C-type cytochromes: Diverse structures and biogenesis systems pose evolutionary problems

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 358, Issue 1429, 2003, Pages 255-266

  Allen, James W A ^a   Daltrop, Oliver ^a   Stevens, Julie M ^a   Ferguson, Stuart J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

C type cytochromes; Disulphide bond; Haem; Lyase; Maturation systems

Indexed keywords

EVOLUTION; HEMATOLOGY;

EID: 0037471690     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2002.1192     Document Type: Conference Paper

References (97)

1. Allen, J. W. A., Tomlinson, E. J., Hong, L. & Ferguson, S. J. 2002 The Escherichia coli cytochrome c maturation (Ccm) system does not detectably attach heme to single cysteine variants of an apocytochrome c. J. Biol. Chem. 277, 33 559-33 563.
2. 562. Biochemistry 38, 8657-8670.
3. 562. Biochemistry 39, 1499-1514.
4. Barker, P. D. & Ferguson, S. J. 1999 Still a puzzle: why is haem covalently attached in c-type cytochromes? Structure Fold Des. 7, R281-R290.
5. Barker, P. D., Ferrer, J. C., Mylrajan, M., Loehr, T. M., Feng, R., Konishi, Y., Funk, W. D., MacGillivray, R. T. & Mauk, A. G. 1993 Transmutation of a heme protein. Proc. Natl Acad. Sci. USA 90, 6542-6546.
6. 562 to c-type cytochromes. Biochemistry 34, 15 191-15 203.
7. Beckett, C. S., Loughman, J. A., Karberg, K. A., Donato, G. M., Goldman, W. E. & Kranz, R. G. 2000 Four genes are required for the system II cytochrorne c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol. Microbiol. 38, 465-481.
8. Brems, D. N. & Stellwagen, E. 1983 Conformational transitions of a cytochrome c having a single thioether bridge. J. Biol. Chem. 258, 10 919-10 923.
9. Cook, G. M. & Poole, R. K. 2000 Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association. Microbiology 146, 527-536.
10. Daltrop, O., Allen, J. W. A., Willis, A. C. & Ferguson, S. J. 2002a In vitro formation of a c-type cytochrome. Proc. Natl Acad. Sci. USA 99, 7872-7876.
11. Daltrop, O., Stevens, J. M., Higham, C. W. & Ferguson, S. J. 2002b The CcmE protein of the c-type cytochrome biogenesis system: unusual in vitro heme incorporation into apoCcmE and transfer from holo-CcmE to apocytochrome. Proc. Natl Acad. Sci. USA 99, 9703-9708.
12. Dumont, M. E., Corin, A. F. & Campbell, G. A. 1994 Non-covalent binding of heme induces a compact apocytochrome c structure. Biochemistry 33, 7368-7378.
13. 552 nitrite reductase from Escherichia coli. Mol. Microbiol. 28, 205-216.
14. Einsle, O., Messerschmidt, A., Stach, P., Bourenkov, G. P., Bartunik, H. D., Huber, R. & Kroneck, P. M. 1999 Structure of cytochrome c nitrite reductase. Nature 400, 476-480.
15. Erlendsson, L. S. & Hederstedt, L. 2002 Mutations in the thiol-disulfide oxidoreductases BdbC and BdbD can suppress cytochrome c deficiency of CcdA-defective Bacillus subtilis cells. J. Bacteriol. 184, 1423-1429.
16. Fabianek, R. A., Hofer, T. & Thöny-Meyer, L. 1999 Characterization of the Escherichia coli CcmH protein reveals new insights into the redox pathway required for cytochrome c maturation. Arch. Microbiol. 171, 92-100.
17. Fabianek, R. A., Hennecke, H. & Thöny-Meyer, L. 2000 Periplasmic protein thiol:disulfide oxidoreductases of Escherichia coli. FEMS Microbiol. Rev. 24, 303-316.
