Alteration of haem-attachment and signal-cleavage sites for Paracoccus denitrificans cytochrome C550 probes pathway of c-type cytochrome biogenesis in Escherichia coli

Molecular Microbiology

Volumn 19, Issue 6, 1996, Pages 1193-1204

  Sambongi, Yoshihiro ^a,b   Stoll, Raphael ^a,c   Ferguson, Stuart J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; PARACOCCUS DENITRIFICANS; SACCHAROMYCES CEREVISIAE;

CYTOCHROME C; HEME;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; MOLECULAR CLONING; NONHUMAN; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CYTOCHROME C GROUP; DNA PRIMERS; ESCHERICHIA COLI; GENE EXPRESSION; GENES, BACTERIAL; GENES, FUNGAL; HEME; MOLECULAR PROBES; MOLECULAR SEQUENCE DATA; MUTATION; PARACOCCUS DENITRIFICANS; PROTEIN SORTING SIGNALS; SACCHAROMYCES CEREVISIAE;

EID: 0029670437     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.1996.tb02465.x     Document Type: Article

References (42)

1. Beckman, D.L., and Kranz, R.G. (1993) Cytochrome c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxin-like protein. Proc Natl Acad Sci USA 90: 2179-2183.
2. Beckman, D.L., Trawick, D.R., and Kranz, R.G. (1992) Bacterial cytochrome c biogenesis. Genes Dev 6: 268-283.
3. 2 signal peptide is not necessary for export and heme attachment. J Bacteriol 176: 602-609.
4. 2 required for export, heme attachment, and function. J Bacteriol 173: 3958-3965.
5. Brickman, E., and Beckwith, J. (1975) Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and φ80 transducing phages. J Mol Biol 96: 307-316.
6. Crooke, H., and Cole, J.A. (1995) The biogenesis of c-type cytochromes in Escherichia coli requires a membrane-bound protein, DipZ, with a protein disulphide isomerase-like domain. Mol Microbiol 15:1139-1150.
7. Dalbey, R.E., and von Heijne, G. (1992) Signal peptidase in prokaryotes and eukaryotes - a new protease family. Trends Biochem Sci 17: 474-478.
8. 552 from Escherichia coli: not a hexahaem but a 50 kDa tetrahaem nitirite reductase. Mol Microbiol 9: 1255-1265.
9. Darwin, A., Tormay, P., Page, L., Griffiths, L., and Cole, J.A. (1993b) Identification of the formate dehydrogenase and genetic determinants of formate-dependent nitirite reduction by Escherichia coli K-12. J Gen Microbiol 139: 1829-1840.
10. De Sutter, K., Remaut, E., and Fiers, W. (1992) Disulphide bridge formation in the periplasm of Escherichia coli: β-lactamase::human IgG3 hinge fusions as a model system. Mol Microbiol 6: 2201-2208.
11. Derman, A.I., and Beckwith, J. (1991) Escherichia coli alkaline phosphatase fails to acquire disulphide bonds when retained in the cytoplasm. J Bacteriol 173: 7719-7722.
12. Drygas, M.E., Lambowitz, A.M., and Nargang, F.E. (1989) Cloning and analysis of the Neurospora crassa gene for cytochrome heme lyase. J Biol Chem 264: 17897-17906.
13. Dumont, M.E., Ernst, J.F., Hampsey, D.M., and Sherman, F. (1987) Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. EMBO J 6: 235-241.
14. 1 into the periplasmic space of Escherichia coli with the aid of the signal peptide of alkaline phosphatase. FEBS Lett 265: 71-74.
15. Goodhew, C.F., Brown, K.R., and Pettigrew, G.W. (1986) Haem staining in gels, a useful tool in the study of c-type cytochromes. Biochim Biophys Acta 852: 288-294.
16. Grove, J., Tanapongpipat, S., Thomas, G., Grifiths, L., Crooke, H., and Cole, J. (1996) Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm. Mol Microbiol 19: 467-481.
17. Iobbi-Nivol, C., Crooke, H., Griffiths, L., Grove, J., Hussain, H., Prommier, J., Mejean, V., and Cole, J.A. (1994) A reassessment of the range of c-type cytochromes synthesized by Escherichia coli K-12. FEMS Microbiol Lett 119: 89-94.
18. Izard, J.W., and Kendall, D.A. (1994) Signal peptides: exquisitely designed transport promoters. Mol Microbiol 13: 765-773.
