A pivotal heme-transfer reaction intermediate in cytochrome c biogenesis

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2342-2352

  Mavridou, Despoina A I ^a   Stevens, Julie M ^a   Mönkemeyer, Leonie ^a   Daltrop, Oliver ^a   Gleria, Katalin Di ^b   Kessler, Benedikt M ^b   Ferguson, Stuart J ^a   Allen, James W A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; PROTEINS; REACTION INTERMEDIATES;

C-TYPE CYTOCHROME; CATALYTIC INTERMEDIATES; COVALENTLY BOUND; HEME BINDING RESIDUES; HEME CHAPERONE; HEME TRANSFERS; POST-TRANSLATIONAL MODIFICATIONS; TERNARY COMPLEX;

PORPHYRINS;

BINDING PROTEIN; CYTOCHROME C; HEMOPROTEIN; PROTEIN CCME; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BIOGENESIS; CATALYSIS; CHEMICAL REACTION; COMPLEX FORMATION; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT;

EID: 84856068331     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.313692     Document Type: Article

References (38)

1. Barker, P. D., and Ferguson, S. J. (1999) Still a puzzle. Why is heme covalently attached in c-type cytochromes? Structure 7, R281-290 (Pubitemid 30007229)
2. Allen, J. W. (2011) Cytochrome c biogenesis in mitochondria, systems III and V. FEBS J. 278, 4198-4216
3. Allen, J. W., Daltrop, O., Stevens, J. M., and Ferguson, S. J. (2003) c-Type cytochromes, diverse structures and biogenesis systems pose evolutionary problems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 255-266 (Pubitemid 36178234)
4. de Vitry, C. (2011) Cytochrome c maturation system on the negative side of bioenergetic membranes, CCB or system IV. FEBS J. 278, 4189-4197
5. Hamel, P., Corvest, V., Giegé, P., and Bonnard, G. (2009) Biochemical requirements for the maturation of mitochondrial c-type cytochromes. Biochim. Biophys. Acta 1793, 125-138
6. Kranz, R. G., Richard-Fogal, C., Taylor, J. S., and Frawley, E. R. (2009) Cytochrome c biogenesis, mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol. Mol. Biol. Rev. 73, 510-528
7. Simon, J., and Hederstedt, L. (2011) Composition and function of cytochrome c biogenesis system II. FEBS J. 278, 4179-4188
8. Stevens, J. M., Mavridou, D. A., Hamer, R., Kritsiligkou, P., Goddard, A. D., and Ferguson, S. J. (2011) Cytochrome c biogenesis system I. FEBS J. 278, 4170-4178
9. Arslan, E., Schulz, H., Zufferey, R., Künzler, P., and Thöny-Meyer, L. (1998) Overproduction of the Bradyrhizobium japonicum c-type cytochrome subunits of the cbb3 oxidase in Escherichia coli. Biochem. Biophys. Res. Commun. 251, 744-747 (Pubitemid 28512781)
10. Schulz, H., Hennecke, H., and Thöny-Meyer, L. (1998) Prototype of a heme chaperone essential for cytochrome c maturation. Science 281, 1197-1200 (Pubitemid 28406296)
11. Lee, D., Pervushin, K., Bischof, D., Braun, M., and Thöny-Meyer, L. (2005) Unusual heme-histidine bond in the active site of a chaperone. J. Am. Chem. Soc. 127, 3716-3717 (Pubitemid 40411410)
12. Ahuja, U., and Thöny-Meyer, L. (2005) CcmD is involved in complex formation between CcmC and the heme chaperone CcmE during cytochrome c maturation. J. Biol. Chem. 280, 236-243 (Pubitemid 40164985)
13. Christensen, O., Harvat, E. M., Thöny-Meyer, L., Ferguson, S. J., and Stevens, J. M. (2007) Loss of ATP hydrolysis activity by CcmAB results in loss of c-type cytochrome synthesis and incomplete processing of CcmE. FEBS J. 274, 2322-2332 (Pubitemid 46633461)
14. Feissner, R. E., Richard-Fogal, C. L., Frawley, E. R., and Kranz, R. G. (2006) ABC transporter-mediated release of a heme chaperone allows cytochrome c biogenesis. Mol. Microbiol. 61, 219-231
15. Richard-Fogal, C., and Kranz, R. G. (2010) The CcmC-heme-CcmE complex in heme trafficking and cytochrome c biosynthesis. J. Mol. Biol. 401, 350-362
16. Schulz, H., Fabianek, R. A., Pellicioli, E. C., Hennecke, H., and 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. U.S.A. 96, 6462-6467
17. Rayapuram, N., Hagenmuller, J., Grienenberger, J. M., Bonnard, G., and Giegé, P. (2008) The three mitochondrial encoded CcmF proteins form a complex that interacts with CCMH and c-type apocytochromes in Arabidopsis. J. Biol. Chem. 283, 25200-25208
18. Reid, E., Eaves, D. J., and Cole, J. A. (1998) The CcmE protein from Escherichia coli is a heme-binding protein. FEMS Microbiol. Lett. 166, 369-375 (Pubitemid 128384184)
19. Meyer, E. H., Giegé, P., Gelhaye, E., Rayapuram, N., Ahuja, U., Thöny-Meyer, L., Grienenberger, J. M., and Bonnard, G. (2005) AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c. Proc. Natl. Acad. Sci. U.S.A. 102, 16113-16118 (Pubitemid 41552876)
