimaera of a redox and conformation-driven proton pump? J Bioenerg Biomembr 33:169–177

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5

    Article  PubMed  CAS  Google Scholar 

  • Garofano A, Zwicker K, Kerscher S, Okun P, Brandt U (2003) Two aspartic acid residues in the PSST-homologous NUKM subunit of complex I from Yarrowia lipolytica are essential for catalytic activity. J Biol Chem 278:42435–42440

    Article  PubMed  CAS  Google Scholar 

  • Ghelli A, Porcelli AM, Zanna C, Vidoni S, Mattioli S, Barbieri A, Iommarini L, Pala M, Achilli A, Torroni A, Rugolo M, Carelli V (2009) The background of mitochondrial DNA haplogroup J increases the sensitivity of Leber’s hereditary optic neuropathy cells to 2,5-hexanedione toxicity. PLoS One 4:e7922

    Article  PubMed  CAS  Google Scholar 

  • Gong X, Xie T, Yu L, Hesterberg M, Scheide D, Friedrich T, Yu CA (2003) The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli. J Biol Chem 278:25731–25737

    Article  PubMed  CAS  Google Scholar 

  • Guénebaut V, Vincentelli R, Mills D, Weiss H, Leonard KR (1997) Three-dimensional structure of NADH-dehydrogenase from Neurospora crassa by electron microscopy and conical tilt reconstruction. J Mol Biol 265:409–418

    Article  PubMed  Google Scholar 

  • Guénebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T (1998) Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276:105–112

    Article  PubMed  Google Scholar 

  • Hattori Y, Furuhata SI, Okajima M, Konno H, Abe M, Miyoshi H, Goto T, Makabe H (2008) Synthesis of pyranicin and its inhibitory action with bovine heart mitochondrial complex I. Org Lett 10:717–720

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75

    Article  PubMed  CAS  Google Scholar 

  • Hinchliffe P, Sazanov LA (2005) Organization of iron-sulfur clusters in respiratory complex I. Science 309:771–774

    Article  PubMed  CAS  Google Scholar 

  • Hinchliffe P, Carroll J, Sazanov LA (2006) Identification of a novel subunit of respiratory complex I from Thermus thermophilus. Biochemistry 45:4413–4420

    Article  PubMed  CAS  Google Scholar 

  • Hinttala R, Kervinen M, Uusimaa J, Maliniemi P, Finnila S, Rantala H, Remes AM, Hassinen IE, Majamaa K (2010) Analysis of functional consequences of haplogroup J polymorphisms m.4216 T  >  C and m.3866 T  >  C in human MT-ND1 Mutagenesis of homologous positions in Escherichia coli. Mitochondrion 10:358–361

    Article  PubMed  CAS  Google Scholar 

  • Hirst J, Carroll J, Fearnley IM, Shannon RJ, Walker JE (2003) The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim Biophys Acta 1604:135–150

    Article  PubMed  CAS  Google Scholar 

  • Hofhaus G, Weiss H, Leonard K (1991) Electron microscopic analysis of the peripheral and membrane parts of mitochondrial NADH dehydrogenase (complex I). J Mol Biol 221:1027–1043

    Article  PubMed  CAS  Google Scholar 

  • Huang G, Lu H, Hao A, Ng DC, Ponniah S, Guo K, Lufei C, Zeng Q, Cao X (2004) GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol Cell Biol 24:8447–8456

    Article  PubMed  CAS  Google Scholar 

  • Ichimaru N, Murai M, Kakutani N, Kako J, Ishihara A, Nakagawa Y, Nishioka T, Yagi T, Miyoshi H (2008) Synthesis and characterization of new piperazine-type inhibitors for mitochondrial NADH-ubiquinone oxidoreductase (complex I). Biochemistry 47:10816–10826

    Article  PubMed  CAS  Google Scholar 

  • Kajiyama Y, Otagiri M, Sekiguchi J, Kudo T, 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

