Biochemical requirements for the maturation of mitochondrial c-type cytochromes

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 1, 2009, Pages 125-138

  Hamel, Patrice ^a   Corvest, Vincent ^a   Giegé, Philippe ^b   Bonnard, Géraldine ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b CNRS   (France)

Author keywords

Cytochrome c assembly; Heme lyase; Heme transport; Mitochondria; Redox chemistry; Thioether linkage

Indexed keywords

CYTOCHROME C; MITOCHONDRIAL ENZYME;

ELECTRON TRANSPORT; ENERGY TRANSFER; ENZYME ANALYSIS; ENZYME SYNTHESIS; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; REVIEW; THYLAKOID;

ANIMALS; APOPROTEINS; CYTOCHROMES C; HEME; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION;

BACTERIA (MICROORGANISMS);

EID: 56349110794     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.06.017     Document Type: Review

References (182)

1. Allen J.W., Daltrop O., Stevens J.M., and Ferguson S.J. C-type cytochromes: diverse structures and biogenesis systems pose evolutionary problems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 255-266
2. Thöny-Meyer L. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61 (1997) 337-376
3. Ambler R.P. Sequence variability in bacterial cytochromes c. Biochim. Biophys. Acta 1058 (1991) 42-47
4. Pettigrew G.W., and Moore G.R. Cytochromes c. Biological Aspects (1987), SpringerVerlag, Berlin-Heidelberg-New York
5. Jungst A., Wakabayashi S., Matsubara H., and Zumft W.G. The nirSTBM region coding for cytochrome cd1-dependent nitrite respiration of Pseudomonas stutzeri consists of a cluster of mono-, di-, and tetraheme proteins. FEBS Lett. 279 (1991) 205-209
6. Hartshorne S., Richardson D.J., and Simon J. Multiple haem lyase genes indicate substrate specificity in cytochrome c biogenesis. Biochem. Soc. Trans. 34 (2006) 146-149
7. Allen J.W., Ginger M.L., and Ferguson S.J. Maturation of the unusual single-cysteine (XXXCH) mitochondrial c-type cytochromes found in trypanosomatids must occur through a novel biogenesis pathway. Biochem. J. 383 (2004) 537-542
8. Daltrop O., Smith K.M., and Ferguson S.J. Stereoselective in vitro formation of c-type cytochrome variants from Hydrogenobacter thermophilus containing only a single thioether bond. J. Biol. Chem. 278 (2003) 24308-24313
9. Howe G., and Merchant S. The biosynthesis of bacterial and plastidic c-type cytochromes. Photosyn. Res. 40 (1994) 147-165
10. Barker P.D., and Ferguson S.J. Still a puzzle: why is haem covalently attached in c-type cytochromes?. Struct. Fold Des. 7 (1999) 281-290
11. Berry E.A., Guergova-Kuras M., Huang L.S., and Crofts A.R. Structure and function of cytochrome bc complexes. Annu. Rev. Biochem. 69 (2000) 1005-1075
12. Kranz R., Lill R., Goldman B., Bonnard G., and Merchant S. Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol. Microbiol. 29 (1998) 383-396
13. Nakamoto S.S., Hamel P., and Merchant S. Assembly of chloroplast cytochromes b and c. Biochimie 82 (2000) 603-614
14. Stevens J.M., Uchida T., Daltrop O., and Ferguson S.J. Covalent cofactor attachment to proteins: cytochrome c biogenesis. Biochem. Soc. Trans. 33 (2005) 792-795
15. Thöny-Meyer L. Cytochrome c maturation: a complex pathway for a simple task?. Biochem. Soc. Trans. 30 (2002) 633-638
16. 6. J. Biol. Chem. 272 (1997) 32427-32435
17. Kuras R., Saint-Marcoux D., Wollman F.A., and de Vitry C. A specific c-type cytochrome maturation system is required for oxygenic photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 9906-9910
18. Lyska D., Paradies S., Meierhoff K., and Westhoff P. HCF208, a homolog of Chlamydomonas CCB2, is required for accumulation of native cytochrome b6 in Arabidopsis thaliana. Plant Cell Physiol. 48 (2007) 1737-1746
19. Stroebel D., Choquet Y., Popot J.L., and Picot D. An atypical haem in the cytochrome b(6)f complex. Nature 426 (2003) 413-418
20. Kurisu G., Zhang H., Smith J.L., and Cramer W.A. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302 (2003) 1009-1014
21. Spielewoy N., Schulz H., Grienenberger J.M., Thöny-Meyer L., and Bonnard G. CCME, a nuclear-encoded heme-binding protein involved in cytochrome c maturation in plant mitochondria. J. Biol. Chem. 276 (2001) 5491-5497
