Projection structure of the cytochrome bo ubiquinol oxidase from Escherichia coli at 6 Å resolution

EMBO Journal

Volumn 16, Issue 6, 1997, Pages 1181-1188

  Gohlke, Ulrich ^a   Warne, Antony ^a   Saraste, Matti ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Cytochrome c oxidase; Electron microscopy; Membrane protein structure; Quinol oxidase; Two dimensional crystallization

Indexed keywords

CYTOCHROME C OXIDASE; MEMBRANE PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; BINDING SITE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; RESPIRATORY CHAIN;

CRYSTALLIZATION; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

ESCHERICHIA COLI;

EID: 0030897302     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.6.1181     Document Type: Article

References (64)

1. Anraku, Y. and Gennis, R.B. (1987) The aerobic respiratory chain of Escherichia coli. Trends Biochem. Sci., 12, 262-266.
2. Bacon, D.J. and Anderson, W.F. (1988) A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graphics, 6, 219-220.
3. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Engng, 6, 37-40.
4. Brown, S., Moody, A.J., Mitchell, R. and Rich, P.R. (1993) Binuclear centre structure of terminal protonmotive oxidases. FEBS Lett., 316, 216-223.
5. Bullough, P.A. and Tulloch, P.A. (1991) High resolution spot-scan electron microscopy of an α-helical coiled-coil protein. J. Mol. Biol., 215, 161-173.
6. B ligands. Biochemistry, 32, 11524-11529.
7. Castresana, J. and Saraste, M. (1995) Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem. Sci., 20, 443-448.
8. Castresana, J., Lübben, M., Saraste, M. and Higgins, D.G. (1994) Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J., 13, 2516-2525.
9. Chepuri, V. and Gennis, R.B. (1990) The use of gene fusions to determine the topology of all of the subunits of the cytochrome o terminal oxidase complex of Escherichia coli. J. Biol. Chem., 265, 12978-12986.
10. 3-type family of cytochrome c oxidases. J. Biol. Chem., 265, 11185-11192.
11. Collaborative Computational Project, Number 4 (1991) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
12. Crowther, R.A., Henderson, R. and Smith, J.M. (1996) MRC image processing programs. J. Struct. Biol., 116, 9-16.
13. Crum, J., Gruys, K.J. and Frey, T.G. (1994) Electron microscopy of cytochrome c oxidase crystals: labeling of subunit III with a monomaleimide undecagold cluster compound. Biochemistry, 33, 13719-13726.
14. Deatherage, J.F., Henderson, R. and Capaldi, R.A. (1982) Three-dimensional structure of cytochrome c oxidase vesicle crystals in negative stain. J. Mol. Biol., 158, 487-499.
15. Dubochet, J., Adrian, M., Chang, J.J., Homo., J.C., Lepault, J., McDowell, A.W. and Schultz, P. (1988) Cryo-electron microscopy of vitrified specimens. Q. Rev. Biochem., 21, 129-228.
16. Frey, T.G. (1994) Cytochrome c oxidase: structural studies by electron microscopy of two dimensional crystals. Microsc. Res. Techn., 27, 319-332.
17. Frey, T.G. and Murray, J.M. (1994) Electron microscopy of cytochrome c oxidase crystals. J. Mol. Biol., 237, 275-297.
18. García-Horsman, J.A., Barquera, B., Rumbley, J., Ma, J. and Gennis, R.B. (1994) The superfamily of haem-copper respiratory oxidases. J. Bacteriol., 176, 5587-5600.
19. Georgiou, C.D., Cokic, P. Carter, K., Webster, D.A. and Gennis, R.B. (1988) Relationships between membrane-bound cytochrome o from Vitreoscilla and that of Escherichia coli. Biochim. Biophys. Acta, 933, 179-183.
20. Haltia, T., Finel, M., Harms, N., Nakari, T., Raitio, M., Wikström, M. and Saraste, M. (1989) Deletion of the gene for subunit III leads to defective assembly of bacterial cytochrome oxidase. EMBO J., 8, 3571-3579.