    Article  PubMed  CAS  Google Scholar 

  • Kakutani N, Murai M, Sakiyama N, Miyoshi H (2010) Exploring the binding site of deltalac-acetogenin in bovine heart mitochondrial NADH-ubiquinone oxidoreductase. Biochemistry 49:4794–4803

    Article  PubMed  CAS  Google Scholar 

  • Kao MC, Di Bernardo S, Matsuno-Yagi A, Yagi T (2003) Characterization and topology of the membrane domain Nqo10 subunit of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. Biochemistry 42:4534–4543

    Article  PubMed  CAS  Google Scholar 

  • Kao MC, Di Bernardo S, Perego M, Nakamaru-Ogiso E, Matsuno-Yagi A, Yagi T (2004a) 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

    Article  PubMed  CAS  Google Scholar 

  • Kao MC, Matsuno-Yagi A, Yagi T (2004b) Subunit proximity in the H+-translocating NADH-quinone oxidoreductase probed by zero-length cross-linking. Biochemistry 43:3750–3755

    Article  PubMed  CAS  Google Scholar 

  • Kao MC, Di Bernardo S, Nakamaru-Ogiso E, Miyoshi H, Matsuno-Yagi A, Yagi T (2005a) Characterization of the membrane domain subunit NuoJ (ND6) of the NADH-quinone oxidoreductase from Escherichia coli by chromosomal DNA manipulation. Biochemistry 44:3562–3571

    Article  PubMed  CAS  Google Scholar 

  • Kao MC, Nakamaru-Ogiso E, Matsuno-Yagi A, Yagi T (2005b) Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli. Biochemistry 44:9545–9554

    Article  PubMed  CAS  Google Scholar 

  • Kervinen M, Patsi J, Finel M, Hassinen IE (2004) 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 43:773–781

    Article  PubMed  CAS  Google Scholar 

  • Kervinen M, Hinttala R, Helander HM, Kurki S, Uusimaa J, Finel M, Majamaa K, Hassinen IE (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

    Article  PubMed  CAS  Google Scholar 

  • Kruse SE, Watt WC, Marcinek DJ, Kapur RP, Schenkman KA, Palmiter RD (2008) Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab 7:312–320

    Article  PubMed  CAS  Google Scholar 

  • Kurki S, Zickermann V, Kervinen M, Hassinen I, 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

    Article  PubMed  CAS  Google Scholar 

  • Link AJ, Phillips D, Church GM (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

    PubMed  CAS  Google Scholar 

  • Lunardi J, Darrouzet E, Dupuis A, Issartel JP (1998) The nuoM arg 368 his 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

    PubMed  CAS  Google Scholar 

  • Maliniemi P, Kervinen M, Hassinen IE (2009) Modeling of human pathogenic mutations in Escherichia coli complex I reveals a sensitive region in the fourth inside loop of NUOH. Mitochondrion 9:394–401

    Article  PubMed  CAS  Google Scholar 

  • Mathiesen C, Hagerhall C (2002) Transmembrane topology of the NuoL, 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

    Article  PubMed  CAS  Google Scholar 

  • Mathiesen C, Hagerhall 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

    Article  PubMed  CAS  Google Scholar 

  • Murai M, Ishihara A, Nishioka T, Yagi T, Miyoshi H (2007) The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I. Biochemistry 46:6409–6416

    Article  PubMed  CAS  Google Scholar 

  • Murai M, Sekiguchi K, Nishioka T, 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

    Article  PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Sakamoto K, Matsuno-Yagi A, Miyoshi H, Yagi T (2003a) The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry 42:746–754

    Article  PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Seo BB, Yagi T, Matsuno-Yagi A (2003b) Amiloride inhibition of the proton-translocating NADH-quinone oxidoreductase of mammals and bacteria. FEBS Lett 549:43–46

    Article  PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Yano T, Yagi T, 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

    PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Matsuno-Yagi A, Yoshikawa S, Yagi T, Ohnishi T (2008) Iron-sulfur cluster N5 is coordinated by a HXXXCXXCXXXXXC motif in the nuog subunit of E. coli NADH:quinone oxidoreductase (complex I). J Biol Chem 283:25979–25987

    Article  PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Han H, Matsuno-Yagi A, Keinan E, Sinha SC, Yagi T, Ohnishi T (2010a) The ND2 subunit was labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor. FEBS Lett 584:883–888

    Article  PubMed  CAS  Google Scholar 

  • Nakamaru-Ogiso E, Kao MC, Chen H, Sinha SC, Yagi T, Ohnishi T (2010b) The membrane subunit NuoL(ND5) is involved in the indirect proton pumping mechanism of E. coli complex I. J Biol Chem 285:39070–39078

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi T (1998) Iron-sulfur clusters semiquinones in complex I. Biochim Biophys Acta 1364:186–206

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi T (2010) Structural biology: piston drives a proton pump. Nature 465:428–429

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi T, Ragan CI, Hatefi Y (1985) EPR studies of iron-sulfur cluster in isolated subunits and subfractions of NADH-ubiquinone oxidoreductase. J Biol Chem 260:2782–2788

    PubMed  CAS  Google Scholar 

  • Ohnishi ST, Salerno JC, Ohnishi T (2010) Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I). Biochim Biophys Acta 1797:1891–1893

    Article  PubMed  CAS  Google Scholar 

  • Patsi J, Kervinen M, Finel M, Hassinen IE (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

    Article  PubMed  CAS  Google Scholar 

  • Perales-Clemente E, Fernandez-Vizarra E, Acin-Perez R, Movilla N, Bayona-Bafaluy MP, Moreno-Loshuertos R, Perez-Martos A, Fernandez-Silva P, Enriquez JA (2010) Five entry points of the mitochondrially encoded subunits in mammalian complex I assembly. Mol Cell Biol 30:3038–3047

    Article  PubMed  CAS  Google Scholar 

  • Pohl T, Bauer T, Dorner K, Stolpe S, Sell P, Zocher G, Friedrich T (2007) Iron-sulfur cluster N7 of the NADH:ubiquinone oxidoreductase (complex I) is essential for stability but not involved in electron transfer. Biochemistry 46:6588–6596

    Article  PubMed  CAS  Google Scholar 

  • Quintana A, Kruse SE, Kapur RP, Sanz E, Palmiter RD (2010) From the cover: complex I deficiency due to loss of Ndufs4 in the brain results in progressive encephalopathy resembling Leigh syndrome. Proc Natl Acad Sci USA 107:10996–11001

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen T, Scheide D, Brors B, Kintscher L, Weiss H, Friedrich T (2001) Identification of two tetranuclear FeS clusters on the ferredoxin-type subunit of NADH:ubiquinone oxidoreductase (complex I). Biochemistry 40:6124–6131

    Article  PubMed  CAS  Google Scholar 

  • Remacle C, Cardol P, Coosemans N, Gaisne M, Bonnefoy N (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci USA 103:4771–4776

    Article  PubMed  CAS  Google Scholar 

  • Roth R, Hagerhall C (2001) Transmembrane orientation and topology of the NADH:quinone oxidoreductase putative quinone binding subunit NuoH. Biochim Biophys Acta 1504:352–362

    Article  PubMed  CAS  Google Scholar 

  • Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430–1436

    Article  PubMed  CAS  Google Scholar 

  • Schneider R, Massow M, Lisowsky T, Weiss H (1995) Different respiratory defective phenotypes of Neurospora crassa and Saccharomyces cerevisiae after inactivation of the gene encoding the mitochondrial acyl carrier protein. Curr Genet 29:10–17

    Article  PubMed  CAS  Google Scholar 

  • Screpanti E, Hunte C (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J Struct Biol 159:261–267

