Comparative genomics and site-directed mutagenesis support the existence of only one input channel for protons in the C-family (cbb3 oxidase) of heme-copper oxygen reductases

Biochemistry

Volumn 46, Issue 35, 2007, Pages 9963-9972

  Hemp, James ^a   Han, Huazhi ^a   Jung, Hyeob Roh ^b   Kaplan, Samuel ^b   Martinez, Todd J ^a   Gennis, Robert B ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; MITOCHONDRIA; NITRIC OXIDE REDUCTASES; VIBRIO CHOLERAE;

AMINO ACIDS; BACTERIA; CATALYSIS; CELL MEMBRANES; HYDROGEN BONDS; MUTAGENESIS; WATER;

PROTONS;

AMINO ACID; COPPER; CYTOCHROME C OXIDASE; HEME; HEME COPPER OXYGEN REDUCTASE; ION CHANNEL; NITRIC OXIDE REDUCTASE; OXIDOREDUCTASE; OXYGEN; UNCLASSIFIED DRUG; WATER;

AEROBIC BACTERIUM; ARCHAEBACTERIUM; ARTICLE; CATALYSIS; CELL MEMBRANE; CYTOPLASM; ENZYME ACTIVE SITE; ENZYME ANALYSIS; GENOMICS; HYDROGEN BOND; MITOCHONDRION; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTON TRANSPORT; REDUCTION; RHODOBACTER SPHAEROIDES; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; COPPER; ELECTRON TRANSPORT COMPLEX IV; HEME; ION CHANNELS; ION TRANSPORT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PHYLOGENY; PROTON PUMPS; PROTONS; RHODOBACTER SPHAEROIDES; SEQUENCE ANALYSIS, DNA; VIBRIO CHOLERAE;

PARACOCCUS DENITRIFICANS; RHODOBACTER SPHAEROIDES; VIBRIO CHOLERAE;

EID: 34548479264     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700659y     Document Type: Article

References (86)