22. Meyer E.H., Giege P., Gelhaye E., Rayapuram N., Ahuja U., Thony-Meyer L., Grienenberger J.M., and Bonnard G. 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 (2005) 16113-16118
23. Rayapuram N., Hagenmuller J., Grienenberger J.M., Giegé P., and Bonnard G. AtCCMA interacts with AtCcmB to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in Arabidopsis. J. Biol. Chem. 282 (2007) 21015-21023
24. Feissner R.E., Richard-Fogal C.L., Frawley E.R., and Kranz R.G. ABC transporter-mediated release of a haem chaperone allows cytochrome c biogenesis. Mol. Microbiol. 61 (2006) 219-231
25. Goldman B.S., and Kranz R.G. ABC transporters associated with cytochrome c biogenesis. Res. Microbiol. 152 (2001) 323-329
26. Thony-Meyer L. A heme chaperone for cytochrome c biosynthesis. Biochemistry 42 (2003) 13099-13105
27. Giege P., Grienenberger J.M., and Bonnard G. Cytochrome c biogenesis in mitochondria. Mitochondrion 8 (2008) 61-73
28. Fabianek R.A., Hennecke H., and Thöny-Meyer L. Periplasmic protein thiol:disulfide oxidoreductases of Escherichia coli. FEMS Microbiol. Rev. 24 (2000) 303-316
29. Kadokura H., Katzen F., and Beckwith J. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72 (2003) 111-135
30. Ahuja U., and Thony-Meyer L. Dynamic features of a heme delivery system for cytochrome c maturation. J. Biol. Chem 278 (2003) 52061-52070
31. Deshmukh M., May M., Zhang Y., Gabbert K.K., Karberg K.A., Kranz R.G., and Daldal F. Overexpression of ccl1-2 can bypass the need for the putative apocytochrome chaperone CycH during the biogenesis of c-type cytochromes. Mol. Microbiol. 46 (2002) 1069-1080
32. Ren Q., Ahuja U., and Thöny-Meyer L. 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 (2002) 7657-7663
33. Sanders C., Deshmukh M., Astor D., Kranz R.G., and Daldal F. Overproduction of CcmG and CcmFH(Rc) fully suppresses the c-type cytochrome biogenesis defect of Rhodobacter capsulatus CcmI-null mutants. J. Bacteriol. 187 (2005) 4245-4256
34. Xie Z., Culler D., Dreyfuss B.W., Kuras R., Wollman F.A., Girard-Bascou J., and Merchant S. Genetic analysis of chloroplast c-type cytochrome assembly in Chlamydomonas reinhardtii: one chloroplast locus and at least four nuclear loci are required for heme attachment. Genetics 148 (1998) 681-692
35. Dreyfuss B.W., and Merchant S. CCS5, a new locus required for chloroplast c-type synthesis. In: Pusztai J., and Garab G. (Eds). Proceedings of the XIth International Congress on Photosynthesis (1999), Kluwer Academic Publishers, The Nederlands 3139-3142
36. Page M.L.D., Hamel P.P., Gabilly S.T., Zegzouti H., Perea J.V., Alonso J.M., Ecker J.R., Theg S.M., Christensen S.K., and Merchant S. A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J. Biol. Chem. 279 (2004) 32474-32482
37. Xie Z., and Merchant S. The plastid-encoded ccsA gene is required for heme attachment to chloroplast c-type cytochromes. J. Biol. Chem. 271 (1996) 4632-4639
38. Inoue K., Dreyfuss B.W., Kindle K.L., Stern D.B., Merchant S., and Sodeinde O.A. CCS1, a nuclear gene required for the post-translational assembly of chloroplast c-type cytochromes. J. Biol. Chem. 272 (1997) 31747-31754
39. Tichy M., and Vermaas W. Accumulation of pre-apocytochrome f in a Synechocystis sp. PCC 6803 mutant impaired in cytochrome c maturation. J. Biol. Chem. 274 (1999) 32396-32401
40. Beckett C.S., Loughman J.A., Karberg K.A., Donato G.M., Goldman W.E., and Kranz R.G. Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol. Microbiol. 38 (2000) 465-481
41. Le Brun N.E., Bengtsson J., and Hederstedt L. Genes required for cytochrome c synthesis in Bacillus subtilis. Mol. Microbiol. 36 (2000) 638-650
42. Goldman B.S., Beck D.L., Monika E.M., and Kranz R.G. Transmembrane heme delivery systems. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 5003-5008
43. Hamel P.P., Dreyfuss B.W., Xie Z., Gabilly S.T., and Merchant S. Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J. Biol. Chem. 278 (2003) 2593-2603