21. Haltia, T., Semo, N., Arrondo, J.L.R., Goñi, F.M. and Freire, E. (1994) Thermodynamic and structural stability of cytochrome c oxidase from Paracoccus dentrificans. Biochemistry, 33, 9731-9740.
22. Havelka, W.A., Henderson, R. and Oesterhelt, D. (1995) Three-dimensional structure of halorhodopsin at 7 Å resolution. J. Mol. Biol., 247, 726-738.
23. Henderson, R., Baldwin, J.M., Downing, K., Lepault, J. and Zemlin, F. (1986) Structure of purple membrane from Halobacterium halobium: recording, measurement, and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy, 19, 147-178.
24. 3 from Paracoccus denitrificans and the 13-subunit beef-heart enzyme. Biophys. J., 60, 415-423.
25. Ishizuka, M., Machida, K., Shimada, S., Mogi, A., Tsuchiya, T., Ohmori, T., Souma, Y., Gonda, M. and Sone, N. (1990) Nucleotide sequence of the gene encoding for four subunits of cytochrome c oxidase from the thermophilic bacterium PS3. J. Biochem., 108, 866-873.
26. Iwata, S., Ostermeier, C., Ludwig, B. and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature, 376, 660-669.
27. 562-o complex, a terminal oxidase of Escherichia coli K12. J. Biol. Chem., 257, 7933-7935.
28. 562-o complex from cells in the early exponential phase of aerobic growth. J. Biol. Chem., 259, 3368-3374.
29. Kraulis, P. (1991) Molscript: a program to produce both detailed and schematic plots of proteins. J. Appl. Crystallogr., 24, 946-950.
30. A domain: identification of substrate-binding residues in cytochrome c oxidase. Biochemistry, 34, 5824-5830.
31. Lemieux, L.J., Calhoun, M.W., Thomas, J.W., Ingledew, W.J. and Gennis, R.B. (1992) Determination of the ligands of the low-spin haem of the cytochrome o ubiquinol oxidase complex using site-directed mutagenesis. J. Biol. Chem., 267, 2105-2113.
32. Lübben, M., Arnaud, S., Castresana, J., Warne, A., Albracht, S.P.J. and Saraste, M. (1994) A second terminal oxidase in Sulfolobus acidocaldarius. Eur. J. Biochem., 224, 151-159.
33. Ma, J., Lemieux, L. and Gennis, R.B. (1993) Genetic fusion of subunits I, II, and III of the cytochrome bo ubiquinol oxidase from Escherichia coli results in a fully assembled and active enzyme. Biochemistry, 32, 7692-7697.
34. Mather, M.W., Springer, P., Hensel, S., Buse, G. and Fee, J.A. (1993) Cytochrome c oxidase from Thermus thermophilus. J. Biol. Chem., 268, 5395-5408.
35. Matsushita, K., Patel, L. and Kaback, H.R. (1984) Cytochrome o type oxidase from Escherichia coli. Characterization of the enzyme and mechanism of electrochemical proton gradient generation. Biochemistry, 23, 4703-4714.
36. Merritt, E.A. and Murphy, M.E.P. (1994) Raster3D version 2.0 - a program for photorealistic molecular graphics. Acta Crystallogr., D50, 869-873.
37. Minagawa, J., Mogi, T., Gennis, R.B. and Anraku, Y. (1992) Identification of haem ligands in subunit I of the cytochrome bo complex in Escherichia coli. J. Biol. Chem., 267, 2096-2104.
38. Puustinen, A. and Wikström, M. (1991) The haem groups of cytochrome o from Escherichia coli. Proc. Natl Acad. Sci. USA, 88, 6122-6126.
39. Puustinen, A., Finel, M., Virrki, M. and Wikström, M. (1989) Cytochrome o (bo) is a proton pump in Paracoccus denitrificans and Escherichia coli. FEBS Lett., 249, 163-167.
40. 3 with dioxygen: the role of a bound ubiquinone molecule. Proc. Natl Acad. Sci. USA, 93, 1545-1548.
41. Riistama, S., Puustinen, A., García-Horsman, A., Iwata, S., Michel, H. and Wikström, M. (1996) Channelling of dioxygen into the respiratory enzyme. Biochim. Biophys. Acta, 1275, 1-4.
42. Saiki, K., Mogi, T. and Anraku, Y. (1992) Haem o biosynthesis in Escherichia coli. The cyoE gene in the cytochrome bo operon encodes a protohaem IX farnesyltransferase. Biochem. Biophys. Res. Commun., 189, 1491-1497.