1. Garcia-Horsman, J. A., Barquera, B., Rumbley, J., Ma, J., and Gennis, R. B. (1994) The Superfamily of Heme-Copper Respiratory Oxidases, J. Bacteriol. 176, 5587-5600.
2. Michel, H. (1998) The Mechanism of Proton Pumping by Cytochrome c Oxidase, Proc. Natl. Acad. Sci. U.S.A. 95, 12819-12824.
3. Wikstrom, M., and Verkhovsky, M. I. (2006) Towards the Mechanism of Proton Pumping by the Haem-Copper Oxidases, Biochim. Biophys. Acta 1757, 1047-1051.
4. Zumft, W. G. (2005) Nitric Oxide Reductases of Prokaryotes with Emphasis on the Respiratory, Heme-Copper Oxidase Type, J. Inorg. Biochem. 99, 194-215.
5. Reimann, J., Flock, U., Lepp, H., Honigmann, A., and Adelroth, P. (2007) A Pathway for Protons in Nitric Oxide Reductase from Paracoccus denitrificans, Biochim. Biophys. Acta 1767, 362-373.
6. Pereira, M. M., Santana, M., and Teixeira, M. (2001) A Novel Scenario for the Evolution of Haem-copper Oxygen Reductases, Biochim. Biophys. Acta 1505, 185-208.
7. Wikström, M. (1977) Proton Pump Coupled to Cytochrome c Oxidase in Mitochondria, Nature 266, 271-273.
8. 3-type Cytochrome c Oxidase from Thermus thermophilus, FEBS Lett. 434, 17-22.
9. 3-type Cytochrome c Oxidases of Paracoccus denitrificans Reveals Significant Differences in Proton-pump Design, Mol. Microbiol. 20, 1247-1260.
10. Gilderson, G., Aagaard, A., Gomes, C. M., Adelroth, P., Teixeira, M., and Brzezinski, P. (2001) Kinetics of Electron and Proton Transfer during O(2) Reduction in Cytochrome aa(3) from A. ambivalens: An Enzyme Lacking Glu(I-286), Biochim. Biophys. Acta 1503, 261-270.
11. Gleissner, M., Kaiser, U., Antonopoulos, E., and Schafer, G. (1997) The Archaeal SoxABCD Complex Is a Proton Pump in Sulfolobus acidocaldarius, J. Biol. Chem. 272, 8417-8426.
12. Lemos, R. S., Gomes, C. M., Santana, M., LeGall, J., Xavier, A. V., and Teixeira, M. (2001) The "Strict" Anaerobe Desulfovibrio gigas Contains a Membrane-Bound Oxygen-Reducing Respiratory Chain, FEBS Lett. 496, 40-43.
13. 3 Terminal Oxidase of Rhodothermus marinus Lacking the Key Glutamate of the D-Channel Is a Proton Pump, Biochemistry 39, 6336-6340.
14. Flock, U., Reimann, J., and Adelroth, P. (2006) Proton Transfer in Bacterial Nitric Oxide Reductase, Biochem. Soc. Trans. 34, 188-190.
15. Flock, U., Watmough, N. J., and Ädelroth, P. (2005) Electron/Proton Coupling in Bacterial Nitric Oxide Reductase during Reduction of Oxygen, Biochemistry 44, 10711-10719.
16. Hendriks, J. H., Jasaitis, A., Saraste, M., and Verkhovsky, M. I. (2002) Proton and Electron Pathways in the Bacterial Nitric Oxide Reductase, Biochemistry 41, 2331-2340.
17. Yoshikawa, S., Shinzawa-Itoh, K., and Tsukihara, T. (1998) Crystal Structure of Bovine Heart Cytochrome c Oxidase at 2.8 Å Resolution, J. Bioenerg. Biomembr. 30, 7-14.
18. Ostermeier, C., Harrenga, A., Ermler, U., and Michel, H. (1997) Structure at 2.7 Å Resolution of the Paracoccus denitrificans Two-Subunit Cytochrome c Oxidase Complexed with an Antibody Fv Fragment, Proc. Natl. Acad. Sci. U.S.A. 94, 10547-10553.
19. Svensson-Ek, M., Abramson, J., Larsson, G., Tornroth, S., Brzezinski, P., and Iwata, S. (2002) The X-ray Crystal Structures of Wild-Type and EQ(I-286) Mutant Cytochrome c Oxidases from Rhodobacter sphaeroides, J. Mol. Biol. 321, 329-339.
20. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puustinen, A., Iwata, S., and Wikström, M. (2000) The Structure of the Ubiquinol Oxidase from Escherichia coli and its Ubiquinone Binding Site, Nat. Struct. Biol. 7, 910-917.
21. Qin, L., Hiser, C., Mulichak, A., Garavito, R. M., and Ferguson-Miller, S. (2006) Identification of Conserved Lipid/Detergent-Binding Sites in a High-Resolution Structure of the Membrane Protein Cytochrome c Oxidase, Proc. Natl. Acad. Sci. U.S.A. 103, 16117-16122.
22. 3-cytochrome c Oxidase from Thermus thermophilus, EMBO J. 19, 1766-1776.