19. Jansson, J.A.T. (1965) A direct spectrophotometric assay for penicillin β-lactamase (penicillinase) Biochim Biophys Acta 99: 171-172.
20. Mejean, V., Iobbi-Nivol, C., Lepelletier, M., Giordano, G., Chippaux, M., and Pascal, M.C. (1994) TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon. Mol Microbiol 11: 1169-1179.
21. Metheringham, R., Griffiths, L., Crooke, H., Forsythe, S., and Cole, J. (1995) An essential role for DsbA in cytochrome c synthesis and formate dependent-nitrite reduction by Escherichia coli K12. Arch Microbiol 164: 301-307.
22. Missiakis, D., Schwager, F., and Raina S. (1995) Identification and characterization of a new disulphide isomerase-like protein (DsbD) in Escherichia coli. EMBO J 14, 3415-3424.
23. Neu, H.C., and Heppel, L.A. (1965) The release of enzymes from Escherichia coli by osmotic shock and during the formation of sphaeroplasts. J Biol Chem 240: 3685-3692.
24. 1 are translocated to the periplasm of Paracoccus denitrificans in the absence of haem incorporation caused by either mutation or inhibition of haem synthesis. Mol Microbiol 4: 1181-1192.
25. 1. Mol Microbiol 15: 307-318.
26. Pettigrew, G.W., Leaver, J.L., Meyer, T.E., and Ryle, A.P. (1975) Purification, properties and amino acid sequence of atypical cytochrome c from two protozoa, Euglena gracilis and Crithidia oncopelti. Biochem J 147: 291-302.
27. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
28. Ramseier, T., Winteler, H.V., and Hennecke, H. (1991) Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem 266: 7793-7803.
29. Richterich, P., Lakey, N., Gryan, G., Haehn, L., Mintz, L., Robison, K., and Church, G.M. (1993) Centisome 49 region of E. coli K-12 BHB2600. Genbank database entry U00008.
30. Ritz, D., Bott, M., and Hennecke, H. (1993) Formation of several c-type cytochromes requires a novel membrane-anchored protein that faces the periplasm. Mol Microbiol 9: 729-740.
31. 552 does not. Implications for c-type cytochrome biogenesis. FEBS Lett 340: 65-70.
32. Sambongi, Y., and Ferguson, S.J. (1994b) 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.
33. 552. FEBS Lett 344: 207-210.
34. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloing: A Laboratory Manual. 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
35. Summers, R.G., and Knowles, J.R. (1989) Illicit secretion of a cytoplasmic protein into the periplasm of Escherichia coli requires a signal peptide plus a portion of the cognate secreted protein. Demarcation of the critical region of the mature protein. J Biol Chem 264: 20074-20081.
36. Tanaka, Y., Ashikari, T., Shibano, Y., Amachi, T., Yoshizumi, H., and Matsubara, H. (1988) Construction of a human cytochrome c gene and its functional expression in Saccharomyces cerevisiae. J Biochem 103: 956-961.
37. Tanaka, Y., Kubota, I., Amachi, T., Yoshizumi, H., and Matsubara, H. (1990) Site-directed mutated human cytochrome c which retains heme c via only one thioether bond. J Biochem 108: 7-8.
38. Thony-Meyer, L., Fischer, F., Kunzler, P., Ritz, D., and Hennecke, H. (1995) Escherichia coli genes required for cytochrome c maturation. J Bacteriol 177: 4321-4326.
39. Vargas, C., Wu, G., Davies, A.E., and Downie, J.A. (1994) Identification of a gene encoding a thioredoxin-like product necessary for cytochrome c biogenesis and symbiotic nitrogen fixation in Rhizobium leguminosarum. J Bacteriol 176: 4117-4123.
40. von Wachenfeldt, C., and Hederstedt, L. (1990) Bacillus subtilis holo-cytochrome c-550 can be synthesised in aerobic Escherichia coli. FEBS Lett 270: 147-151.
41. Windass, J.D., Worsey, M.J., Pioli, E.M., Pioli, D., Barth, P.T., Atherton, K.T., Dart, E.G., Byron, D., Powell, K., and Senior, P.J. (1980) Improved conversion of methanol to single-cell protein by Methylophilus methylotrophus. Nature 289: 396-401.
42. 1-heme lyase. Eur J Biochem 207: 1093-1100.