The architecture of respiratory complex I (original) (raw)

References

  1. Walker, J. E. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q. Rev. Biophys. 25, 253–324 (1992)
    Article CAS PubMed Google Scholar
  2. Yagi, T. & Matsuno-Yagi, A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42, 2266–2274 (2003)
    Article CAS PubMed Google Scholar
  3. Brandt, U. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75, 69–92 (2006)
    Article CAS PubMed Google Scholar
  4. Ohnishi, T. Iron-sulfur clusters/semiquinones in complex I. Biochim. Biophys. Acta 1364, 186–206 (1998)
    Article CAS PubMed Google Scholar
  5. Sazanov, L. A. Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46, 2275–2288 (2007)
    Article CAS PubMed Google Scholar
  6. Schapira, A. H. Human complex I defects in neurodegenerative diseases. Biochim. Biophys. Acta 1364, 261–270 (1998)
    Article CAS PubMed Google Scholar
  7. Dawson, T. M. & Dawson, V. L. Molecular pathways of neurodegeneration in Parkinson’s disease. Science 302, 819–822 (2003)
    Article ADS CAS PubMed Google Scholar
  8. Balaban, R. S., Nemoto, S. & Finkel, T. Mitochondria, oxidants, and aging. Cell 120, 483–495 (2005)
    Article CAS PubMed Google Scholar
  9. Carroll, J. et al. Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 281, 32724–32727 (2006)
    Article CAS PubMed Google Scholar
  10. Clason, T. et al. The structure of eukaryotic and prokaryotic complex I. J. Struct. Biol. 169, 81–88 (2010)
    Article ADS CAS PubMed Google Scholar
  11. Morgan, D. J. & Sazanov, L. A. Three-dimensional structure of respiratory complex I from Escherichia coli in ice in the presence of nucleotides. Biochim. Biophys. Acta 1777, 711–718 (2008)
    Article CAS PubMed Google Scholar
  12. Sazanov, L. A. & Hinchliffe, P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus . Science 311, 1430–1436 (2006)
    Article ADS CAS PubMed Google Scholar
  13. Berrisford, J. M. & Sazanov, L. A. Structural basis for the mechanism of respiratory complex I. J. Biol. Chem. 284, 29773–29783 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  14. Fearnley, I. M. & Walker, J. E. Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim. Biophys. Acta 1140, 105–134 (1992)
    Article CAS PubMed Google Scholar
  15. Mathiesen, C. & Hagerhall, C. 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 (2002)
    Article CAS PubMed Google Scholar
  16. Friedrich, T. Complex I: a chimaera of a redox and conformation-driven proton pump? J. Bioenerg. Biomembr. 33, 169–177 (2001)
    Article CAS PubMed Google Scholar
  17. Sazanov, L. A., Carroll, J., Holt, P., Toime, L. & Fearnley, I. M. 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, 19483–19491 (2003)
    Article CAS PubMed Google Scholar
  18. Guénebaut, V., Schlitt, A., Weiss, H., Leonard, K. & Friedrich, T. Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Mol. Biol. 276, 105–112 (1998)
    Article PubMed Google Scholar
  19. Baranova, E. A., Holt, P. J. & Sazanov, L. A. Projection structure of the membrane domain of Escherichia coli respiratory complex I at 8 Å resolution. J. Mol. Biol. 366, 140–154 (2007)
    Article CAS PubMed Google Scholar
  20. Kao, M. C., Di Bernardo, S., Matsuno-Yagi, A. & Yagi, T. Characterization of the membrane domain Nqo11 subunit of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans . Biochemistry 41, 4377–4384 (2002)
    Article CAS PubMed Google Scholar
  21. Kao, M. C., Di Bernardo, S., Matsuno-Yagi, A. & Yagi, T. Characterization and topology of the membrane domain Nqo10 subunit of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans . Biochemistry 42, 4534–4543 (2003)
    Article CAS PubMed Google Scholar
  22. Bernardo, S. D., Yano, T. & Yagi, T. Exploring the membrane domain of the reduced nicotinamide adenine dinucleotide-quinone oxidoreductase of Paracoccus denitrificans: characterization of the NQO7 subunit. Biochemistry 39, 9411–9418 (2000)
    Article CAS PubMed Google Scholar
  23. Mamedova, A. A., Holt, P. J., Carroll, J. & Sazanov, L. A. Substrate-induced conformational change in bacterial complex I. J. Biol. Chem. 279, 23830–23836 (2004)
    Article CAS PubMed Google Scholar
  24. Screpanti, E. & Hunte, C. Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261–267 (2007)
    Article CAS PubMed Google Scholar
  25. Torres-Bacete, J., Sinha, P. K., Castro-Guerrero, N., Matsuno-Yagi, A. & Yagi, T. 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 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  26. Holt, P. J., Morgan, D. J. & Sazanov, L. A. The location of NuoL and NuoM subunits in the membrane domain of the Escherichia coli complex I: implications for the mechanism of proton pumping. J. Biol. Chem. 278, 43114–43120 (2003)
    Article CAS PubMed Google Scholar
  27. Baranova, E. A., Morgan, D. J. & Sazanov, L. A. Single particle analysis confirms distal location of subunits NuoL and NuoM in Escherichia coli complex I. J. Struct. Biol. 159, 238–242 (2007)
    Article CAS PubMed Google Scholar
  28. Kao, M. C., Nakamaru-Ogiso, E., Matsuno-Yagi, A. & Yagi, T. Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli . Biochemistry 44, 9545–9554 (2005)
    Article CAS PubMed Google Scholar
  29. Roth, R. & Hagerhall, C. Transmembrane orientation and topology of the NADH:quinone oxidoreductase putative quinone binding subunit NuoH. Biochim. Biophys. Acta 1504, 352–362 (2001)