23. Hemp, J., Robinson, D. E., Ganesan, K. B., Martinez, T. J., Kelleher, N. L., and Gennis, R. B. (2006) Evolutionary Migration of a Post-Translationally Modified Active-Site Residue in the Proton-Pumping Heme-Copper Oxygen Reductases, Biochemistry 45, 15405-15410.
24. Buse, G., Soulimane, T., Dewor, M., Meyer, H. E., and Blüggel, M. (1999) Evidence for a Copper-Coordinated Histidine-Tyrosine Cross-Link in the Active Site of Cytochrome Oxidase, Protein Sci. 8, 985-990.
25. 3-type cytochrome c oxidase from Rhodobacter sphaeroides, Proc. Natl. Acad. Sci. U.S.A. 103, 16135-16140.
26. 3 Oxidases, Biochemistry 44, 10766-10775.
27. 3 and Cytochrome bo, J. Bioenerg. Biomembr. 25, 121-136.
28. Gennis, R. B. (1998) Multiple Proton-conducting Pathways in Cytochrome Oxidase and a Proposed Role for the Active-Site Tyrosine, Biochim. Biophys. Acta 1365, 241-248.
29. Gennis, R. B. (2004) Coupled Proton and Electron Transfer Reactions in Cytochrome Oxidase, Front. Biosci. 9, 581-591.
30. Namslauer, A., Pawate, A., Gennis, R. B., and Brzezinski, P. (2003) Redox-Coupled Proton Translocation in Biological Systems: Proton Shuttling in Cytochrome c Oxidase, Proc. Natl. Acad. Sci. U.S.A. 100, 15543-15547.
31. Pfitzner, U., Hoffmeier, K., Harrenga, A., Kannt, A., Michel, H., Bamberg, E., Richter, O.-M. H., and Ludwig, B. (2000) Tracing the D-Pathway in Reconstituted Site-Directed Mutants of Cytochrome c Oxidase from Paracoccus denitrificans, Biochemistry 39, 6756-6762.
32. Brändén, M., Sigurdson, H., Namslauer, A., Gennis, R. B., Ädelroth, P., and Brzezinski, P. (2001) On the Role of the K-proton Transfer Pathway in Cytochrome c Oxidase, Proc. Natl. Acad. Sci. U.S.A. 98, 5013-5018.
33. Brändén, M., Tomson, F. L., Gennis, R. B., and Brzezinski, P. (2002) The Entry Point of the K-Proton-Transfer Pathway in Cytochrome c Oxidase, Biochemistry 41, 10794-10798.
34. Konstantinov, A. A., Siletsky, S., Mitchell, D., Kaulen, A., and Gennis, R. B. (1997) The Roles of the Two Proton Input Channels in Cytochrome c Oxidase from Rhodobacter sphaeroides Probed by the Effects of Site-Directed Mutations on Time-Resolved Electrogenic Intraprotein Proton Transfer, Proc. Natl. Acad. Sci. U.S.A. 94, 9085-9090.
35. Yoshikawa, S., Muramoto, K., Shinzawa-Itoh, K., Aoyama, H., Tsukihara, T., Ogura, T., Shimokata, K., Katayama, Y., and Shimada, H. (2006) Reaction Mechanism of Bovine Heart Cytochrome c Oxidase, Biochim. Biophys. Acta 1757, 395-400.
36. Yoshikawa, S. (2003) A Cytochrome c Oxidase Proton Pumping Mechanism that Excludes the O2 Reduction Site, FEBS Lett. 555, 8-12.
37. Shimokata, K., Katayama, Y., Murayama, H., Suematsu, M., Tsukihara, T., Muramoto, K., Aoyama, H., Yoshikawa, S., and Shimada, H. (2007) The Proton Pumping Pathway of Bovine Heart Cytochrome c Oxidase, Proc. Natl. Acad. Sci. U.S.A. 104, 4200-4205.
38. Lee, H.-m., Das, T. K., Rousseau, D. L., Mills, D. A., Ferguson-Miller, S., and Gennis, R. B. (2000) Mutations in the Putative H-Channel in the Cytochrome c Oxidase from Rhodobacter sphaeroides Show That This Channel Is Not Important for Proton Conduction but Reveal Modulation of the Properties of Heme a, Biochemistry 39, 2989-2996.
39. Salje, J., Ludwig, B., and Richter, O. M. (2005) Is a Third Proton-Conducting Pathway Operative in Bacterial Cytochrome c Oxidase?, Biochem. Soc. Trans. 33, 829-831.
40. Branden, G., Gennis, R. B., and Brzezinski, P. (2006) Transmembrane Proton Translocation by Cytochrome c Oxidase, Biochim. Biophys. Acta 1757, 1052-1063.
41. Wraight, C. A. (2006) Chance and Design - Proton Transfer in Water, Channels and Bioenergetic Proteins, Biochim. Biophys. Acta 1757, 886-912.
42. Olsson, M. H. M., Sharma, P. K., and Warshel, A. (2005) Simulating Redox Coupled Proton Transfer in Cytochrome c Oxidase: Looking for the Proton Bottleneck, FEBS Lett. 579, 2026-2034.
43. Kato, M., Pisliakov, A. V., and Warshel, A. (2006) The Barrier for Proton Transport in Aquaporins as a Challenge for Electrostatic Models: The Role of Protein Relaxation in Mutational Calculations, Proteins 64, 829-844.
