The roles of Rhodobacter sphaeroides copper chaperones PCuAC and Sco (PrrC) in the assembly of the copper centers of the aa3-type and the cbb3-type cytochrome c oxidases

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 6, 2012, Pages 955-964

  Thompson, Audie K ^a,b   Gray, Jimmy ^a   Liu, Aimin ^a,c   Hosler, Jonathan P ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b Texas A M University System   (United States)

^c GEORGIA STATE UNIVERSITY   (United States)

Author keywords

aa3 type cytochrome c oxidase; cbb3 type cytochrome c oxidase; Copper center assembly; Copper chaperone; CuA; Sco protein

Indexed keywords

BACTERIAL PROTEIN; CUPRIC ION; CYTOCHROME C OXIDASE; METALLOCHAPERONE; PERIPLASMIC COPPER A CHAPERONE; PROTEIN COX11; SCO PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RHODOBACTER SPHAEROIDES;

BACTERIAL PROTEINS; CELL MEMBRANE; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX IV; GENE DELETION; MOLECULAR CHAPERONES; OXYGEN; RHODOBACTER SPHAEROIDES;

RHODOBACTER SPHAEROIDES; THERMUS THERMOPHILUS;

EID: 84860653311     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.01.003     Document Type: Article

References (78)

1. 3 of Rhodobacter sphaeroides as a model for mitochondrial cytochrome c oxidase. Purification, kinetics, proton pumping, and spectral analysis J. Biol. Chem. 267 1992 24264 24272
2. 3 of Rhodobacter sphaeroides as a model for mitochondrial cytochrome c oxidase. The coxII/coxIII operon codes for structural and assembly proteins homologous to those in yeast J. Biol. Chem. 267 1992 24273 24278
3. 3-type cytochrome c oxidase of Rhodobacter sphaeroides Mol. Microbiol. 6 1992 635 642
4. M. Svensson-Ek, J. Abramson, G. Larsson, S. Tornroth, P. Brzezinski, and S. Iwata The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides J. Mol. Biol. 321 2002 329 339
5. L. Qin, C. Hiser, A. Mulichak, R.M. Garavito, and S. Ferguson-Miller 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 2006 16117 16122
6. A Biochemistry 33 1994 3113 3119
7. J. Hemp, D.E. Robinson, K.B. Ganesan, T.J. Martinez, N.L. Kelleher, and R.B. Gennis Evolutionary migration of a post-translationally modified active-site residue in the proton-pumping heme-copper oxygen reductases Biochemistry 45 2006 15405 15410
8. 3 and cytochrome bo J. Bioenerg. Biomembr. 25 1993 121 136
9. 3 J. Biol. Chem. 274 1999 38032 38041
10. K. Wang, Y. Zhen, R. Sadoski, S. Grinnell, L. Geren, S. Ferguson-Miller, B. Durham, and F. Millett Definition of the interaction domain for cytochrome c on cytochrome c oxidase. II. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants J. Biol. Chem. 274 1999 38042 38050
11. 1 in the electron transport network of Paracoccus denitrificans: redundant or subtly different in function? J. Bacteriol. 183 2001 7017 7026
12. 2 proteins with altered heme attachment sites Arch. Biochem. Biophys. 389 2001 234 244
13. y of Rhodobacter capsulatus is attached to the cytoplasmic membrane by an uncleaved signal sequence-like anchor J. Bacteriol. 179 1997 2623 2631
14. 3 oxidase Eur. J. Biochem. 269 2002 2980 2988
15. P. Brzezinski, J. Reimann, and P. Adelroth Molecular architecture of the proton diode of cytochrome c oxidase Biochem. Soc. Trans. 36 2008 1169 1174
16. B site in cytochrome c oxidase and the importance of its unique His-Tyr bond Biochim. Biophys. Acta 1787 2009 221 233