44. Dreyfuss B.W., Hamel P.P., Nakamoto S.S., and Merchant S. Functional analysis of a divergent system II protein, Ccs1, involved in c-type cytochrome biogenesis. J. Biol. Chem. 278 (2003) 2604-2613
45. Feissner R.E., Richard-Fogal C.L., Frawley E.R., Loughman J.A., Earley K.W., and Kranz R.G. Recombinant cytochromes c biogenesis systems I and II and analysis of haem delivery pathways in Escherichia coli. Mol. Microbiol. 60 (2006) 563-577
46. Deshmukh M., Brasseur G., and Daldal F. Novel Rhodobacter capsulatus genes required for the biogenesis of various c-type cytochromes. Mol. Microbiol. 35 (2000) 123-138
47. Bardischewsky F., and Friedrich C.G. Identification of ccdA in Paracoccus pantotrophus GB17: disruption of ccdA causes complete deficiency in c-type cytochromes. J. Bacteriol. 183 (2001) 257-263
48. Erlendsson L.S., and Hederstedt L. Mutations in the thiol-disulfide oxidoreductases BdbC and BdbD can suppress cytochrome c deficiency of CcdA-defective Bacillus subtilis cells. J. Bacteriol. 184 (2002) 1423-1429
49. 6f complex in Arabidopsis. Plant Cell 13 (2001) 2351-2539
50. Erlendsson L.S., Acheson R.M., Hederstedt L., and Le Brun N.E. Bacillus subtilis ResA is a thiol-disulfide oxidoreductase involved in cytochrome c synthesis. J. Biol. Chem. 278 (2003) 17852-17858
51. Dumont M.E., Ernst J.F., Hampsey D.M., and Sherman F. Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. EMBO J. 6 (1987) 235-241
52. Drygas M.E., Lambowitz A.M., and Nargang F.E. Cloning and analysis of the Neurospora crassa gene for cytochrome c heme lyase. J. Biol. Chem. 264 (1989) 17897-17906
53. 1-heme lyase. Eur. J. Biochem. 207 (1992) 1093-1100
54. Cervera A.M., Gozalbo D., McCreath K.J., Gow N.A., Martinez J.P., and Casanova M. Molecular cloning and characterization of a Candida albicans gene coding for cytochrome c haem lyase and a cell wall-related protein. Mol. Microbiol. 30 (1998) 67-81
55. Bernard D.G., Gabilly S.T., Dujardin G., Merchant S., and Hamel P.P. Overlapping specificities of the mitochondrial cytochrome c and c1 heme lyases. J. Biol. Chem. 278 (2003) 49732-49742
56. Stuart R.A., and Neupert W. Apocytochrome c: an exceptional mitochondrial precursor protein using an exceptional import pathway. Biochimie 72 (1990) 115-121
57. Dumont M.E. Mitochondrial import of cytochrome c. In: Hart F.-U. (Ed). Advances in Molecular and Cell Biology (1996), JAI Press, Greenwich, UK 103-126
58. Steiner H., Kispal G., Zollner A., Haid A., Neupert W., and Lill R. Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J. Biol. Chem. 271 (1996) 32605-32611
59. Sherman F. Studies of yeast cytochrome c: how and why started and why they continued. Genetics 125 (1990) 9-12
60. Nicholson D.W., and Neupert W. 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. U. S. A. 86 (1989) 4340-4344
61. 1 heme lyase and of the two proteolytic processing steps during import into mitochondria. J. Biol. Chem. 264 (1989) 10156-10168
62. Bernard D.G., Quevillon-Cheruel S., Merchant S., Guiard B., and Hamel P.P. Cyc2p, a membrane-bound flavoprotein involved in the maturation of mitochondrial c-type cytochromes. J. Biol. Chem. 280 (2005) 39852-39859
63. Diekert K., Kispal G., Guiard B., and Lill R. An internal targeting signal directing proteins into the mitochondrial intermembrane space. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11752-11757
64. Diekert K., de Kroon A.I., Ahting U., Niggemeyer B., Neupert W., de Kruijff B., and Lill R. Apocytochrome c requires the TOM complex for translocation across the mitochondrial outer membrane. EMBO J. 20 (2001) 5626-5635
65. Wiedemann N., Kozjak V., Prinz T., Ryan M.T., Meisinger C., Pfanner N., and Truscott K.N. Biogenesis of yeast mitochondrial cytochrome c: a unique relationship to the TOM machinery. J. Mol. Biol. 327 (2003) 465-474
66. Mayer A., Neupert W., and Lill R. Translocation of apocytochrome c across the outer membrane of mitochondria. J. Biol. Chem. 270 (1995) 12390-12397
67. Dumont M.E., Ernst J.F., and Sherman F. Coupling of heme attachment to import of cytochrome c into yeast mitochondria. Studies with heme lyase-deficient mitochondria and altered apocytochromes c. J. Biol. Chem. 263 (1988) 15928-15937