18. 552 synthesized by Escherichia coli cells expressing the host-specific cytochrome c maturation genes, ccmABCDEFGH: biochemical, spectral, and structural characterization of the recombinant protein. Protein Sci. 9, 2074-2084.
19. Ferguson, S. J. 2001 Keilin's cytochromes: how bacteria use them, vary them and make them. Biochem Soc. Trans. 29, 629-640.
20. Florens, L. 552 Bruschi, M. 1994 Recent advances in the characterization of the hexadecahemic cytochrome c from Desulfovibrio. Biochimie 76, 561-568.
21. 1. Cell 81, 369-377.
22. Goldman, B. S. & Kranz, R. G. 2001 ABC transporters associated with cytochrome c biogenesis. Res. Microbiol. 152, 323-329.
23. Goldman, B. S., Gabbert, K. K. & Kranz, R. G. 1996 Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J. Bacteriol. 178, 6338-6347.
24. Goldman, B. S., Beck, D. L., Monika, E. M. & Kranz, R. G. 1998 Transmembrane heme delivery systems. Proc. Natl Acad. Sci. USA 95, 5003-5008.
25. Hallberg, B. M., Bergfors, T., Backbro, K., Pettersson, G., Henriksson, G. & Divne, C. 2000 A new scaffold for binding haem in the cytochrome domain of the extracellular flavocytochrome cellobiose dehydrogenase. Structure Fold Des. 8, 79-88.
26. Hanlon, S. P., Toh, T. H., Solomon, P. S., Holt, R. A. & McEwan, A. G. 1996 Dimethylsulfide:acceptor oxidoreductase from Rhodobacter sulfidophilus. The purified enzyme contains b-type haem and a pterin molybdenum cofactor. Eur. J. Biochem. 239, 391-396.
27. 1 biosynthesis in Pseudomonas stutzeri. J. Bacteriol. 183, 1663-1671.
28. 3 when the ccm genes are co-expressed. Biochim. Biophys. Acta 1481, 18-24.
29. 3 at 1.8 Å resolution. J. Mol. Biol. 172, 109-139.
30. 1 and other heme groups. J. Biol. Chem. 253, 489-495.
31. Igarashi, N., Moriyama, H., Fujiwara, T., Fukumori, Y. & Tanaka, N. 1997 The 2.8 Å structure of hydroxylamine oxidoreductase from a nitrifying chemoautotrophic bacterium, Nitrosomonas europaea. Nature Struct. Biol. 4, 276-284.
32. Johnson, M. K. 1994 Iron-sulfur proteins. In Encyclopedia of inorganic chemistry (ed. R. B. King), pp. 1896-1915. Chichester, UK: Wiley.
33. Kaderbhai, M. A., Ugochukwu, C. C., Lamb, D. C. & Kelly, S. L. 2000 Targeting of active human cytochrome P4501A1 (CYP1A1) to the periplasmic space of Escherichia coli. Biochem. Biophys. Res. Commun. 279, 803-807.
34. 552 expressed in the cytoplasm and periplasm of Escherichia coli. J. Biol. Inorg. Chem. 7, 260-272.
35. Karim, A., Kaderbhai, N., Evans, A., Harding, V. & Kaderbhai, M. A. 1993 Efficient bacterial export of a eukaryotic cytoplasmic cytochrome. Biotechnology NY 11, 612-618.
36. 552 gene from Thermus thermophilus HB8. Evidence for genetic linkage to an ATP-binding cassette protein and initial characterization of the cycA gene products. J. Biol. Chem. 273, 12 006-12 016.
37. Kniemeyer, O. & Heider, J. 2001 Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J. Biol. Chem. 276, 21 381-21 386.
38. Kranz, R. G., Beckett, C. S. & Goldman, B. S. 2002 Genomic analyses of bacterial respiratory and cytochrome c assembly systems: Bordetella as a model for the system II cytochrome c biogenesis pathway. Res. Microbiol. 153, 1-6.
39. Lawson, D. M., Stevenson, C. E., Andrew, C. R. & Eady, R. R. 2000 Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase. EMBO J. 19, 5661-5671.