17. 3 oxidases and an atomic model for the Rhodobacter sphaeroides enzyme Biochemistry 45 2006 5754 5765
18. 3 oxidases Biochemistry 44 2005 10766 10775
19. 3 cytochrome oxidase provides insights into proton pumping Science 329 2010 327 330
20. 3-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides J. Bacteriol. 183 2001 2013 2024
21. B.M. Brown, Z. Wang, K.R. Brown, J.A. Cricco, and E.L. Hegg Heme O synthase and heme A synthase from Bacillus subtilis and Rhodobacter sphaeroides interact in Escherichia coli Biochemistry 43 2004 13541 13548
22. I.C. Soto, F. Fontanesi, J. Liu, and A. Barrientos Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core Biochim. Biophys. Acta 2011 doi: 10.1016/j.bbabio.2011.09.005
23. D. Smith, J. Gray, L. Mitchell, W.E. Antholine, and J.P. Hosler Assembly of cytochrome c oxidase in the absence of assembly protein Surf1p leads to loss of the active site heme J. Biol. Chem. 280 2005 17652 17656
24. A. Hannappel, F.A. Bundschuh, B. Ludwig, Role of Surf1 in heme recruitment for bacterial COX biogenesis, Biochim. Biophys. Acta (in press), doi: 10.1016/j.bbabio.2011.09.007.
25. 3-type cytochrome c oxidase complex J. Mol. Biol. 355 2006 989 1004
26. 3-type cytochrome oxidase J. Bacteriol. 192 2010 6378 6389
27. 3-type cytochrome oxidase Arch. Microbiol. 165 1996 297 305
28. 3-type cytochrome c oxidase in Rhodobacter capsulatus, Biochim. Biophys. Acta (in press), doi: 10.1016/j.bbabio.2011.09.007.
29. L. Banci, I. Bertini, G. Cavallaro, and S. Ciofi-Baffoni Seeking the determinants of the elusive functions of Sco proteins FEBS J. 278 2011 2244 2262
30. P.A. Cobine, F. Pierrel, and D.R. Winge Copper trafficking to the mitochondrion and assembly of copper metalloenzymes Biochim. Biophys. Acta 1763 2006 759 772
31. L. Banci, I. Bertini, V. Calderone, S. Ciofi-Baffoni, S. Mangani, M. Martinelli, P. Palumaa, and S. Wang A hint for the function of human Sco1 from different structures Proc. Natl. Acad. Sci. U. S. A. 103 2006 8595 8600
32. Y.C. Horng, S.C. Leary, P.A. Cobine, F.B. Young, G.N. George, E.A. Shoubridge, and D.R. Winge Human Sco1 and Sco2 function as copper-binding proteins J. Biol. Chem. 280 2005 34113 34122
33. S.C. Leary, F. Sasarman, T. Nishimura, and E.A. Shoubridge Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1 Hum. Mol. Genet. 18 2009 2230 2240
34. A. Lode, M. Kuschel, C. Paret, and G. Rodel Mitochondrial copper metabolism in yeast: interaction between Sco1p and Cox2p FEBS Lett. 485 2000 19 24
35. A. Lode, C. Paret, and G. Rodel Molecular characterization of Saccharomyces cerevisiae Sco2p reveals a high degree of redundancy with Sco1p Yeast 19 2002 909 922
36. N.R. Mattatall, J. Jazairi, and B.C. Hill Characterization of YpmQ, an accessory protein required for the expression of cytochrome c oxidase in Bacillus subtilis J. Biol. Chem. 275 2000 28802 28809
37. D. Buhler, R. Rossmann, S. Landolt, S. Balsiger, H.M. Fischer, and H. Hennecke Disparate pathways for the biogenesis of cytochrome oxidases in Bradyrhizobium japonicum J. Biol. Chem. 285 2010 15704 15713
38. A.G. McEwan, A. Lewin, S.L. Davy, R. Boetzel, A. Leech, D. Walker, T. Wood, and G.R. Moore PrrC from Rhodobacter sphaeroides, a homologue of eukaryotic Sco proteins, is a copper-binding protein and may have a thiol-disulfide oxidoreductase activity FEBS Lett. 518 2002 10 16