68. Dumont M.D., Mathews A.J., Nall B.T., Baim S.B., Eustice D.C., and Sherman F. Differential stability of two apo-isocytochromes c in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 265 (1990) 2733-2739
69. Dumont M.E., Cardillo T.S., Hayes M.K., and Sherman F. Role of cytochrome c heme lyase in mitochondrial import and accumulation of cytochrome c in Saccharomyces cerevisiae. Mol. Cell. Biol. 11 (1991) 5487-5496
70. Nargang F.E., Drygas M.E., Kwong P.L., Nicholson D.W., and Neupert W. A mutant of Neurospora crassa deficient in cytochrome c heme lyase activity cannot import cytochrome c into mitochondria. J. Biol. Chem. 263 (1988) 9388-9394
71. Schwarz Q.P., and Cox T.C. Complementation of a yeast CYC3 deficiency identifies an X-linked mammalian activator of apocytochrome c. Genomics 79 (2002) 51-57
72. Arnold I., Folsch H., Neupert W., and Stuart R.A. Two distinct and independent mitochondrial targeting signals function in the sorting of an inner membrane protein, cytochrome c1. J. Biol. Chem. 273 (1998) 1469-1476
73. 1 and the adenine nucleotide translocator. EMBO J. 11 (1992) 4787-4794
74. 2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell 69 (1992) 809-822
75. 1 is processed in two steps, one of them heme-dependent. J. Biol. Chem. 257 (1982) 13042-13047
76. Nunnari J., Fox T.D., and Walter P. A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262 (1993) 1997-2004
77. Zollner A., Rodel G., and Haid A. Molecular cloning and characterization of the Saccharomyces cerevisiae CYT2 gene encoding cytochrome-c1-heme lyase. Eur. J. Biochem. 207 (1992) 1093-1100
78. Steiner H., Kispal G., Zollner A., Haid A., Neupert W., and Lill R. Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J. Biol. Chem. 271 (1996) 32605-32611
79. Priest J.W., and Hajduk S.L. Trypanosoma brucei cytochrome c1 is imported into mitochondria along an unusual pathway. J. Biol. Chem. 278 (2003) 15084-15094
80. Tanaka R., and Tanaka A. Tetrapyrrole biosynthesis in higher plants. Annu. Rev. Plant Biol. 58 (2007) 321-346
81. Masuda T. Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth. Res. 96 (2008) 121-143
82. Elder G.H., and Evans J.O. Evidence that the coproporphyrinogen oxidase activity of rat liver is situated in the intermembrane space of mitochondria. Biochem. J. 172 (1978) 345-347
83. Grandchamp B., Phung N., and Nordmann Y. The mitochondrial localization of coproporphyrinogen III oxidase. Biochem. J. 176 (1978) 97-102
84. Camadro J.M., Chambon H., Jolles J., and Labbe P. Purification and properties of coproporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 156 (1986) 579-587
85. Koch M., Breithaupt C., Kiefersauer R., Freigang J., Huber R., and Messerschmidt A. Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. Embo J. 23 (2004) 1720-1728
86. Rao A.U., Carta L.K., Lesuisse E., and Hamza I. Lack of heme synthesis in a free-living eukaryote. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4270-4275
87. Atteia A., van Lis R., and Beale S.I. Enzymes of the heme biosynthetic pathway in the nonphotosynthetic alga Polytomella sp. Eukaryot. Cell 4 (2005) 2087-2097
88. Cornah J.E., Roper J.M., Pal Singh D., and Smith A.G. Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem. J. 362 (2002) 423-432
89. Smith A.G., Marsh O., and Elder G.H. Investigation of the subcellular location of the tetrapyrrole-biosynthesis enzyme coproporphyrinogen oxidase in higher plants. Biochem. J. 292 (1993) 503-508
90. Santana M.A., Tan F.-C., and Smith A.G. Molecular characterisation of coproporphyrinogen oxidase from Glycine max and Arabidopsis thaliana. Plant Physiol. Biochem. 40 (2002) 289-298
91. Williams P., Hardeman K., Fowler J., and Rivin C. Divergence of duplicated genes in maize: evolution of contrasting targeting information for enzymes in the porphyrin pathway. Plant J. 45 (2006) 727-739
92. Hoa le T.P., Nomura M., Kajiwara H., Day D.A., and Tajima S. Proteomic analysis on symbiotic differentiation of mitochondria in soybean nodules. Plant Cell Physiol. 45 (2004) 300-308
