Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I)

Journal of Molecular Biology

Volumn 348, Issue 4, 2005, Pages 857-870

  Gabaldón, Toni ^a   Rainey, Daphne ^a   Huynen, Martijn A ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Comparative genome analysis; Complex I; NADH:ubiquinone oxidoreductase; Pathway evolution

Indexed keywords

DNA; PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

AMINO ACID SEQUENCE; ARTICLE; CELL LINEAGE; EUKARYOTE; EVOLUTION; GENE DUPLICATION; GENE LOSS; GENOME; MITOCHONDRION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN INTERACTION;

EID: 17444385984     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.02.067     Document Type: Article

References (69)

1. A.H. Schapira Mitochondrial disorders Curr. Opin. Neurol. 13 2000 527 532
2. B.H. Robinson Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect Biochim. Biophys. Acta 1364 1998 271 286
3. J. Smeitink, R. Sengers, F. Trijbels, and L. van den Heuvel Human NADH:ubiquinone oxidoreductase J. Bioenerg. Biomembr. 33 2001 259 266
4. U. Weidner, S. Geier, A. Ptock, T. Friedrich, H. Leif, and H. Weiss 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 1993 109 122
5. X. Xu, A. Matsuno-Yagi, and T. Yagi DNA sequencing of the seven remaining structural genes of the gene cluster encoding the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans Biochemistry 32 1993 968 981
6. 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
7. T. Friedrich, and H. Weiss Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules J. Theor. Biol. 187 1997 529 540
8. T. Gabaldón, and M.A. Huynen Reconstruction of the proto-mitochondrial metabolism Science 301 2003 609
9. V.V. Emelyanov Common evolutionary origin of mitochondrial and rickettsial respiratory chains Arch. Biochem. Biophys. 420 2003 130 141
10. T. Friedrich Complex I: a chimera of a redox and conformation-driven proton pump? J. Bioenerg. Biomembr. 33 2001 169 177
11. J. Hirst, J. Carroll, I.M. Fearnley, R.J. Shannon, and J.E. Walker The nuclear encoded subunits of complex I from bovine heart mitochondria Biochim. Biophys. Acta 1604 2003 135 150
12. J. Carroll, I.M. Fearnley, R.J. Shannon, J. Hirst, and J.E. Walker Analysis of the subunit composition of complex I from bovine heart mitochondria Mol. Cell. Proteomics 2 2003 117 126
13. I. Bourges, C. Ramus, B. Mousson De Camaret, R. Beugnot, C. Remacle, and P. Cardol Structural organization of mitochondrial human complex I: role of the ND4 and ND5 mitochondria-encoded subunits and interaction with the prohibitin Biochem. J. 383 2004 491 499
14. A. Abdrakhmanova, V. Zickermann, M. Bostina, M. Radermacher, H. Schagger, S. Kerscher, and U. Brandt Subunit composition of mitochondrial complex I from the yeast Yarrowia lipolytica Biochim. Biophys. Acta 1658 2004 148 156
15. A. Videira, and M. Duarte From NADH to ubiquinone in Neurospora mitochondria Biochim. Biophys. Acta 1555 2002 187 191
16. P. Cardol, F. Vanrobaeys, B. Devreese, J. Van Beeumen, R.F. Matagne, and C. Remacle Higher plant-like subunit composition of mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes Biochim. Biophys. Acta 1658 2004 212 224
17. J.L. Heazlewood, K.A. Howell, and A.H. Millar Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits Biochim. Biophys. Acta 1604 2003 159 169
18. P. Dehal, Y. Satou, R.K. Campbell, J. Chapman, B. Degnan, and A. De Tomaso The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins Science 298 2002 2157 2167
19. J. Krungkrai, R. Kanchanarithisak, S.R. Krungkrai, and S. Rochanakij Mitochondrial NADH dehydrogenase from Plasmodium falciparum and Plasmodium berghei Expt. Parasitol. 100 2002 54 61
20. P. Xu, G. Widmer, Y. Wang, L.S. Ozaki, J.M. Alves, and M.G. Serrano The genome of Cryptosporidium hominis Nature 431 2004 1107 1112
21. W.Y. Tsang, and B.D. Lemire The role of mitochondria in the life of the nematode, Caenorhabditis elegans Biochim. Biophys. Acta 1638 2003 91 105