    Article  PubMed  CAS  Google Scholar 

  • Sekiguchi K, Murai M, Miyoshi H (2009) Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I. Biochim Biophys Acta 1787:1106–1111

    Article  PubMed  CAS  Google Scholar 

  • Sinha PK, Torres-Bacete J, Nakamaru-Ogiso E, Castro-Guerrero N, Matsuno-Yagi A, 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

    Article  PubMed  CAS  Google Scholar 

  • Steuber J (2001) Na+ translocation by bacterial NADH:quinone oxidoreductases: an extension to the complex-I family of primary redox pumps. Biochim Biophys Acta 1505:45–56

    Article  PubMed  CAS  Google Scholar 

  • Steuber J (2003) The C-terminally Truncated NuoL Subunit (ND5 Homologue) of the Na+-dependent complex I from Escherichia coli Transports Na+. J Biol Chem 278:26817–26822

    Article  PubMed  CAS  Google Scholar 

  • Tachibana M, Sparman M, Sritanaudomchai H, Ma H, Clepper L, Woodward J, Li Y, Ramsey C, Kolotushkina O, Mitalipov S (2009) Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature 461:367–372

    Article  PubMed  CAS  Google Scholar 

  • Tocilescu MA, Zickermann V, Zwicker K, Brandt U (2010) Quinone binding and reduction by respiratory complex I. Biochim Biophys Acta 1797:1883–1890

    Article  PubMed  CAS  Google Scholar 

  • Torres-Bacete J, Nakamaru-Ogiso E, Matsuno-Yagi A, 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

    Article  PubMed  CAS  Google Scholar 

  • Torres-Bacete J, Sinha PK, Castro-Guerrero N, Matsuno-Yagi A, 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

    Article  PubMed  CAS  Google Scholar 

  • Torres-Bacete J, Sinha PK, Matsuno-Yagi A, 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

    Article  PubMed  CAS  Google Scholar 

  • Velazquez I, Nakamaru-Ogiso E, Yano T, Ohnishi T, Yagi T (2005) Amino acid residues associated with cluster N3 in the NuoF subunit of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. FEBS Lett 579:3164–3168

    Article  PubMed  CAS  Google Scholar 

  • Verkhovskaya ML, Belevich N, Euro L, Wikstrom M, Verkhovsky MI (2008) Real-time electron transfer in respiratory complex I. Proc Natl Acad Sci USA 105:3763–3767

    Article  PubMed  CAS  Google Scholar 

  • Vgenopoulou I, Gemperli AC, Steuber J (2006) Specific modification of a Na+ binding site in NADH:quinone oxidoreductase from Klebsiella pneumoniae with dicyclohexylcarbodiimide. J Bacteriol 188:3264–3272

    Article  PubMed  CAS  Google Scholar 

  • Videira A, Duarte M (2002) From NADH to ubiquinone in Neurospora mitochondria. Biochim Biophys Acta 1555:187–191

    Article  PubMed  CAS  Google Scholar 

  • Weidner U, Geier S, Ptock A, Friedrich T, Leif H, Weiss H (1993) The gene locus of the proton-translocating NADH:ubiquinone oxidoreductase in Escherichia coli. Organization of the 14 genes and relationship between the derived proteins and subunits of mitochondrial complex I. J Mol Biol 233:109–122

    Article  PubMed  CAS  Google Scholar 

  • Wittekindt C, Schwarz M, Friedrich T, Koslowski T (2009) Aromatic amino acids as stepping stones in charge transfer in respiratory complex I: an unusual mechanism deduced from atomistic theory and bioinformatics. J Am Chem Soc 131:8134–8140

    Article  PubMed  CAS  Google Scholar 

  • Yadava N, Potluri P, Smith EN, Bisevac A, Scheffler IE (2002) Species-specific and mutant MWFE proteins: their effect on the assembly of a functional mammalian mitochondrial complex I. J Biol Chem 277:21221–21230