93. Lermontova I., Kruse E., Mock H.P., and Grimm B. Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8895-8900
94. Patzoldt W.L., Hager A.G., McCormick J.S., and Tranel P.J. A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 12329-12334
95. Watanabe N., Che F.S., Iwano M., Takayama S., Yoshida S., and Isogai A. Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J. Biol. Chem. 276 (2001) 20474-20481
96. Chow K.S., Singh D.P., Roper J.M., and Smith A.G. A single precursor protein for ferrochelatase-I from Arabidopsis is imported in vitro into both chloroplasts and mitochondria. J. Biol. Chem. 272 (1997) 27565-27571
97. Cleary S.P., Tan F.C., Nakrieko K.A., Thompson S.J., Mullineaux P.M., Creissen G.P., von Stedingk E., Glaser E., Smith A.G., and Robinson C. Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J. Biol. Chem. 277 (2002) 5562-5569
98. Lister R., Chew O., Rudhe C., Lee M.N., and Whelan J. Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett. 506 (2001) 291-295
99. Masuda T., Suzuki T., Shimada H., Ohta H., and Takamiya K. Subcellular localization of two types of ferrochelatase in cucumber. Planta 217 (2003) 602-609
100. van Lis R., Atteia A., Nogaj L.A., and Beale S.I. Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii. Plant Physiol. 139 (2005) 1946-1958
101. Bannister L.H., Hopkins J.M., Fowler R.E., Krishna S., and Mitchell G.H. A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol. Today 16 (2000) 427-433
102. Kobayashi T., Sato S., Takamiya S., Komaki-Yasuda K., Yano K., Hirata A., Onitsuka I., Hata M., Mi-ichi F., Tanaka T., Hase T., Miyajima A., Kawazu S.-i., Watanabe Y.-i., and Kita K. Mitochondria and apicoplast of Plasmodium falciparum: behaviour on subcellular fractionation and the implication. Mitochondrion 7 (2007) 125-132
103. Waller R.F., and McFadden G.I. The apicoplast: a review of the derived plastid of apicomplexan parasites. Curr. Issues Mol. Biol. 7 (2005) 57-79
104. Hamza I. Intracellular trafficking of porphyrins. ACS Chem. Biol. 1 (2006) 627-629
105. Taketani S., Kohno H., Okuda M., Furukawa T., and Tokunaga R. Induction of peripheral-type benzodiazepine receptors during differentiation of mouse erythroleukemia cells. A possible involvement of these receptors in heme biosynthesis. J. Biol. Chem. 269 (1994) 7527-7531
106. Lindemann P., Koch A., Degenhardt B., Hause G., Grimm B., and Papadopoulos V. A novel Arabidopsis thaliana protein is a functional peripheral-type benzodiazepine receptor. Plant Cell Physiol. 45 (2004) 723-733
107. Krishnamurthy P.C., Du G., Fukuda Y., Sun D., Sampath J., Mercer K.E., Wang J., Sosa-Pineda B., Murti K.G., and Schuetz J.D. Identification of a mammalian mitochondrial porphyrin transporter. Nature 443 (2006) 586-589
108. Kispal G., Csere P., Prohl C., and Lill R. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. Embo J. 18 (1999) 3981-3989
109. Kabe Y., Ohmori M., Shinouchi K., Tsuboi Y., Hirao S., Azuma M., Watanabe H., Okura I., and Handa H. Porphyrin accumulation in mitochondria is mediated by 2-oxoglutarate carrier. J. Biol. Chem. 281 (2006) 31729-31735
110. Goldman B.S., Gabbert K.K., and Kranz R.G. Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J. Bacteriol. 178 (1996) 6338-6347
111. Throne-Holst M., Thöny-Meyer L., and Hederstedt L. Escherichia coli ccm in-frame deletion mutants can produce periplasmic cytochrome b but not cytochrome c. FEBS Lett. 410 (1997) 351-355
112. Baert B., Baysse C., Matthijs S., and Cornelis P. Multiple phenotypic alterations caused by a c-type cytochrome maturation ccmC gene mutation in Pseudomonas aeruginosa. Microbiology 154 (2008) 127-138
113. Baysse C., Budzikiewicz H., Uria Fernandez D., and Cornelis P. Impaired maturation of the siderophore pyoverdine chromophore in Pseudomonas fluorescens ATCC 17400 deficient for the cytochrome c biogenesis protein CcmC. FEBS Lett. 523 (2002) 23-28
114. Lee H.C., Hon T., Lan C., and Zhang L. Structural environment dictates the biological significance of heme-responsive motifs and the role of Hsp90 in the activation of the heme activator protein Hap1. Mol. Cell. Biol. 23 (2003) 5857-5866