40. McCarthy, A. A., Haebel, P. W., Torronen, A., Rybin, V., Baker, E. N. & Metcalf, P. 2000 Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nature Struct. Biol. 7, 196-199.
41. 557 obtained from Escherichia coli cells expressing a truncated Thermus thermophilus cycA gene. Heme inversion in an improperly matured protein. J. Biol. Chem. 276, 6537-6544.
42. Martinez, S. E., Huang, D., Szczepaniak, A., Cramer, W. A. & Smith, J. L. 1994 Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2, 95-105.
43. Martinou, J. C., Desagher, S. & Antonsson, B. 2000 Cytochrome c release from mitochondria: all or nothing. Nature Cell Biol. 2, E41-E43.
44. Metheringham, R., Tyson, K. L., Crooke, H., Missiakas, D., Raina, S. & Cole, J. A. 1996 Effects of mutations in genes for proteins involved in disulphide bond formation in the periplasm on the activities of anaerobically induced electron transfer chains in Escherichia coli K12. Mol. Gen. Genet. 253, 95-102.
45. Moore, G. R. & Pettigrew, G. W. 1990 Cytochromes c: evolutionary, structural, and physicochemical aspects. Springer series in molecular biology. New York: Springer.
46. Nicholson, D. W. & Neupert, W. 1989 Import of cytochrome c into mitochondria: reduction of heme, mediated by NADH and flavin nucleotides, is obligatory for its covalent linkage to apocytochrome c. Proc. Natl Acad. Sci. USA 86, 4340-4344.
47. Page, C. C., Moser, C. C., Chen, X. & Dutton, P. L. 1999 Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52.
48. Page, M. D., Pearce, D. A., Norris, H. A. & Ferguson, S. J. 1997a The Paracoccus denitrificans ccmA, B and C genes: cloning and sequencing, and analysis of the potential of their products to form a haem or apo- c-type cytochrome transporter. Microbiology 143, 563-576.
49. Page, M. D., Tomlinson, E. & Ferguson, S. J. 1997b Unexpected implications from the Helicobacter pylori genome for understanding periplasmic c-type cytochrome assembly in Gram-negative bacteria in coexistence with disulphide bond formation. Mol. Microbiol. 26, 413-415.
50. Page, M. D., Sambongi, Y. & Ferguson, S. J. 1998 Contrasting routes of c-type cytochrome assembly in mitochondria, chloroplasts and bacteria. Trends Biochem Sci. 23, 103-108.
51. Pearce, D. A., Page, M. D., Norris, H. A., Tomlinson, E. J. & Ferguson, S. J. 1998 Identification of the contiguous Paracoccus denitrificans ccmF and ccmH genes: disruption of ccmF, encoding a putative transporter, results in formation of an unstable apocytochrome c and deficiency in siderophore production. Microbiology 144, 467-477.
52. Pettigrew, G. W. & Moore, G. R. 1987 Cytochromes: biological aspects. Springer series in molecular biology. New York: Springer.
53. Pettigrew, G. W., Aviram, I. & Schejter, A. 1975 Physicochemical properties of two atypical cytochromes c, Crithidia cytochrome c-557 and Euglena cytochrome c-558. Biochem. J. 149, 155-167.
54. Pisa, R., Stein, T., Eichler, R., Gross, R. & Simon, J. 2002 The nrfI gene is essential for the attachment of the active site haem group of Wolinella succinogenes cytochrome c nitrite reductase. Mol. Microbiol. 43, 763-770.
55. Pollock, W. B., Rosell, F. I., Twitchett, M. B., Dumont, M. E. & Mauk, A. G. 1998 Bacterial expression of a mitochondrial cytochrome c. Trimethylation of lys72 in yeast iso-1-cytochrome c and the alkaline conformational transition. Biochemistry 37, 6124-6131.
56. Poole, R. K., Gibson, F. & Wu, G. 1994 The cydD gene product, component of a heterodimeric ABC transporter, is required for assembly of periplasmic cytochrome c and of cytochrome bd in Escherichia coli. FEMS Microbiol. Lett. 117, 217-223.
