Structural and functional characterization of CcmG from pseudomonas aeruginosa, a key component of the bacterial cytochrome c maturation apparatus

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 10, 2010, Pages 2213-2221

  Di Matteo, Adele ^a   Calosci, Nicoletta ^a   Gianni, Stefano ^a   Jemth, Per ^b   Brunori, Maurizio ^a   Travaglini Allocatelli, Carlo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Cytochrome c heme binding motif; Cytocrome c biogenesis; DTNB; pKa; Thiol disulfide oxidoreductases; Thioredoxin like protein

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C; DISULFIDE; PROTEIN CCMG; THIOREDOXIN; UNCLASSIFIED DRUG; HYBRID PROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; PERIPLASMIC PROTEIN; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE);

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME METABOLISM; IN VITRO STUDY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; X RAY CRYSTALLOGRAPHY; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME STABILITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN TERTIARY STRUCTURE; SOLUBILITY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYTOCHROMES C; ENZYME STABILITY; KINETICS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTANT PROTEINS; OXIDATION-REDUCTION; PERIPLASMIC PROTEINS; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; SOLUBILITY; THIOREDOXINS;

EID: 77955822694     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22733     Document Type: Article

References (32)

1. Steiner H, Kispal G, Zollner A, Haid A, Neupert W, Lill R. Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J Biol Chem 1996;271:32605-32611.
2. Ferguson SJ, Stevens JM, Allen JW Robertson IB. Cytochrome c assembly: a tale of ever increasing variation and mystery? Biochim Biophys Acta 2008;1777:980-984.
3. Hamel P, Corvest V, Giegá P, Bonnard G. Biochemical requirements for the maturation of mitochondrial c-type cytochromes. Biochim Biophys Acta 2009;1793:125-138.
4. Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER. Cytochrome C biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 2009;73:510-528.
5. Monika EM, Goldman BS, Beckman DL, Kranz RG. A thioreduction pathway tethered to the membrane for periplasmic cytochromes c biogenesis; in vitro and in vivo studies. J Mol Biol 1997;271:679-692.
6. Reid E, Cole J, Eaves DJ. The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly. Biochem J 2001;355:51-58.
7. Fabianek RA. Huber-Wunderlich M, Glockshuber R, Künzler P, Hennecke H, Thöny-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 1997;272:4467-4473.
8. Stirnimann CU, Rozhkova A, Grauschopf U, Grütter MG, Glockshuber R, Capitani G. Structural basis and kinetics of DsbD-dependent cytochrome c maturation. Structure 2005;13:985-993.
9. Edeling MA, Guddat LW, Fabianek RA, Thöny-Meyer L, Martin JL. Structure of CcmG/DsbE at 1.14 A resolution: high-fidelity reducing activity in an indiscriminately oxidizing environment. Structure 2002;10:973-979.
10. Ouyang N, Gao YG, Hu HY, Xia ZX. Crystal structures of E. coli CcmG and its mutants reveal key roles of the N-terminal beta-sheet and the fingerprint region. Proteins 2006;65:1021-1031.
11. Matteo A, Gianni S, Schininà ME, Giorgi A, Altieri F, Calosci N, Brunori M, Travaglini-Allocatelli C. A strategic protein in cytochrome c maturation: three-dimensional structure of CcmH and binding to apocytochrome c. J Biol Chem 2007;282:27012-27019.
12. Robertson IB, Stevens JM, Ferguson SJ. Dispensable residues in the active site of the cytochrome c biogenesis protein CcmH. FEBS Lett 2008;582:3067-3072.
13. Turkarslan S, Sanders C, Ekici S, Daldal F. Compensatory thioredox interactions between DsbA. Ccd A and Ccm G unveil the apocytochrome c holdase role of Ccm G during cytochrome c maturation. Mol Microbiol 2008;70:652-666.
14. Fabianek RA, Hofer T, Thöny-Meyer L. Characterization of the Escherichia coli CcmH protein reveals new insights into the redox pathway required for cytochrome c maturation. Arch Microbiol 1999;171:92-100.
15. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
16. Collaborative Computational Project N. 4. The CCP4 suite: programs for protein crystallography Acta Crystallogr D Biol Crystallogr 1994;50:760-763.
17. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Crystallogr 1997;30:1022-1025.
18. Murshudov GN, Vagin AA, Dodson and EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997;53:240-255.
19. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-2132.
20. Lamzin VS, Perrakis A, Wilson KS. The ARP/wARP suite for automated construction and refinement of protein models. In: Rossmann MG, Arnold E. editors. Int. Tables for crystallography. Vol. F: Crystallography of biological macromolecules. Dordrecht, The Netherland: Kluwer Academic Publisher; 2001. pp 720-722.
21. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PRO-CHECK-a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
22. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004;60:2256-2268.
23. Santoro MM, Bolen DW. Unfolding free energy changes determined by the linear extrapolation method. I. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 1988;27:8063-8074.
24. Nelson JW, Creighton TE. Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry 1994;33:5974-5983.
25. Fabianek RA, Hennecke H, Thöny-Meyer L. Periplasmic protein thiol:disulfide oxidoreductases of Escherichia coli. FEMS Microbiol Rev 2000;24:303-316.
26. Ren G, Stephan D, Xu Z, Zheng Y, Tang D, Harrison RS, Kurz M, Jarrot R, Shouldice SR, Hinker JL, Heras B, Bardwell JC. Properties of the thioredoxin fold superfamily are modulated by a single amino acid residue. J Biol Chem 2009;284:10150-10159.
27. Jackson SE, Fersht AR. Folding of chymotrypsin inhibitor 2. I. Evidence for a two-state transition. Biochemistry 1991;30:10428-10443.
28. Zander T, Phadke ND, Bardwell JC. Disulfide bond catalysts in Escherichia coli. Methods Enzymol 1998;290:59-74.
29. Kallis GB, Holmgren A. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli. J Biol Chem 1980;255:10261-10265.
30. Chivers PT, Raines RT. General acid/base catalysis in the active site of Escherichia coli thioredoxin. Biochemistry 1997;36:15810-15816.
31. Selzer T, Schreiber G. New insights into the mechanism of proteinprotein association. Proteins 2001;45:190-198.
32. Ahuja U, Rozhkova A, Glockshuber R, Thöny-Meyer L, Einsley O. Helix swapping leads to dimerization of the N-terminal domain of the c-type cytochrome maturation protein CcmH from Escherichia coli. FEBS Lett 2008;582:2779-2786.