22. M.A. Huynen, T. Dandekar, and P. Bork Variation and evolution of the citric-acid cycle: a genomic perspective Trends Microbiol. 7 1999 281 291
23. C. Gille, A. Goede, C. Schloetelburg, R. Preissner, P.M. Kloetzel, U.B. Gobel, and C. Frommel A comprehensive view on proteasomal sequences: implications for the evolution of the proteasome J. Mol. Biol. 326 2003 1437 1448
24. J.M. Peregrin-Alvarez, S. Tsoka, and C.A. Ouzounis The phylogenetic extent of metabolic enzymes and pathways Genome. Res. 13 2003 422 427
25. B. Snel, and M.A. Huynen Quantifying modularity in the evolution of biomolecular systems Genome. Res. 14 2004 391 397
26. W.M. Fitch Distinguishing homologous from analogous proteins Syst. Zool. 19 1970 99 113
27. L.J. McGuffin, K. Bryson, and D.T. Jones The PSIPRED protein structure prediction server Bioinformatics 16 2000 404 405
28. L. Holm, and C. Sander Dali: a network tool for protein structure comparison Trends Biochem. Sci. 20 1995 478 480
29. R.C. Edgar MUSCLE: a multiple sequence alignment method with reduced time and space complexity BMC Bioinformatics 5 2004 113
30. R. Sadreyev, and N. Grishin COMPASS: a tool for comparison of multiple protein alignments with assessment of statistical significance J. Mol. Biol. 326 2003 317 336
31. U. Schulte Biogenesis of respiratory complex I J. Bioenerg. Biomembr. 33 2001 205 212
32. R. Janssen, J. Smeitink, R. Smeets, and L. van Den Heuvel CIA30 complex I assembly factor: a candidate for human complex I deficiency? Hum. Genet. 110 2002 264 270
33. K. Nakai, and P. Horton PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization Trends Biochem. Sci. 24 1999 34 36
34. O. Emanuelsson, H. Nielsen, S. Brunak, and G. von Heijne Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J. Mol. Biol. 300 2000 1005 1016
35. N. Wiedemann, A.E. Frazier, and N. Pfanner The protein import machinery of mitochondria J. Biol. Chem. 279 2004 14473 14476
36. X. Gan, M. Kitakawa, K. Yoshino, N. Oshiro, K. Yonezawa, and K. Isono Tag-mediated isolation of yeast mitochondrial ribosome and mass spectrometric identification of its new components Eur. J. Biochem. 269 2002 5203 5214
37. E.C. Koc, W. Burkhart, K. Blackburn, A. Moseley, H. Koc, and L.L. Spremulli A proteomics approach to the identification of mammalian mitochondrial small subunit ribosomal proteins J. Biol. Chem. 275 2000 32585 32591
38. S.B. Hedges, J.E. Blair, M.L. Venturi, and J.L. Shoe A molecular timescale of eukaryote evolution and the rise of complex multicellular life BMC Evol. Biol. 4 2004 2
39. S.L. Baldauf, A.J. Roger, I. Wenk-Siefert, and W.F. Doolittle A kingdom-level phylogeny of eukaryotes based on combined protein data Science 290 2000 972 977
40. M.W. Gray, G. Burger, and B.F. Lang Mitochondrial evolution Science 283 1999 1476 1481
41. S. Berry Endosymbiosis and the design of eukaryotic electron transport Biochim. Biophys. Acta 1606 2003 57 72
42. M.J. Runswick, I.M. Fearnley, J.M. Skehel, and J.E. Walker Presence of an acyl carrier protein in NADH:ubiquinone oxidoreductase from bovine heart mitochondria FEBS Letters 286 1991 121 124
43. U. Sackmann, R. Zensen, D. Rohlen, U. Jahnke, and H. Weiss The acyl-carrier protein in Neurospora crassa mitochondria is a subunit of NADH:ubiquinone reductase (complex I) Eur. J. Biochem. 200 1991 463 469
44. U. Schulte, V. Haupt, A. Abelmann, W. Fecke, B. Brors, and T. Rasmussen A reductase/isomerase subunit of mitochondrial NADH:ubiquinone oxidoreductase (complex I) carries an NADPH and is involved in the biogenesis of the complex J. Mol. Biol. 292 1999 569 580
45. V. Guenebaut, A. Schlitt, H. Weiss, K. Leonard, and T. Friedrich Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Mol. Biol. 276 1998 105 112
46. A. Grigoriev A relationship between gene expression and protein interactions on the proteome scale: analysis of the bacteriophage T7 and the yeast Saccharomyces cerevisiae Nucl. Acids Res. 29 2001 3513 3519