57. 1. J. Biol. Chem. 267, 20 188-20 195.
58. Pugsley, A. P., Bayan, N. & Sauvonnet, N. 2001 Disulfide bond formation in secreton component PulK provides a possible explanation for the role of DsbA in pullulanase secretion. J. Bacteriol. 183, 1312-1319.
59. Reid, E., Eaves, D. J. & Cole, J. A. 1998 The CcmE protein from Escherichia coli is a haem-binding protein. FEMS Microbiol. Lett. 166, 369-375.
60. Reid, E., Cole, J. & Eaves, D. J. 2001 The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly. Biochem. J. 355, 51-58.
61. Ren, Q., Ahuja, U. & Thöny-Meyer, L. 2002 A bacterial cytochrome c heme lyase. CcmF forms a complex with the heme chaperone CcmE and CcmH but not with apocytochrome c. J. Biol. Chem. 277, 7657-7663.
62. Richardson, D. J. 2000 Bacterial respiration: a flexible process for a changing environment. Microbiology 146, 551-571.
63. 2 proteins with altered heme attachment sites. Arch. Biochem. Biophys. 389, 234-244.
64. Robinson, C. & Bolhuis, A. 2001 Protein targeting by the twin-arginine translocation pathway. Nature Rev. Mol. Cell Biol. 2, 350-356.
65. Roldan, M. D., Sears, H. J., Cheesman, M. R., Ferguson, S. J., Thomson, A. J., Berks, B. C. & Richardson, D. J. 1998 Spectroscopic characterization of a novel multiheme c-type cytochrome widely implicated in bacterial electron transport. J. Biol. Chem. 273, 28 785-28 790.
66. Rosell, F. I. & Mauk, A. G. 2002 Spectroscopic properties of a mitochondrial cytochrome c with a single thioether bond to the heme prosthetic group. Biochemistry 41, 7811-7818.
67. Sambongi, Y. & Ferguson, S. J. 1994a Specific thiol compounds complement deficiency in c-type cytochrome biogenesis in Escherichia coli carrying a mutation in a membrane-bound disulphide isomerase-like protein. FEBS Lett. 353, 235-238.
68. 552 does not. Implications for c-type cytochrome biogenesis. FEBS Lett. 340, 65-70.
69. Sambongi, Y. & Ferguson, S. J. 1996 Mutants of Escherichia coli lacking disulphide oxidoreductases DsbA and DsbB cannot synthesise an exogenous monohaem c-type cytochrome except in the presence of disulphide compounds. FEBS Lett. 398, 265-268.
70. 550 probes pathway of c-type cytochrome biogenesis in Escherichia coli. Mol. Microbiol. 19, 1193-1204.
71. 552 gene from Hydrogenobacter thermophilus. Eur. J. Biochem. 198, 7-12.
72. Sanders, C. & Lill, H. 2000 Expression of prokaryotic and eukaryotic cytochromes c in Escherichia coli. Biochim. Biophys. Acta 1459, 131-138.
73. Sanders, C., Wethkamp, N. & Lill, H. 2001 Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41, 241-246.
74. Sargent, F., Berks, B. C. & Palmer, T. 2002 Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch. Microbiol. 178, 77-84.
75. Schlarb, B. G., Wagner, M. J., Vijgenboom, E., Ubbink, M., Bendall, D. S. & Howe, C. J. 1999 Expression of plastocyanin and cytochrome f of the cyanobacterium Phormidium laminosum in Escherichia coli and Paracoccus denitrificans and the role of leader peptides. Gene 234, 275-283.
76. Schroder, I., Rech, S., Krafft, T. & Macy, J. M. 1997 Purification and characterization of the selenate reductase from Thauera selenatis. J. Biol. Chem. 272, 23 765-23 768.
77. Schulz, H., Hennecke, H. & Thöny-Meyer, L. 1998 Prototype of a heme chaperone essential for cytochrome c maturation. Science 281, 1197-1200.