    Article CAS PubMed Google Scholar
  30. Kao, M. C., Matsuno-Yagi, A. & Yagi, T. Subunit proximity in the H+-translocating NADH-quinone oxidoreductase probed by zero-length cross-linking. Biochemistry 43, 3750–3755 (2004)
    Article CAS PubMed Google Scholar
  31. Murai, M., Sekiguchi, K., Nishioka, T. & Miyoshi, H. Characterization of the inhibitor binding site in mitochondrial NADH-ubiquinone oxidoreductase by photoaffinity labeling using a quinazoline-type inhibitor. Biochemistry 48, 688–698 (2009)
    Article CAS PubMed Google Scholar
  32. Sekiguchi, K., Murai, M. & Miyoshi, H. Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I. Biochim. Biophys. Acta 1787, 1106–1111 (2009)
    Article CAS PubMed Google Scholar
  33. Page, C. C., Moser, C. C., Chen, X. & Dutton, P. L. Natural engineering principles of electron tunnelling in biological oxidation–reduction. Nature 402, 47–52 (1999)
    Article ADS CAS PubMed Google Scholar
  34. Yano, T., Dunham, W. R. & Ohnishi, T. Characterization of the ΔμH+-sensitive ubisemiquinone species (SQNf) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44, 1744–1754 (2005)
    Article CAS PubMed Google Scholar
  35. 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 42, 746–754 (2003)
    Article CAS PubMed Google Scholar
  36. Gong, X. et al. The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli . J. Biol. Chem. 278, 25731–25737 (2003)
    Article CAS PubMed Google Scholar
  37. Berrisford, J. M., Thompson, C. J. & Sazanov, L. A. Chemical and NADH-induced, ROS-dependent, cross-linking between subunits of complex I from Escherichia coli and Thermus thermophilus . Biochemistry 47, 10262–10270 (2008)
    Article CAS PubMed Google Scholar
  38. Belogrudov, G. & Hatefi, Y. Catalytic sector of complex I (NADH:ubiquinone oxidoreductase): subunit stoichiometry and substrate-induced conformation changes. Biochemistry 33, 4571–4576 (1994)
    Article CAS PubMed Google Scholar
  39. Gondal, J. A. & Anderson, W. M. The molecular morphology of bovine heart mitochondrial NADH-ubiquinone reductase. Native disulfide-linked subunits and rotenone-induced conformational changes. J. Biol. Chem. 260, 12690–12694 (1985)
    CAS PubMed Google Scholar
  40. Verkhovskaya, M. L., Belevich, N., Euro, L., Wikstrom, M. & Verkhovsky, M. I. Real-time electron transfer in respiratory complex I. Proc. Natl Acad. Sci. USA 105, 3763–3767 (2008)
    Article ADS CAS PubMed PubMed Central Google Scholar
  41. Euro, L., Belevich, G., Verkhovsky, M. I., Wikstrom, M. & Verkhovskaya, M. 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 (2008)
    Article CAS PubMed Google Scholar
  42. Torres-Bacete, J., Nakamaru-Ogiso, E., Matsuno-Yagi, A. & Yagi, T. 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 (2007)
    Article CAS PubMed Google Scholar
  43. Kervinen, M., Patsi, J., Finel, M. & Hassinen, I. E. 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 (2004)
    Article CAS PubMed Google Scholar
  44. Kajiyama, Y., Otagiri, M., Sekiguchi, J., Kudo, T. & Kosono, S. 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 (2009)
    Article CAS PubMed Google Scholar
  45. Sazanov, L. A., Carroll, J., Holt, P., Toime, L. & Fearnley, I. M. 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, 19483–19491 (2003)
    Article CAS PubMed Google Scholar
  46. Hinchliffe, P., Carroll, J. & Sazanov, L. A. Identification of a novel subunit of respiratory complex I from Thermus thermophilus . Biochemistry 45, 4413–4420 (2006)
    Article CAS PubMed Google Scholar
  47. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760–763 (1994)
  48. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD . Acta Crystallogr. D 58, 1772–1779 (2002)
    Article PubMed CAS Google Scholar
  49. de La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472–494 (1997)
    Article CAS PubMed Google Scholar
  50. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948–1954 (2002)
    Article MathSciNet PubMed CAS Google Scholar
  51. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658–674 (2007)
    Article CAS Google Scholar
  52. Jones, T. A. & Kjeldgaard, M. Electron-density map interpretation. Methods Enzymol. 277, 173–208 (1997)
    Article CAS PubMed Google Scholar
  53. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004)
    Article CAS PubMed Google Scholar
  54. Rudolph, M. G., Wingren, C., Crowley, M. P., Chien, Y. H. & Wilson, I. A. Combined pseudo-merohedral twinning, non-crystallographic symmetry and pseudo-translation in a monoclinic crystal form of the γδ T-cell ligand T10. Acta Crystallogr. D 60, 656–664 (2004)
    Article PubMed CAS Google Scholar
  55. Berrisford, J. M. & Sazanov, L. A. Structural basis for the mechanism of respiratory complex I. J. Biol. Chem. 284, 29773–29783 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  56. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007)
    Article CAS PubMed Google Scholar
  57. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001)
    Article CAS PubMed Google Scholar
  58. McGuffin, L. J., Bryson, K. & Jones, D. T. The PSIPRED protein structure prediction server. Bioinformatics 16, 404–405 (2000)
    Article CAS PubMed Google Scholar
  59. Rost, B., Yachdav, G. & Liu, J. The PredictProtein server. Nucleic Acids Res. 32, W321–W326 (2004)
    Article CAS PubMed PubMed Central Google Scholar

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