Compensatory thio-redox interactions between DsbA, CcdA and CcmG unveil the apocytochrome c holdase role of CcmG during cytochrome c maturation

Molecular Microbiology

Volumn 70, Issue 3, 2008, Pages 652-666

  Turkarslan, Serdar ^a   Sanders, Carsten ^a   Ekici, Seda ^a   Daldal, Fevzi ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C;

ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; IN VITRO STUDY; MATURATION; NONHUMAN; PRIORITY JOURNAL; RHODOBACTER CAPSULATUS;

BACTERIAL PROTEINS; CYTOCHROMES C; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; OXIDATION-REDUCTION; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); PROTEIN DISULFIDE-ISOMERASES; RHODOBACTER CAPSULATUS;

RHODOBACTER CAPSULATUS;

EID: 53849121947     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06441.x     Document Type: Article

References (55)

1. Allen, J.W., Daltrop, O., Stevens, J.M. Ferguson, S.J. (2003a) C-type cytochromes: diverse structures and biogenesis systems pose evolutionary problems. Philos Trans R Soc Lond B Biol Sci 358 : 255 266.
2. Allen, J.W., Barker, P.D. Ferguson, S.J. (2003b) 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.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
4. Barker, P.D. Ferguson, S.J. (1999) Still a puzzle: why is haem covalently attached in c-type cytochromes? Structure 7 : 281 290.
5. Beckman, D.L. Kranz, R.G. (1993) Cytochromes c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxin-like protein. Proc Natl Acad Sci USA 90 : 2179 2183.
6. Beckman, D.L., Trawick, D.R. Kranz, R.G. (1992) Bacterial cytochromes c biogenesis. Genes Dev 6 : 268 283.
7. Benning, C. Somerville, C.R. (1992) Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J Bacteriol 174 : 2352 2360.
8. Colbert, C.L., Wu, Q., Erbel, P.J., Gardner, K.H. Deisenhofer, J. (2006) Mechanism of substrate specificity in Bacillus subtilis ResA, a thioredoxin-like protein involved in cytochrome c maturation. Proc Natl Acad Sci USA 103 : 4410 4415.
9. Crow, A., Acheson, R.M., Le Brun, N.E. Oubrie, A. (2004) Structural basis of Redox-coupled protein substrate selection by the cytochrome c biosynthesis protein ResA. J Biol Chem 279 : 23654 23660.
10. Daldal, F., Cheng, S., Applebaum, J., Davidson, E. Prince, R.C. (1986) Cytochrome c(2) is not essential for photosynthetic growth of Rhodopseudomonas capsulata. Proc Natl Acad Sci USA 83 : 2012 2016.
11. Daltrop, O., Allen, J.W., Willis, A.C. Ferguson, S.J. (2002) In vitro formation of a c-type cytochrome. Proc Natl Acad Sci USA 99 : 7872 7876.
12. Davidson, E. Daldal, F. (1987) Primary structure of the bc1 complex of Rhodopseudomonas capsulata. Nucleotide sequence of the pet operon encoding the Rieske cytochrome b, and cytochrome c1 apoproteins. J Mol Biol 195 : 13 24.
13. Deshmukh, M., Brasseur, G. Daldal, F. (2000) Novel Rhodobacter capsulatus genes required for the biogenesis of various c-type cytochromes. Mol Microbiol 35 : 123 138.
14. Deshmukh, M., May, M., Zhang, Y., Gabbert, K.K., Karberg, K.A., Kranz, R.G. Daldal, F. (2002) Overexpression of ccl1-2 can bypass the need for the putative apocytochrome chaperone CycH during the biogenesis of c-type cytochromes. Mol Microbiol 46 : 1069 1080.
15. Deshmukh, M., Turkarslan, S., Astor, D., Valkova-Valchanova, M. Daldal, F. (2003) 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 : 3361 3372.
16. Di Matteo, A., Gianni, S., Schinina, M.E., Giorgi, A., Altieri, F., Calosci, N., et al. (2007) A strategic protein in cytochrome c maturation: three-dimensional structure of CcmH and binding to apocytochrome c. J Biol Chem 282 : 27012 27019.
17. Ditta, G., Schmidhauser, T., Yakobson, E., Lu, P., Liang, X.W., Finlay, D.R., et al. (1985) Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13 : 149 153.
18. Edeling, M.A., Guddat, L.W., Fabianek, R.A., Thony-Meyer, L. Martin, J.L. (2002) Structure of CcmG/DsbE at 1.14 A resolution: high-fidelity reducing activity in an indiscriminately oxidizing environment. Structure 10 : 973 979.
19. Edeling, M.A., Ahuja, U., Heras, B., Thony-Meyer, L. Martin, J.L. (2004) The acidic nature of the CcmG redox-active center is important for cytochrome c maturation in Escherichia coli. J Bacteriol 186 : 4030 4033.
20. 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.
21. Fabianek, R.A., Hennecke, H. Thony-Meyer, L. (1998) 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 : 1947 1950.
22. Fabianek, R.A., Hofer, T. Thony-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.
23. Gao, T. O'Brian, M.R. (2007) Control of DegP-dependent degradation of c-type cytochromes by heme and the cytochrome c maturation system in Escherichia coli. J Bacteriol 189 : 6253 6259.
24. Georgiou, C.D., Fang, H. Gennis, R.B. (1987) Identification of the cydC locus required for expression of the functional form of the cytochrome d terminal oxidase complex in Escherichia coli. J Bacteriol 169 : 2107 2112.