43. Saiki, K., Nakamura, H., Mogi, T. and Anraku, Y. (1996) Probing a role of subunit IV of the Escherichia coli bo-type ubiquinol oxidase by deletion and cross-linking analyses. J. Biol. Chem., 271, 15336-15340.
44. Salerno, J.C., Bolgiano, B., Poole, R.K., Gennis, R.B. and Ingledew, W.J. (1990) Haem-copper and haem-haem interactions in the cytochrome bo-containing quinol oxidase of Escherichia coli. J. Biol. Chem., 265, 4364-4368.
45. 3-600 quinol oxidase. J. Biol. Chem., 267, 10225-10231.
46. Saraste, M. (1990) Structural features of cytochrome oxidase. Q. Rev. Biophys., 23, 331-366.
47. Saraste, M., Metso, T., Nakari, T., Jalli, T., Laureus, M. and van der Oost, J. (1991) The Bacillus subtilis cytochrome-c oxidase. Eur. J. Biochem., 195, 517-525.
48. Sato-Watanabe, M., Itoh, S., Mogi, T., Matsura, K., Miyoshi, H. and Anraku, Y. (1995) Stabilization of a semiquinone radical at the high affinity quinone-binding site (QH) of the Escherichia coli bo-type ubiquinol oxidase. FERS Lett., 374, 265-269.
49. Taha, T.S.M. and Ferguson-Miller, S. (1992) Interaction of cytochiome c with cytochrome c oxidase studied by monoclonal antibodies and protein modifiying agent. Biochemistry, 31, 9090-9097.
50. Toyoshima, C. (1989) On the use of holey grids in electron crystallography. Ultramicroscopy, 30, 439-444.
51. Trumpower, B.L. and Gennis, R.B. (1994) Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration. Annu. Rev. Biochem., 63, 675-716.
52. Tsubaki, M., Mogi, T., Hori, H., Hirota, S., Ogura, T., Kitagawa, T. and Anraku, Y. (1994) Molecular structure of redox metal centers of the cytochrome bo complex from E.coli. J. Biol. Chem., 269, 30861-30868.
53. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R. and Yoshikawa, S. (1995) Structures of metal sites of bovine heart cytochrome c oxidase at 2.8 Å. Science, 269, 1069-1074.
54. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R. and Yoshikawa, S. (1996) The whole structure of the 13 subunit oxidized cytochrome c oxidase at 2.8 Å. Science, 272, 1136-1144.
55. Uno, T., Mogi. T., Tsubaki. M., Nishimura, Y. and Anraku, Y. (1994) Resonance Raman and Fourier transform infrared studies on the subunit I histidine mutants of the cytochrome bo complex in Escherichia coli. J. Biol. Chem., 269, 11912-11920.
56. Unwin, N. (1993) Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol., 229, 1101-1124.
57. Unwin, N. and Henderson, R. (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol., 94, 425-440.
58. Valpuesta, J.M., Henderson, R. and Frey, T.G. (1990) Electron cryomicroscopic analysis of crystalline cytochrome oxidase. J. Mol. Biol., 214, 237-251.
59. Valpuesta, J.M., Carrascosa, J.L. and Henderson, R. (1994) Analysis of electron microscope images and electron diffraction patterns of thin crystals of Ø29 connectors in ice. J. Mol. Biol., 240, 281-287.
60. van der Oost, J. et al. (1992) Restoration of a lost metal-binding site: construction of two different copper sites into a subunit of the E.coli cytochrome o quinol oxidase complex. EMBO J., 11, 3209-3217.
61. van der Oost, J., de Boer, A.P.N., de Gier, J.W.L., Zumft, W.G., Stouthamer, A.H. and van Spanning, R.J.M. (1994). The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol. Lett., 121, 1-10.
62. Warne, A., Wang, D.N. and Saraste, M. (1995) Purification and two-dimensional crystallization of bacterial cytochrome oxidases. Eur. J. Biochem., 234, 443-451.
63. 3-ubiquinol oxidase of Escherichia coli. J. BM. Chem., 269, 28834-28838.
64. Wilmanns, M., Lappalainen, P., Kelly, M., Sauer-Eriksson, E. and Saraste, M. (1995) Crystal structure of the membrane-exposed domain from a respiratory quinol oxidase complex with an engineered dinuclear copper center. Proc. Natl Acad. Sci. USA, 92, 11955-11959.