20. Turkarslan, S., Sanders, C., Ekici, S., and Daldal, F. (2008) Compensatory thio-redox interactions between DsbA, CcdA, and CcmG unveil the apocytochrome c holdase role of CcmG during cytochrome c maturation. Mol. Microbiol. 70, 652-666
21. Allen, J. W., Barker, P. D., and Ferguson, S. J. (2003) A cytochrome b562 variant with a c-type cytochrome CXXCH heme-binding motif as a probe of the Escherichia coli cytochrome c maturation system. J. Biol. Chem. 278, 52075-52083 (Pubitemid 38035793)
22. Barker, P. D., Nerou, E. P., Freund, S. M., and Fearnley, I. M. (1995) Conversion of cytochrome b562 to c-type cytochromes. Biochemistry 34, 15191-15203 (Pubitemid 3005523)
23. Allen, J. W., Tomlinson, E. J., Hong, L., and 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, 33559-33563
24. Goddard, A. D., Stevens, J. M., Rondelet, A., Nomerotskaia, E., Allen, J. W., and Ferguson, S. J. (2010) Comparing the substrate specificities of cytochrome c biogenesis systems I and II. FEBS J. 277, 726-737
25. Daltrop, O., Stevens, J. M., Higham, C. W., and Ferguson, S. J. (2002) The CcmE protein of the c-type cytochrome biogenesis system. Unusual in vitro heme incorporation into apo-CcmE and transfer from holo-CcmE to apocytochrome. Proc. Natl. Acad. Sci. U.S.A. 99, 9703-9708 (Pubitemid 34831111)
26. Goodhew, C. F., Brown, K. R., and Pettigrew, G. W. (1986) Haem staining in gels, a useful tool in the study of bacterial c-type cytochromes. Biochim. Biophys. Acta 852, 288-294
27. Batycka, M., Inglis, N. F., Cook, K., Adam, A., Fraser-Pitt, D., Smith, D. G., Main, L., Lubben, A., and Kessler, B. M. (2006) Ultra-fast tandem mass spectrometry scanning combined with monolithic column liquid chromatography increases throughput in proteomic analysis. Rapid Commun. Mass Spectrom. 20, 2074-2080 (Pubitemid 44049032)
28. Kramer, H. B., Lavender, K. J., Qin, L., Stacey, A. R., Liu, M. K., di Gleria, K., Simmons, A., Gasper-Smith, N., Haynes, B. F., McMichael, A. J., Borrow, P., and Kessler, B. M. (2010) Elevation of intact and proteolytic fragments of acute phase proteins constitutes the earliest systemic antiviral response in HIV-1 infection. PLoS Pathog. 6, e1000893
29. Daltrop, O., and Ferguson, S. J. (2003) Cytochrome c maturation. The in vitro reactions of horse heart apocytochrome c and Paracoccus dentrificans apocytochrome c550 with heme. J. Biol. Chem. 278, 4404-4409 (Pubitemid 36800932)
30. Daltrop, O., Smith, K. M., and Ferguson, S. J. (2003) Stereoselective in vitro formation of c-type cytochrome variants from Hydrogenobacter thermophilus containing only a single thioether bond. J. Biol. Chem. 278, 24308-24313 (Pubitemid 37548581)
31. Bartsch, R. G. (1971) Cytochromes: Bacterial. Methods Enzymol. 23, 344-363
32. Mavridou, D. A., Saridakis, E., Kritsiligkou, P., Goddard, A. D., Stevens, J. M., Ferguson, S. J., and Redfield, C. (2011) Oxidation state-dependent protein-protein interactions in disulfide cascades. J. Biol. Chem. 286, 24943-24956
33. Goddard, A. D., Stevens, J. M., Rao, F., Mavridou, D. A., Chan, W., Richardson, D. J., Allen, J. W., and Ferguson, S. J. (2010) c-Type cytochrome biogenesis can occur via a natural Ccm system lacking CcmH, CcmG, and the heme-binding histidine of CcmE. J. Biol. Chem. 285, 22882-22889
34. Allen, J. W., and Ferguson, S. J. (2003) Variation of the axial heme ligands and heme-binding motif as a probe of the Escherichia coli c-type cytochrome maturation (Ccm) system. Biochem. J. 375, 721-728 (Pubitemid 37433521)
35. Allen, J. W., Leach, N., and Ferguson, S. J. (2005) The histidine of the c-type cytochrome CXXCH heme-binding motif is essential for heme attachment by the Escherichia coli cytochrome c maturation (Ccm) apparatus. Biochem. J. 389, 587-592 (Pubitemid 41021162)
36. Daltrop, O., Allen, J. W., Willis, A. C., and Ferguson, S. J. (2002) In vitro formation of a c-type cytochrome. Proc. Natl. Acad. Sci. U.S.A. 99, 7872-7876 (Pubitemid 34650972)
37. Daltrop, O., and Ferguson, S. J. (2004) In vitro studies on thioether bond formation between Hydrogenobacter thermophilus apocytochrome c(552) with metalloprotoporphyrin derivatives. J. Biol. Chem. 279, 45347- 45353
38. Robertson, I. B., Stevens, J. M., and Ferguson, S. J. (2008) Dispensable residues in the active site of the cytochrome c biogenesis protein CcmH. FEBS Lett. 582, 3067-3072