    Article  PubMed  CAS  Google Scholar 

  • Yadava N, Potluri P, Scheffler IE (2007) Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly. Int J Biochem Cell Biol 40:447–460

    Article  PubMed  CAS  Google Scholar 

  • Yagi T (1993) The bacterial energy-transducing NADH-quinone oxidoreductases. Biochim Biophys Acta 1141:1–17

    Article  PubMed  CAS  Google Scholar 

  • Yagi T, Di Bernardo S, Nakamaru-Ogiso E, Kao MC, Seo BB, Matsuno-Yagi A (2004) NADH dehydrogenase (NADH-quinone oxidoreductase). In: Zannoni D (ed) Respiration in archaea and bacteria, vol 15. Kluwer Academic Publishers, Dordrecht, pp 15–40. Advances in photosynthesis and respiration. Govindjee

    Google Scholar 

Ref Type: Serial (Book, Monograph)

  • Yagi T, Hatefi Y (1988) Identification of the DCCD-binding subunit of NADH-ubiquinone oxidoreductase (complex I). J Biol Chem 263:16150–16155

    PubMed  CAS  Google Scholar 

  • Yagi T, Matsuno-Yagi A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42:2266–2274

    Article  PubMed  CAS  Google Scholar 

  • Yagi T, Yano T, Matsuno-Yagi A (1993) Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches. J Bioenerg Biomembr 25:339–345

    Article  PubMed  CAS  Google Scholar 

  • Yagi T, Yano T, Di Bernardo S, Matsuno-Yagi A (1998) Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1364:125–133

    Article  PubMed  CAS  Google Scholar 

  • Yano T, Chu SS, Sled’ VD, Ohnishi T, Yagi T (1997) The proton-translocating NADH-quinone oxidoreductase (NDH-1) of thermophilic bacterium Thermus thermophilus HB-8: complete DNA sequence of the gene cluster and thermostable properties of the expressed NQO2 subunit. J Biol Chem 272:4201–4211

    Article  PubMed  CAS  Google Scholar 

  • Yano T, Magnitsky S, Sled’ VD, Ohnishi T, Yagi T (1999) Characterization of the putative 2x[4Fe-4S] binding NQO9 subunit of the proton-translocating NADH-quinone oxidoreductase (NDH-1) of Paracoccus denitrificans: expression, reconstitution, and EPR characterization. J Biol Chem 274:28598–28605

    Article  PubMed  CAS  Google Scholar 

  • Yano T, Sklar J, Nakamaru-Ogiso E, Takahashi Y, Yagi T, Ohnishi T (2003) Characterization of cluster N5 as a fast-relaxing [4Fe-4S] cluster in the Nqo3 subunit of the proton-translocating NADH-ubiquinone oxidoreductase from Paracoccus denitrificans. J Biol Chem 278:15514–15522

    Article  PubMed  CAS  Google Scholar 

  • Zannoni D (2004) Respiration in archaea and bacteria: diversity of prokaryotic electron transport carriers. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

Ref Type: Edited Book

  • Zickermann V, Drose S, Tocilescu MA, Zwicker K, Kerscher S, Brandt U (2008) Challenges in elucidating structure and mechanism of proton pumping NADH:ubiquinone oxidoreductase (complex I). J Bioenerg Biomembr 40:475–483

    Article  PubMed  CAS  Google Scholar 

  • Zu Y, Di Bernardo S, Yagi T, Hirst J (2002) Redox properties of the [2Fe-2S] center in the 24 kDa (NQO2) subunit of NADH:ubiquinone oxidoreductase (complex I). Biochemistry 41:10056–10069

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takao Yagi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Yagi, T., Torres-Bacete, J., Sinha, P.K., Castro-Guerrero, N., Matsuno-Yagi, A. (2012). Characterization of Bacterial Complex I (NDH-1) by a Genetic Engineering Approach. In: Sazanov, L. (eds) A Structural Perspective on Respiratory Complex I. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4138-6_8

Download citation

Publish with us

Policies and ethics