115. Pfeifer K., Kim K.S., Kogan S., and Guarente L. Functional dissection and sequence of yeast HAP1 activator. Cell 56 (1989) 291-301
116. Hickman M.J., and Winston F. Heme levels switch the function of Hap1 of Saccharomyces cerevisiae between transcriptional activator and transcriptional repressor. Mol. Cell. Biol. 27 (2007) 7414-7424
117. Ogawa K., Sun J., Taketani S., Nakajima O., Nishitani C., Sassa S., Hayashi N., Yamamoto M., Shibahara S., Fujita H., and Igarashi K. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. Embo J. 20 (2001) 2835-2843
118. Hira S., Tomita T., Matsui T., Igarashi K., and Ikeda-Saito M. Bach1, a heme-dependent transcription factor, reveals presence of multiple heme binding sites with distinct coordination structure. IUBMB Life 59 (2007) 542-551
119. Chen J.-J., and London I.M. Regulation of protein synthesis by heme-regulated eIF-2[alpha] kinase. Trends Biochem. Sci. 20 (1995) 105-108
120. Lathrop J.T., and Timko M.P. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259 (1993) 522-525
121. Zhang L., and Guarente L. Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J. 14 (1995) 313-320
122. Schulz H., Hennecke H., and Thöny-Meyer L. Prototype of a heme chaperone essential for cytochrome c maturation. Science 281 (1998) 1197-1200
123. Arnesano F., Banci L., Barker P.D., Bertini I., Rosato A., Su X.C., and Viezzoli M.S. Solution structure and characterization of the heme chaperone CcmE. Biochemistry 41 (2002) 13587-13594
124. Enggist E., Thöny-Meyer L., Guntert P., and Pervushin K. NMR structure of the heme chaperone CcmE reveals a novel functional motif. Structure (Camb.) 10 (2002) 1551-1557
125. Enggist E., Schneider M.J., Schulz H., and Thöny-Meyer L. Biochemical and mutational characterization of the heme chaperone CcmE reveals a heme binding site. J. Bacteriol. 185 (2003) 175-183
126. Lee D., Pervushin K., Bischof D., Braun M., and Thöny-Meyer L. Unusual heme-histidine bond in the active site of a chaperone. J. Am. Chem. Soc. 127 (2005) 3716-3717
127. Ren Q., and Thöny-Meyer L. Physical interaction of CcmC with heme and the heme chaperone CcmE during cytochrome c maturation. J. Biol. Chem. 276 (2001) 32591-32596
128. Schulz H., Fabianek R.A., Pellicioli E.C., Hennecke H., and Thöny-Meyer L. 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 (1999) 6462-6467
129. Cianciotto N.P., Cornelis P., and Baysse C. Impact of the bacterial type I cytochrome c maturation system on different biological processes. Mol. Microbiol. 56 (2005) 1408-1415
130. Liu C.E., Liu P.Q., and Ames G.F.L. Characterization of the adenosine triphosphatase activity of the periplasmic histidine permease, a traffic ATPase (ABC transporter). J. Biol. Chem. 272 (1997) 21883-21891
131. Christensen O., Harvat E.M., Thöny-Meyer L., Ferguson S.J., and Stevens J.M. Loss of ATP hydrolysis activity by CcmAB results in loss of c-type cytochrome synthesis and incomplete processing of CcmE. FEBS J. 274 (2007) 2322-2332
132. Cook G.M., and Poole R.K. Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association. Microbiology 146 Pt 2 (2000) 527-536
133. Daltrop O., Stevens J.M., Higham C.W., and Ferguson S.J. 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 (2002) 9703-9708
134. Metcalfe C.L., Daltrop O., Ferguson S.J., and Raven E.L. Tuning the formation of a covalent haem-protein link by selection of reductive or oxidative conditions as exemplified by ascorbate peroxidase. Biochem. J. 408 (2007) 355-361
135. Stevens J.M., Daltrop O., Allen J.W., and Ferguson S.J. C-type cytochrome formation: chemical and biological enigmas. Acc. Chem. Res. 37 (2004) 999-1007
136. Pittman M.S., Robinson H.C., and Poole R.K. A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J. Biol. Chem. 280 (2005) 32254-32261
137. Ahuja U., and Thöny-Meyer L. CcmD is involved in complex formation between CcmC and the heme chaperone CcmE during cytochrome c maturation. J. Biol. Chem. 280 (2005) 236-243
138. Richard-Fogal C.L., Frawley E.R., and Kranz R.G. Topology and function of CcmD in cytochrome c maturation. J. Bacteriol. 190 (2008) 3489-3493