25. Gray, K.A., Grooms, M., Myllykallio, H., Moomaw, C., Slaughter, C. Daldal, F. (1994) Rhodobacter capsulatus contains a novel cb-type cytochrome c oxidase without a CuA center. Biochemistry 33 : 3120 3127.
26. Katzen, F. Beckwith, J. (2000) Transmembrane electron transfer by the membrane protein DsbD occurs via a disulfide bond cascade. Cell 103 : 769 779.
27. Katzen, F., Deshmukh, M., Daldal, F. Beckwith, J. (2002) Evolutionary domain fusion expanded the substrate specificity of the transmembrane electron transporter DsbD. EMBO J 21 : 3960 3969.
28. Keen, N.T., Tamaki, S., Kobayashi, D. Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70 : 191 197.
29. Koch, H.G., Hwang, O. Daldal, F. (1998) Isolation and characterization of Rhodobacter capsulatus mutants affected in cytochrome cbb3 oxidase activity. J Bacteriol 180 : 969 978.
30. Kojima, N., Yamanaka, M., Ichiki, S. Sambongi, Y. (2005) Unexpected elevated production of Aquifex aeolicus cytochrome c555 in Escherichia coli cells lacking disulfide oxidoreductases. Biosci Biotechnol Biochem 69 : 1418 1421.
31. Kranz, R., Lill, R., Goldman, B., Bonnard, G. Merchant, S. (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol Microbiol 29 : 383 396.
32. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 : 680 685.
33. Lowry, O.H., Rosebrough, N.J., Farr, A.L. Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193 : 265 275.
34. 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.
35. Monika, E.M., Goldman, B.S., Beckman, D.L. Kranz, R.G. (1997) A thioreduction pathway tethered to the membrane for periplasmic cytochromes c biogenesis; in vitro and in vivo studies. J Mol Biol 271 : 679 692.
36. Onder, O., Turkarslan, S., Sun, D. Daldal, F. (2008) Overproduction or absence of the periplasmic protease DegP severely compromises bacterial growth in the absence of the dithiol: disulfide oxidoreductase DsbA. Mol Cell Proteomics 7 : 875 890.
37. Pittman, M.S., Robinson, H.C. Poole, R.K. (2005) A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J Biol Chem 280 : 32254 32261.
38. 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.
39. Prentki, P. Krisch, H.M. (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29 : 303 313.
40. Ren, Q., Ahuja, U. Thony-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.
41. Robertson, I.B., Stevens, J.M. Ferguson, S.J. (2008) Dispensable residues in the active site of the cytochrome c biogenesis protein CcmH. FEBS Lett 582 : 3067 3072.
42. Sambrook, J. Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
43. Sanders, C., Wethkamp, N. Lill, H. (2001) Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol Microbiol 41 : 241 246.
44. Sanders, C., Deshmukh, M., Astor, D., Kranz, R.G. Daldal, F. (2005a) Overproduction of CcmG and CcmFH (Rc) fully suppresses the c-type cytochrome biogenesis defect of Rhodobacter capsulatus CcmI-null mutants. J Bacteriol 187 : 4245 4256.
45. Sanders, C., Turkarslan, S. Daldal, F. (2005b) Periplasmic oxidative folding and cytochrome c maturation: a mechanistic view of stereo-selective heme attachment. In Photosynthesis: Fundamental Aspects to Global Perspectives. Van der Est, A. Bruce, D. (eds Lawrence, KS : Allen Press, pp. 421 424.
46. Sanders, C., Boulay, C. Daldal, F. (2007) Membrane-spanning and periplasmic segments of CcmI have distinct functions during cytochrome c biogenesis in Rhodobacter capsulatus. J Bacteriol 189 : 789 800.
47. Sanders, C., Turkarslan, S., Lee, D.-W., Onder, O., Kranz, R.G. Daldal, F. (2008) The cytochrome c maturation components CcmF, CcmH and CcmI form a membrane-integral multisubunit heme ligation complex. J Biol Chem (in press). [Epub ahead of print], PMID 18753134.
48. Schagger, H. von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166 : 368 379.
49. Scolnik, P.A., Walker, M.A. Marrs, B.L. (1980) Biosynthesis of carotenoids derived from neurosporene in Rhodopseudomonas capsulata. J Biol Chem 255 : 2427 2432.
50. Sistrom, W.R. (1960) A requirement for sodium in the growth of Rhodopseudomonas spheroides. J Gen Microbiol 22 : 778 785.
51. Thomas, P.E., Ryan, D. Levin, W. (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75 : 168 176.
52. Thony-Meyer, L. (2000) Haem-polypeptide interactions during cytochrome c maturation. Biochim Biophys Acta 1459 : 316 324.
53. Thony-Meyer, L. (2002) Cytochrome c maturation: a complex pathway for a simple task? Biochem Soc Trans 30 : 633 638.
54. Yen, H.C., Hu, N.T. Marrs, B.L. (1979) Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. J Mol Biol 131 : 157 168.
55. Zannoni, D. Daldal, F. (1993) The role of c-type cytochromes in catalyzing oxidative and photosynthetic electron transport in the dual functional plasmamembrane of facultative phototrophs. Arch Microbiol 160 : 413 423.