47. M. Duarte, and A. Videira Respiratory chain complex I is essential for sexual development in neurospora and binding of iron sulfur clusters are required for enzyme assembly Genetics 156 2000 607 615
48. W.Y. Tsang, L.C. Sayles, L.I. Grad, D.B. Pilgrim, and B.D. Lemire Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased life span J. Biol. Chem. 276 2001 32240 32246
49. A. Harington, C.J. Herbert, B. Tung, G.S. Getz, and P.P. Slonimski Identification of a new nuclear gene (CEM1) encoding a protein homologous to a beta-keto-acyl synthase which is essential for mitochondrial respiration in Saccharomyces cerevisiae Mol. Microbiol. 9 1993 545 555
50. R. Schneider, M. Massow, T. Lisowsky, and H. Weiss Different respiratory-defective phenotypes of Neurospora crassa and Saccharomyces cerevisiae after inactivation of the gene encoding the mitochondrial acyl carrier protein Curr. Genet. 29 1995 10 17
51. S. Brody, C. Oh, U. Hoja, and E. Schweizer Mitochondrial acyl carrier protein is involved in lipoic acid synthesis in Saccharomyces cerevisiae FEBS Letters 408 1997 217 220
52. Y.M. Galante, and Y. Hatefi Purification and molecular and enzymic properties of mitochondrial NADH dehydrogenase Arch. Biochem. Biophys. 192 1979 559 568
53. S.J. Pilkington, J.M. Skehel, R.B. Gennis, and J.E. Walker Relationship between mitochondrial NADH-ubiquinone reductase and a bacterial NAD-reducing hydrogenase Biochemistry 30 1991 2166 2175
54. A. Akhmanova, F. Voncken, T. van Alen, A. van Hoek, B. Boxma, and G. Vogels A hydrogenosome with a genome Nature 396 1998 527 528
55. P. Prommeenate, A.M. Lennon, C. Markert, M. Hippler, and P.J. Nixon Subunit composition of NDH-1 complexes of Synechocystis sp. PCC 6803: identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex J. Biol. Chem. 279 2004 28165 28173
56. J.E. Maul, J.W. Lilly, L. Cui, C.W. dePamphilis, W. Miller, E.H. Harris, and D.B. Stern The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats Plant Cell 14 2002 2659 2679
57. C. Mathiesen, and C. Hagerhall The "antiporter module" of respiratory chain complex I includes the MrpC/NuoK subunit-a revision of the modular evolution scheme FEBS Letters 549 2003 7 13
58. C. Ugalde, R. Vogel, R. Huijbens, B. Van Den Heuvel, J. Smeitink, and L. Nijtmans Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies Hum. Mol. Genet. 13 2004 2461 2472
59. T.F. Smith, and M.S. Waterman Identification of common molecular subsequences J. Mol. Biol. 147 1981 195 197
60. S.R. Eddy Profile hidden Markov models Bioinformatics 14 1998 755 763
61. 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 Nucl. Acids Res. 22 1994 4673 4680
62. Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package). Department of Genetics, University of Washington, Seattle, USA. http://evolution.genetics. washington.edu/phylip.html
63. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucl. Acids Res. 25 1997 3389 3402
64. L.A. Sazanov, S.Y. Peak-Chew, I.M. Fearnley, and J.E. Walker Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme Biochemistry 39 2000 7229 7235
65. M. Yamaguchi, and Y. Hatefi Mitochondrial NADH:ubiquinone oxidoreductase (complex I): proximity of the subunits of the flavoprotein and the iron-sulfur protein subcomplexes Biochemistry 32 1993 1935 1939
66. C. von Mering, M. Huynen, D. Jaeggi, S. Schmidt, P. Bork, and B. Snel STRING: a database of predicted functional associations between proteins Nucl. Acids Res. 31 2003 258 261
67. 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
68. A. Aiyar The use of CLUSTAL W and CLUSTAL X for multiple sequence alignment Methods Mol. Biol. 132 2000 221 241
69. R.L. Tatusov, N.D. Fedorova, J.J. Jackson, A.R. Jacobs, B. Kiryutin, and E.V. Koonin The COG database: an updated version includes eukaryotes BMC Bioinformatics 4 2003 41