Essential histidine pairs indicate conserved haem binding in epsilonproteobacterial cytochrome c haem lyases

Microbiology

Volumn 156, Issue 12, 2010, Pages 3773-3781

  Kern, Melanie ^a   Scheithauer, Juliane ^a   Kranz, Robert G ^b   Simon, Jörg ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL PROTEIN; CYTOCHROME; CYTOCHROME C; CYTOCHROME C HEME LYASE; CYTOCHROME C MCCA; HEME; HISTIDINE; IMIDAZOLE; PROTEIN CCSA1; PROTEIN CCSA2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRFA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BINDING SITE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME SYNTHESIS; EPSILONPROTEOBACTERIA; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WOLINELLA SUCCINOGENES;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BINDING SITES; CONSERVED SEQUENCE; HEME; HISTIDINE; LYASES; WOLINELLA;

BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; ESCHERICHIA COLI; WOLINELLA SUCCINOGENES;

EID: 78650036448     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.042838-0     Document Type: Article

References (33)

1. Ahuja, U., Kjelgaard, P., Schulz, B. L., Thöny-Meyer, L. & Hederstedt, L. (2009). Haem-delivery proteins in cytochrome c maturation system II. Mol Microbiol 73, 1058-1071.
2. Barrick, D. (1994). Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93→Gly. Biochemistry 33, 6546-6554.
3. Bode, C., Goebell, H. & Stähler, E. (1968). Zur Eliminierung von Trübungsfehlern bei der Eiweißbestimmung mit der Biuretmethode. Z Klin Chem Klin Biochem 6, 418-422.
4. Dreyfuss, B. W., Hamel, P. P., Nakamoto, S. S. & Merchant, S. (2003). Functional analysis of a divergent system II protein, Ccs1, involved in c-type cytochrome biogenesis. J Biol Chem 278, 2604-2613.
5. Feissner, R. E., Richard-Fogal, C. L., Frawley, E. R., Loughman, J. A., Earley, K. W. & Kranz, R. G. (2006). Recombinant cytochromes c biogenesis systems I and II and analysis of haem delivery pathways in Escherichia coli. Mol Microbiol 60, 563-577.
6. Ferguson, S. J., Stevens, J. M., Allen, J. W. A. & Robertson, I. B. (2008). Cytochrome c assembly: a tale of ever increasing variation and mystery? Biochim Biophys Acta 1777, 980-984.
7. Frawley, E. R. & Kranz, R. G. (2009). CcsBA is a cytochrome c synthetase that also functions in heme transport. Proc Natl Acad Sci U S A 106, 10201-10206.
8. Goddard, A. D., Stevens, J. M., Rondelet, A., Nomerotskaia, E., Allen, J. W. A. & Ferguson, S. J. (2010). Comparing the substrate specificities of cytochrome c biogenesis systems I and II: bioenergetics. FEBS J 277, 726-737.
9. Hamel, P. P., Dreyfuss, B. W., Xie, Z., Gabilly, S. T. & Merchant, S. (2003). Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J Biol Chem 278, 2593-2603.
10. Hartshorne, S., Richardson, D. J. & Simon, J. (2006). Multiple haem lyase genes indicate substrate specificity in cytochrome c biogenesis. Biochem Soc Trans 34, 146-149.
11. Hartshorne, R. S., Kern, M., Meyer, B., Clarke, T. A., Karas, M., Richardson, D. J. & Simon, J. (2007). A dedicated haem lyase is required for the maturation of a novel bacterial cytochrome c with unconventional covalent haem binding. Mol Microbiol 64, 1049-1060.
12. Kern, M. & Simon, J. (2008). Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogenes nitrate respiration. Mol Microbiol 69, 1137-1152.
13. Kern, M. & Simon, J. (2009a). Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta 1787, 646-656.
14. Kern, M. & Simon, J. (2009b). Periplasmic nitrate reduction in Wolinella succinogenes: cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment. Microbiology 155, 2784-2794.
15. Kern, M., Mager, A. M. & Simon, J. (2007). Role of individual nap gene cluster products in NapC-independent nitrate respiration of Wolinella succinogenes. Microbiology 153, 3739-3747. (Pubitemid 350168252)
16. Kern, M., Eisel, F., Scheithauer, J., Kranz, R. G. & Simon, J. (2010). Substrate specificity of three cytochrome c haem lyase isoenzymes from Wolinella succinogenes: unconventional haem c binding motifs are not sufficient for haem c attachment by NrfI and CcsA1. Mol Microbiol 75, 122-137.
17. Kranz, R. G., Richard-Fogal, C., Taylor, J.-S. & 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.
18. Kröger, A., Geisler, V. & Duchêne, A. (1994). Isolation of Wolinella succinogenes hydrogenase, chromatofocusing. In A Practical Guide to Membrane Protein Purification, pp. 141-147. Edited by G. von Jagow & H. Schägger. London: Academic Press.
19. Merchant, S. S. (2009). His protects heme as it crosses the membrane. Proc Natl Acad Sci U S A 106, 10069-10070.
20. 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. (Pubitemid 34597268)
21. 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.
22. Richard-Fogal, C. L. & Kranz, R. G. (2010). The CcmC : heme : CcmE complex in heme trafficking and cytochrome c biosynthesis. J Mol Biol 401, 350-362.
23. Richard-Fogal, C. L., Frawley, E. R., Feissner, R. E. & Kranz, R. G. (2007). Heme concentration dependence and metalloprotein inhibition of the system I and II cytochrome c assembly pathways. J Bacteriol 189, 455-463.
24. Richard-Fogal, C. L., Bonner, E. R., Zhu, H., San Francisco, B. & Kranz, R. G. (2009). A conserved haem redox and trafficking pathway for cofactor attachment. EMBO J 28, 2349-2359.
25. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
26. Sanders, C., Turkarslan, S., Lee, D.-W. & Daldal, F. (2010). Cytochrome c biogenesis: the Ccm system. Trends Microbiol 18, 266-274.
27. Schulz, H., Pellicioli, E. C. & Thöny-Meyer, L. (2000). New insights into the role of CcmC, CcmD and CcmE in the haem delivery pathway during cytochrome c maturation by a complete mutational analysis of the conserved tryptophan-rich motif of CcmC. Mol Microbiol 37, 1379-1388.
28. Simon, J. (2002). Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26, 285-309.
29. Simon, J. & Kern, M. (2008). Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial anaerobic respiration. Biochem Soc Trans 36, 1011-1016.
30. Simon, J., Gross, R., Ringel, M., Schmidt, E. & Kröger, A. (1998). Deletion and site-directed mutagenesis of the Wolinella succinogenes fumarate reductase operon. Eur J Biochem 251, 418-426. (Pubitemid 28080942)
31. Simon, J., Gross, R., Einsle, O., Kroneck, P. M. H., Kröger, 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.
32. Simon, J., Pisa, R., Stein, T., Eichler, R., Klimmek, O. & Gross, R. (2001). The tetraheme cytochrome c NrfH is required to anchor the cytochrome c nitrite reductase (NrfA) in the membrane of Wolinella succinogenes. Eur J Biochem 268, 5776-5782.
33. Simon, J., van Spanning, R. J. M. & Richardson, D. J. (2008). The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim Biophys Acta 1777, 1480-1490.