39. A.C. Badrick, A.J. Hamilton, P.V. Bernhardt, C.E. Jones, U. Kappler, M.P. Jennings, and A.G. McEwan PrrC, a Sco homologue from Rhodobacter sphaeroides, possesses thiol-disulfide oxidoreductase activity FEBS Lett. 581 2007 4663 4667
40. A assembly Nat. Chem. Biol. 4 2008 599 601
41. B and magnesium centers of cytochrome c oxidase J. Biol. Chem. 275 2000 619 623
42. B of cytochrome c oxidase Biochemistry 49 2010 5651 5661
43. D.L. Swem, L.R. Swem, A. Setterdahl, and C.E. Bauer Involvement of SenC in assembly of cytochrome c oxidase in Rhodobacter capsulatus J. Bacteriol. 187 2005 8081 8087
44. E. Frangipani, and D. Haas Copper acquisition by the SenC protein regulates aerobic respiration in Pseudomonas aeruginosa PAO1 FEMS Microbiol. Lett. 298 2009 234 240
45. F. Borsetti, V. Tremaroli, F. Michelacci, R. Borghese, C. Winterstein, F. Daldal, and D. Zannoni Tellurite effects on Rhodobacter capsulatus cell viability and superoxide dismutase activity under oxidative stress conditions Res. Microbiol. 156 2005 807 813
46. A center of bacterial cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 102 2005 3994 3999
47. Y.C. Horng, P.A. Cobine, A.B. Maxfield, H.S. Carr, and D.R. Winge Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome c oxidase J. Biol. Chem. 279 2004 35334 35340
48. H. Arunothayanan, M. Nomura, R. Hamaguchi, M. Itakura, K. Minamisawa, and S. Tajima Copper metallochaperones are required for the assembly of bacteroid cytochrome c oxidase which is functioning for nitrogen fixation in soybean nodules Plant Cell Physiol. 51 2010 1242 1246
49. D. Yang, Y. Oyaizu, H. Oyaizu, G.J. Olsen, and C.R. Woese Mitochrondrial origins Proc. Natl. Acad. Sci. U. S. A. 82 1985 4443 4447
50. F.R. Whatley The establishment of mitochondria: Paracoccus and Rhodopseudomonas Ann. N. Y. Acad. Sci. 361 1981 330 340
51. M.R. Bratton, L. Hiser, W.E. Antholine, C. Hoganson, and J.P. Hosler Identification of the structural subunits required for formation of the metal centers in subunit I of cytochrome c oxidase of Rhodobacter sphaeroides Biochemistry 39 2000 12989 12995
52. L. Hiser, and J.P. Hosler Heme A is not essential for assembly of the subunits of cytochrome c oxidase of Rhodobacter sphaeroides J. Biol. Chem. 276 2001 45403 45407
53. W.R. Sistrom A requirement for sodium in the growth of Rhodopseudomonas spheroides J. Gen. Microbiol. 22 1960 778 785
54. M.E. Kovach, R.W. Phillips, P.H. Elzer, R.M. Roop II, and K.M. Peterson pBBR1MCS: a broad-host-range cloning vector Biotechniques 16 1994 800 802
55. L. Varanasi, D. Mills, A. Murphree, J. Gray, C. Purser, R. Baker, and J. Hosler Altering conserved lipid binding sites in cytochrome c oxidase of Rhodobacter sphaeroides perturbs the interaction between subunits I and III and promotes suicide inactivation of the enzyme Biochemistry 45 2006 14896 14907
56. T. Donohue, and S. Kaplan Genetic techniques in Rhodospirillaceae Methods Enzymol. 204 1991 459 485
57. M.F. Alexeyev The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria Biotechniques 26 1999 824 826 828
58. J.M. Eraso, and S. Kaplan From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1 Biochemistry 39 2000 2052 2062