139. Faivre-Nitschke S.E., Nazoa P., Gualberto J.M., Grienenberger J.M., and Bonnard G. Wheat mitochondria ccmB encodes the membrane domain of a putative ABC transporter involved in cytochrome c biogenesis. Biochim. Biophys. Acta 1519 (2001) 199-208
140. Raczynska K.D., Le Ret M., Rurek M., Bonnard G., Augustyniak H., and Gualberto J.M. Plant mitochondrial genes can be expressed from mRNAs lacking stop codons. FEBS Lett. 580 (2006) 5641-5646
141. Basile G., Di Bello C., and Taniuchi H. Formation of an iso-1-cytochrome c-like species containing a covalently bonded heme group from the apoprotein by a yeast cell-free system in the presence of hemin. J. Biol. Chem 255 (1980) 7181-7191
142. Tong J., and Margoliash E. Cytochrome c heme lyase activity of yeast mitochondria. J. Biol. Chem. 273 (1998) 25695-25702
143. Barker P.D., Ferrer J.C., Mylrajan M., Loehr T.M., Feng R., Konishi Y., Funk W.D., MacGillivray R.T., and Mauk A.G. Transmutation of a heme protein. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 6542-6546
144. Messens J., and Collet J.-F. Pathways of disulfide bond formation in Escherichia coli. Int. J. Biochem. Cell Biol. 38 (2006) 1050-1062
145. Mapller M., and Hederstedt L. Role of membrane-bound thiol and #x2013;disulfide oxidoreductases in endospore-forming bacteria. Antioxid. Redox Signal. 8 (2006) 823-833
146. Metheringham R., Griffiths L., Crooke H., Forsythe S., and Cole J. An essential role for DsbA in cytochrome c synthesis and formate-dependent nitrite reduction by Escherichia coli K-12. Arch. Microbiol. 164 (1995) 301-307
147. Metheringham R., Tyson K.L., Crooke H., Missiakas D., Raina S., and Cole J.A. 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 (1996) 95-102
148. Sambongi Y., and Ferguson S.J. 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 (1996) 265-268
149. Kranz R.G., Beckett C.S., and Goldman B.S. 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 (2002) 1-6
150. Allen J.W., Barker P.D., and Ferguson S.J. 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 (2003) 52075-52083
151. Deshmukh M., Turkarslan S., Astor D., Valkova-Valchanova M., and Daldal F. The dithiol:disulfide oxidoreductases DsbA and DsbB of Rhodobacter capsulatus are not directly involved in cytochrome c biogenesis, but their inactivation restores the cytochrome c biogenesis defect of CcdA-null mutants. J. Bacteriol. 185 (2003) 3361-3372
152. Feissner R.E., Beckett C.S., Loughman J.A., and Kranz R.G. Mutations in cytochrome assembly and periplasmic redox pathways in Bordetella pertussis. J. Bacteriol. 187 (2005) 3941-3949
153. Ritz D., and Beckwith J. Roles of thiol-redox pathways in bacteria. Annu. Rev. Microbiol. 55 (2001) 21-48
154. Monika E.M., Goldman B.S., Beckman D.L., and Kranz R.G. A thioreduction pathway tethered to the membrane for periplasmic cytochromes c biogenesis; in vitro and in vivo studies. J. Mol. Biol. 271 (1997) 679-692
155. Setterdahl A.T., Goldman B.S., Hirasawa M., Jacquot P., Smith A.J., Kranz R.G., and Knaff D.B. Oxidation-reduction properties of disulfide-containing proteins of the Rhodobacter capsulatus cytochrome c biogenesis system. Biochemistry 39 (2000) 10172-10176
156. Beckett C.S., Loughman J.A., Karberg K.A., Donato G.M., Goldman W.E., and Kranz R.G. Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol. Microbiol. 38 (2000) 465-481
157. Deshmukh M., Brasseur G., and Daldal F. Novel Rhodobacter capsulatus genes required for the biogenesis of various c-type cytochromes. Mol. Microbiol. 35 (2000) 123-138
158. Daltrop O., Allen J.W., Willis A.C., and Ferguson S.J. In vitro formation of a c-type cytochrome. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7872-7876
159. Daltrop O., and Ferguson S.J. Cytochrome c maturation. The in vitro reactions of horse heart apocytochrome c and Paracoccus dentrificans apocytochrome c550 with heme. J. Biol. Chem. 278 (2003) 4404-4409
160. Daltrop O., and Ferguson S.J. In vitro studies on thioether bond formation between Hydrogenobacter thermophilus apocytochrome c(552) with metalloprotoporphyrin derivatives. J. Biol. Chem. 279 (2004) 45347-45353