44. Arslan, E., Kannt, A., Thony-Meyer, L., and Hennecke, H. (2000) The Symbiotically Essential cbb(3)-Type Oxidase of Bradyrhizobium japonicum Is a Proton Pump, FEBS Lett. 470, 7-10.
45. 3-Type Cytochrome c Oxidase from Rhodobacter sphaeroides, a Proton-Pumping Heme-Copper Oxidase, Biochim. Biophys. Acta 1365, 421-434.
46. Sone, N., Tsukita, S., and Sakamoto, J. (1999) Direct Correlationship Between Proton Translocation and Growth Yield: An Analysis of the Respiratory Chain of Bacillus stearothermophilus, J. Biosci. Bioeng. 87, 495-499.
47. 3 Oxidases and an Atomic Model for the Rhodobacter sphaeroides Enzyme, Biochemistry 45, 5754-5765.
48. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic Local Alignment Search Tool, J. Mol. Biol. 215, 403-410.
49. Edgar, R. C. (2004) MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput, Nucleic Acids Res. 32, 1792-1797.
50. Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004) The Jalview Java Alignment Editor, Bioinformatics 20, 426-427.
51. Milpetz, F., Argos, P., and Persson, B. (1995) TMAP: A New Email and WWW Service for Membrane-Protein Structural Predictions, Trends Biochem. Sci. 20, 204-205.
52. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An Environment for Comparative Protein Modeling, Electrophoresis 18, 2714-2723.
53. Zhang, L., and Hermans, J. (1996) Hydrophilicity of Cavities in Proteins, Proteins 24, 433-438.
54. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable Molecular Dynamics with NAMD, J. Comput. Chem. 26, 1781-1802.
55. Foloppe, N., and MacKerell, A. D., Jr. (2000) All-Atom Empirical Force Field for Nucleic Acids: I. Parameter Optimization Based on Small Molecule and Condensed Phase Macromolecular Target Data, J. Comput. Chem. 21, 86-104.
56. 3 Cytochrome c Oxidase on Its Function, J. Microbiol. 44, 284-292.
57. Thomas, P. E., Ryan, D., and Leven, W. (1976) An Improved Straining Procedure for the Detection of the Peroxidase Activity of Cytochrome P-450 on Sodium Dodecyl Sulfate Polyacrylamide Gels, Anal. Biochem. 75, 168-176.
58. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G. L. (2006) Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB, Appl. Environ. Microbiol. 72, 5069-5072.
59. Thorndycroft, F. H., Butland, G., Richardson, D. J., and Watmough, N. J. (2007) A New Assay for Nitric Oxide Reductase Reveals Two Conserved Glutamate Residues Form the Entrance to a Proton-Conducting Channel in the Bacterial Enzyme, Biochem. J. 401, 111-119.
60. Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S., and Saraste, M. (2000) Nitric Oxide Reductases in Bacteria, Biochim. Biophys. Acta 1459, 266-273.
61. Pawate, A. S., J., M., Namslauer, A., Mills, D. A., Brzezinski, P., Ferguson-Miller, S., and Gennis, R. B. (2002) A Mutation in Subunit I of Cytochrome Oxidase from Rhodobacter sphaeroides Results in an Increase in Steady-State Activity but Completely Eliminates Proton Pumping, Biochemistry 41, 13417-13423.
62. Siletsky, S. A., Pawate, A. S., Weiss, K., Gennis, R. B., and Konstantinov, A. A. (2004) Transmembrane Charge Separation During the Ferryl-Oxo Oxidized Transition in a Nonpumping Mutant of Cytochrome c Oxidase, J. Biol. Chem. 279, 52558-52565.
63. 3-Type Cytochrome c Oxidase from Rhodobacter sphaeroides, Biochemistry 44, 12767-12774.
64. + Translocation Along the Single-File Water Chain in the Gramicidin A Channel, Biophys. J. 71, 19-39.
65. Wraight, C. A. (2005) Intraprotein Proton Transfer - Concepts and Realities from the Bacterial Photosynthetic Reaction Center, in Biophysical and Structual Aspects of Bioenergetics (Wïkstrom, M., Ed.) pp 273-312, Royal Society of Chemistry, Cambridge.
66. Ferguson-Miller, S., and Babcock, G. T. (1996) Heme/Copper Terminal Oxidases, Chem. Rev. 7, 2889-2907.