59. L. Varanasi, and J. Hosler Alternative initial proton acceptors for the D pathway of Rhodobacter sphaeroides cytochrome c oxidase Biochemistry 50 2011 2820 2828
60. N. Sone, M. Yoshida, H. Hirata, and Y. Kagawa Asolectin purification procedure J. Biochem. (Tokyo) 81 1977 519 528
61. 3 Can. J. Biochem. 58 1980 969 977
62. 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum J. Bacteriol. 178 1996 1532 1538
63. C. Mackenzie, M. Choudhary, F.W. Larimer, P.F. Predki, S. Stilwagen, J.P. Armitage, R.D. Barber, T.J. Donohue, J.P. Hosler, J.E. Newman, J.P. Shapleigh, R.E. Sockett, J. Zeilstra-Ryalls, and S. Kaplan The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1 Photosynth. Res. 70 2001 19 41
64. N.J. Mouncey, E. Gak, M. Choudhary, J. Oh, and S. Kaplan Respiratory pathways of Rhodobacter sphaeroides 2.4.1(T): identification and characterization of genes encoding quinol oxidases FEMS Microbiol. Lett. 192 2000 205 210
65. 3 terminal oxidase of Rhodobacter sphaeroides 2.4.1: structural and functional implications for the regulation of spectral complex formation Biochemistry 38 1999 2688 2696
66. S. Arnaud, F. Malatesta, B. Guigliarelli, J.P. Gayda, P. Bertrand, R. Miraglio, and M. Denis Purification and characterization of the oxidase from the marine bacterium Pseudomonas nautica 617 Eur. J. Biochem. 198 1991 349 356
67. B FEBS Lett. 412 1997 43 47
68. R. Aasa, P.J. Albracht, K.E. Falk, B. Lanne, and T. Vanngard EPR signals from cytochrome c oxidase Biochim. Biophys. Acta 422 1976 260 272
69. A-binding domain from the Paracoccus cytochrome c oxidase J. Biol. Chem. 268 1993 26416 26421
70. J. van der Oost, P. Lappalainen, A. Musacchio, A. Warne, L. Lemieux, J. Rumbley, R.B. Gennis, R. Aasa, T. Pascher, and B.G. Malmstrom 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 1992 3209 3217
71. A redox site in cytochrome c oxidase into a mononuclear copper center Biochemistry 36 1997 3232 3236
72. M. Jaksch, C. Paret, R. Stucka, N. Horn, J. Muller-Hocker, R. Horvath, N. Trepesch, G. Stecker, P. Freisinger, C. Thirion, J. Muller, R. Lunkwitz, G. Rodel, E.A. Shoubridge, and H. Lochmuller Cytochrome c oxidase deficiency due to mutations in SCO2, encoding a mitochondrial copper-binding protein, is rescued by copper in human myoblasts Hum. Mol. Genet. 10 2001 3025 3035
73. L. Salviati, E. Hernandez-Rosa, W.F. Walker, S. Sacconi, S. DiMauro, E.A. Schon, and M.M. Davidson Copper supplementation restores cytochrome c oxidase activity in cultured cells from patients with SCO2 mutations Biochem. J. 363 2002 321 327
74. 3 and development of symbiosis EMBO J. 12 1993 3373 3383
75. S. Elsen, L.R. Swem, D.L. Swem, and C.E. Bauer RegB/RegA, a highly conserved redox-responding global two-component regulatory system Microbiol. Mol. Biol. Rev. 68 2004 263 279
76. Y.J. Kim, I.J. Ko, J.M. Lee, H.Y. Kang, Y.M. Kim, S. Kaplan, and J.I. Oh Dominant role of the cbb3 oxidase in regulation of photosynthesis gene expression through the PrrBA system in Rhodobacter sphaeroides 2.4.1 J. Bacteriol. 189 2007 5617 5625
77. 3 cytochrome c oxidase of Rhodobacter sphaeroides 2.4.1 J. Biol. Chem. 277 2002 16220 16228
78. Y. Zhen, J. Qian, K. Follmann, T. Hayward, T. Nilsson, M. Dahn, Y. Hilmi, A.G. Hamer, J.P. Hosler, and S. Ferguson-Miller Overexpression and purification of cytochrome c oxidase from Rhodobacter sphaeroides Protein Expr. Purif. 13 1998 326 336