161. Fabianek R.A., Hofer T., and Thony-Meyer L. Characterization of the Escherichia coli CcmH protein reveals new insights into the redox pathway required for cytochrome c maturation. Arch. Microbiol. 171 (1999) 92-100
162. Reid E., Cole J., and Eaves D.J. The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly. Biochem. J. 355 (2001) 51-58
163. Rios-Velazquez C., Coller R., and Donohue T.J. Features of Rhodobacter sphaeroides CcmFH. J. Bacteriol. 185 (2003) 422-431
164. Di Matteo A., Gianni S., Schinina M.E., Giorgi A., Altieri F., Calosci N., Brunori M., and Travaglini-Allocatelli C. A strategic protein in cytochrome c maturation: three-dimensional structure of CcmH and binding to apocytochrome c. J. Biol. Chem. 282 (2007) 27012-27019
165. Fabianek R.A., Huber-Wunderlich M., Glockshuber R., Kunzler P., Hennecke H., and Thony-Meyer L. Characterization of the Bradyrhizobium japonicum CycY protein, a membrane-anchored periplasmic thioredoxin that may play a role as a reductant in the biogenesis of c-type cytochromes. J. Biol. Chem. 272 (1997) 4467-4473
166. Page M.D., and Ferguson S.J. Paracoccus denitrificans CcmG is a periplasmic protein-disulphide oxidoreductase required for c- and aa3-type cytochrome biogenesis; evidence for a reductase role in vivo. Mol. Microbiol. 24 (1997) 977-990
167. Fabianek R.A., Hennecke H., and Thöny-Meyer L. The active-site cysteines of the periplasmic thioredoxin-like protein CcmG of Escherichia coli are important but not essential for cytochrome c maturation in vivo. J. Bacteriol. 180 (1998) 1947-1950
168. Sanchez N.S., Pearce D.A., Cardillo T.S., Uribe S., and Sherman F. Requirements of Cyc2p and the porin, Por1p, for ionic stability and mitochondrial integrity in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 392 (2001) 326-332
169. Pearce D.A., Cardillo T.S., and Sherman F. Cyc2p is required for maintaining ionic stability and efficient cytochrome c import and mitochondrial function in Saccharomyces cerevisiae. FEBS Lett. 439 (1998) 307-311
170. Hell K. The Erv1-Mia40 disulfide relay system in the intermembrane space of mitochondria. Biochim. Biophys. Acta (2007)
171. Enosawa S., and Ohashi A. A simple and rapid assay for heme attachment to apocytochrome c. Anal. Biochem. 160 (1987) 211-216
172. Korb H., and Neupert W. Biogenesis of cytochrome c in Neurospora crassa. Synthesis of apocytochrome c, transfer to mitochondria and conversion to holocytochrome c. Eur. J. Biochem. 91 (1978) 609-620
173. Nicholson D.W., Hergersberg C., and Neupert W. Role of cytochrome c heme lyase in the import of cytochrome c into mitochondria. J. Biol. Chem. 263 (1988) 19034-19042
174. Nicholson D.W., Kohler H., and Neupert W. Import of cytochrome c into mitochondria. Cytochrome c heme lyase. Eur. J. Biochem. 164 (1987) 147-157
175. 1 heme lyase. Curr. Genet. 25 (1994) 291-298
176. Matner R.R., and Sherman F. Differential accumulation of two apo-iso-cytochromes c in processing mutants of yeast. J. Biol. Chem. 257 (1982) 9811-9821
177. 1 sorting pathway. J. Biol. Chem 265 (1990) 20210-20219
178. Stuart R.A., Nicholson D.W., and Neupert W. Early steps in mitochondrial protein import: receptor functions can be substituted by the membrane insertion activity of apocytochrome c. Cell 60 (1990) 31-43
179. Steiner H., Zollner A., Haid A., Neupert W., and Lill R. Biogenesis of mitochondrial heme lyases in yeast. Import and folding in the intermembrane space. J. Biol. Chem. 270 (1995) 22842-22849
180. Veloso D., Juillerat M., and Taniuchi H. Synthesis of a heme fragment of horse cytochrome c which forms a productive complex with a native apofragment. J. Biol. Chem. 259 (1984) 6067-6073
181. Ren Q., Ahuja U., and Thony-Meyer L. 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 (2002) 7657-7663
182. Eaves D.J., Grove J., Staudenmann W., James P., Poole R.K., White S.A., Griffiths L., and Cole J.A. Involvement of products of the nrfEFG genes in the covalent attachment of haem c to a novel cysteine-lysine motif in the cytochrome c552 nitrite reductase from Escherichia coli. Mol. Microbiol. 28 (1998) 205-216