67. Ädelroth, P., Paddock, M. L., Sagle, L. B., Feher, G., and Okamura, M. Y. (2000) Identification of the Proton Pathway in Bacterial Reaction Centers: Both Protons Associated with Reduction of QB to QBH2 Share a Common Entry Point, Proc. Natl. Acad. Sci. U.S.A. 97, 13086-13091.
68. Ädelroth, P., Paddock, M. L., Tehrani, A., Beatty, J. T., Feher, G., and Okamura, M. Y. (2001) Identification of the Proton Pathway in Bacterial Reaction Centers: Decrease of Proton Transfer Rate by Mutation of Surface Histidines at H126 and H128 and Chemical Rescue by Imidazole Identifies the Initial Proton Donors, Biochemistry 40, 14538-14546.
69. +-translocating Function Retained, Proc. Natl. Acad. Sci. U.S.A. 87, 4900-4904.
70. Fillingame, R. H., Angevine, C. M., and Dmitriev, O. Y. (2003) Mechanics of Coupling Proton Movements to C-Ring Rotation in ATP Synthase, FEBS Lett. 555, 29-34.
71. 1 complex, Proc. Natl. Acad. Sci. U.S.A. 96, 10021-10026.
72. Izrailev, S., Crofts, A. R., Berry, E. A., and Schulten, K. (1999) Steered Molecular Dynamics Simulation of the Rieske Subunit Motion in the Cytochrome bc(1) Complex, Biophys. J. 77, 1753-1768.
73. 1 Complex: A New Crystal Structure Reveals an Altered Intramolecular Hydrogen-Bonding Pattern, J. Mol. Biol. 351, 573-597.
74. Hunte, C., Koepke, J., Lange, C., Rossmanith, T., and Michel, H. (2000) Structure at 2.3 Å Resolution of the Cytochrome bc(1) Complex from the Yeast Saccharomyces cerevisiae Co-crystallized with an Antibody Fv Fragment, Structure 8, 669-684.
75. Lanyi, J. K. (2006) Proton Transfers in the Bacteriorhodopsin Photocycle, Biochim. Biophys. Acta 1757, 1012-1018.
76. Horsefield, R., Yankovskaya, V., Sexton, G., Whittingham, W., Shiomi, K., Omura, S., Byrne, B., Cecchini, G., and Iwata, S. (2006) Structural and Computational Analysis of the Quinone-Binding Site of Complex II (Succinate-Ubiquinone Oxidoreductase): A Mechanism of Electron Transfer and Proton Conduction during Ubiquinone Reduction, J. Biol. Chem. 281, 7309-7316.
77. Madej, M. G., Nasiri, H. R., Hilgendorff, N. S., Schwalbe, H., and Lancaster, C. R. (2006) Evidence for Transmembrane Proton Transfer in a Dihaem-Containing Membrane Protein Complex, EMBO J. 25, 4963-4970.
78. Tomson, F. L., Morgan, J. E., Gu, G., Barquera, B., Vygodina, T. V., and Gennis, R. B. (2003) Substitutions for Glutamate 101 in Subunit II of Cytochrome c Oxidase from Rhodobacter sphaeroides Result in Blocking the Proton-Conducting K-Channel, Biochemistry 42, 1711-1717.
79. 3-Type Oxidases, J. Biol. Chem. 273, 6452-6459.
80. Ozturk, M., and Mandaci, S. (2006) Two Conserved Non-canonical Histidines Are Essential for Activity of the cbb(3)-Type Oxidase in Rhodobacter capsulatus, Mol. Biol. Rep. (in press).
81. Mitchell, D. M., Fetter, J. R., Mills, D. A., Ädelroth, P., Pressler, M. A., Kim, Y., Aasa, R., Brzezinski, P., Malmström, B. G., Alben, J. O., Babcock, G. T., Ferguson-Miller, S., and Gennis, R. B. (1996) Site-Directed Mutagenesis of Residues Lining a Putative Proton Transfer Pathway in Cytochrome c Oxidase from Rhodobacter sphaeroides, Biochemistry 35, 13089-13093.
82. de Vries, S., and Schroder, I. (2002) Comparison between the Nitric Oxide Reductase Family and Its Aerobic Relatives, the Cytochrome Oxidases, Biochem. Soc. Trans. 30, 662-667.
83. Belevich, I., Tuukkanen, A., Wikstrom, M., and Verkhovsky, M. I. (2006) Proton-Coupled Electron Equilibrium in Soluble and Membrane-Bound Cytochrome c Oxidase from Paracoccus denitrificans, Biochemistry 45, 4000-4006.
84. Wikström, M., Verkhovsky, M. I., and Hummer, G. (2003) Water-Gated Mechanism of Proton Translocation by Cytochrome c Oxidase, Biochim. Biophys. Acta 1604, 61-65.
85. Morgan, J. E., Verkhovsky, M. I., and Wikström, M. (1994) The Histidine Cycle: A New Model for Proton Translocation in the Respiratory Heme-Copper Oxidases, J. Bioenerg. Biomembr. 26, 599-608.
86. Michel, H. (1999) Cytochrome c Oxidase: Catalytic Cycle and Mechanisms of Proton Pumping - A Discussion, Biochemistry 38, 15129-15140.