78. Schulz, H., Fabianek, R. A., Pellicioli, E. C., Hennecke, H. & Thöny-Meyer, L. 1999 Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB. Proc. Natl Acad. Sci. USA 96, 6462-6467.
79. Scott, R. A. & Mauk, A. G. 1995 Cytochrome c: a multidisciplinary approach. Mill Valley, CA: University Science Books.
80. Setterdahl, A. T., Goldman, B. S., Hirasawa, M., Jacquot, P., Smith, A. J., Kranz, R. G. & Knaff, D. B. 2000 Oxidation-reduction properties of disulfide-containing proteins of the Rhodobacter capsulatus cytochrome c biogenesis system. Biochemistry 39, 10 172-10 176.
81. Simon, J., Gross, R., Einsle, O., Kroneck, P. M., Kroger, A. & Klimmek, O. 2000 A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes. Mol. Microbiol. 35, 686-696.
82. Simon, J., Eichler, R., Pisa, R., Biel, S. & Gross, R. 2002 Modification of heme c binding motifs in the small subunit (NrfH) of the Wolinella succinogenes cytochrome c nitrite reductase complex. FEBS Lett. 522, 83-87.
83. 552 maturation. FEMS Microbiol. Lett. 161, 1-6.
84. Spielewoy, N., Schulz, H., Grienenberger, J. M., Thöny-Meyer, L. & Bonnard, G. 2001 CcmE, a nuclear-encoded heme-binding protein involved in cytochrome c maturation in plant mitochondria. J. Biol. Chem. 276, 5491-5497.
85. Steiner, H., Kispal, G., Zollner, A., Haid, A., Neupert, W. & Lill, R. 1996 Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J. Biol. Chem. 271, 32 605-32 611.
86. Tanaka, Y., Kubota, I., Amachi, T., Yoshizumi, H. & Matsubara, H. 1990 Site-directedly mutated human cytochrome c which retains heme c via only one thioether bond. J. Biochem. (Tokyo) 108, 7-8.
87. Tezcan, F. A., Winkler, J. R. & Gray, H. B. 1998 Effects of ligation and folding on reduction potentials of heme proteins. J. Am. Chem. Soc. 120, 13 383-13 388.
88. Thöny-Meyer, L. 1997 Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61, 337-376.
89. Thöny-Meyer, L. 2000 Haem-polypeptide interactions during cytochrome c maturation. Biochim. Biophys. Acta 1459, 316-324.
90. Thöny-Meyer, L. & Kunzler, P. 1997 Translocation to the periplasm and signal sequence cleavage of preapocytochrome c depend on sec and lep, but not on the ccm gene products. Eur. J. Biochem. 246, 794-799.
91. Throne-Holst, M., Thöny-Meyer, L. & Hederstedt, L. 1997 Escherichia coli ccm in-frame deletion mutants can produce periplasmic cytochrome b but not cytochrome c. FEBS Lett. 410, 351-355.
92. Tomlinson, E. J. & Ferguson, S. J. 2000a Conversion of a c type cytochrome to a b type that spontaneously forms in vitro from apo protein and heme: implications for c type cytochrome biogenesis and folding. Proc. Natl Acad. Sci. USA 97, 5156-5160.
93. Tomlinson, E. J. & Ferguson, S. J. 2000b Loss of either of the two heme-binding cysteines from a class I c-type cytochrome has a surprisingly small effect on physicochemical properties. J. Biol. Chem. 275, 32 530-32 534.
94. Tong, J. & Margoliash, E. 1998 Cytochrome c heme lyase activity of yeast mitochondria. J. Biol. Chem. 273, 25 695-25 702.
95. Vu, B. C., Jones, A. D. & Lecomte, J. T. J. 2002 Novel histidine-heme covalent linkage in a hemoglobin. J. Am. Chem. Soc. 124, 8544-8545.
96. Wood, P. M. 1983 Why do c-type cytochromes exist? FEBS Lett. 164, 223-226.
97. Zumft, W. G. 1997 Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616.