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Escherichia coli K-12 substr. MG1655 Protein: CcmEFGH holocytochrome c synthetase

Subunit composition of CcmEFGH holocytochrome c synthetase = [CcmE][CcmF][CcmG][CcmH]
         membrane anchored periplasmic heme chaperone CcmE = CcmE (summary available)
         cytochrome c-type biogenesis protein = CcmF (summary available)

Summary:
CcmA-H in E. coli make up a type 1 cytochrome c biogenesis system. In cytochrome c biogenesis, apocytochrome c is translocated across the cytoplasmic membrane into the oxidizing environment of the periplasm through the sec secretion system where it complexes with heme--also transported across the cytoplasmic membrane. An intramolecular disulfide bond in the apocyctochrome c must be reduced to the dithiol form in order for the covalent attachment of heme cofactor to occur. ccmE, ccmF, ccmG, and ccmH in Escherichia coli are members of an operon whose gene products (CcmA-H) have been shown to be cytoplasmic membrane proteins required for cytochrome c maturation. CcmE is the periplasmic heme chaperone that shuttles heme from the CcmABCDE protoheme IX ABC transporter to the CcmEFGH holocytochrome c synthetase. CcmF interacts with CcmE and CcmH in transferring heme from CcmE to apocytochromes c. CcmH maintains cytochromes c in the reduced dithiol forms so that attachment of heme can occur. After its own intramolecular disulfide bond is reduced by DsbD, CcmG probably acts by reducing the intramolecular disulfide of CcmH, which in turn reduces the apocytochrome c disulfide. The pathway for reduction of Ccm protein and apocytochrome c disulfides and the mechanism for attachment of heme to apocytochromes c remain unclear.

The structure of CcmE has been determined by NMR spectroscopy [Enggist02, Vogeli02, Hu05a]. Radiolabeling and spectroscopic analyses indicate that CcmE is a heme-binding protein, and site-directed mutagenesis showed that heme binds transiently to a conserved periplasmic histidine residue [Schulz98a]. The structure of the CcmE heme binding site has been studied [Harvat09]. CcmF has been shown through co-immunoprecipitation experiments to interact directly with CcmE and CcmH, but not apocytochrome c [Ren02]. Membrane topology predictions using experimentally determined C terminus locations indicate that CcmF has 15 transmembrane helices and the C-terminus is located in the cytoplasm [Rapp04]. CcmG is a cytoplasmic membrane-bound protein that faces the periplasm with its C-terminal, hydrophilic domain [Fabianek98]. The structures of CcmG and two of its mutants have been determined by X-ray crystallography to resolutions of 1.9 Å, 1.9 Å, 2.2 Å [Ouyang06], and 1.9 Å [Ouyang03]. The structure of CcmG in a mixed disulfide complex with DsbD has been determined to a resolution of 1.94 Å [Stirnimann05]. The crystal structure of a CcmG orthologue from Bradyrhizobium japonicum was determined at 1.14 Å resolution [Edeling02]. CcmG and CcmH have been identified as having the characteristic C-X-X-C motif of oxidoreductases and to function in the redox pathway of cytochrome c maturation [Fabianek98, Fabianek99]. Variations in this heme-binding motif and their effect on cytochrome c maturation have been studied [Allen05] [Allen08].

Purification and characterisation of the complexes of the Ccm pathway has helped elucidate the mechanisms of haem binding and trafficking [RichardFogal09]. Purified CcmF/H compex contains β-haem which is a stable component of the the CcmF protein. β-haem is bound to the CcmF/H complex with a stoichiometry of 1:1 and His261 of CcmF functions as the axial ligand. β-haem of CcmF is reduced by ubiquinol-1 and dimethylquinone [RichardFogal09]. The physiological role of CcmF may be to reduce the iron of holoCcmE (Fe3+ to Fe2+) before covalent bonding to apocytochromes c.

ccmA, ccmB, ccmC, ccmD, ccmE, ccmF, ccmG, and ccmH mutants are deficient in the ability to produce c-type cytochromes [ThonyMeyer95, Grove96, Grove96a, ThroneHolst97, Fabianek98, Tanapongpipat98, Schulz98a, Fabianek99, Reid01, Enggist03, Edeling04, Ahuja06]. In the absence of CcmF, CcmG, or CcmH, heme is not released from CcmE to apocytochrome c, and heme-bound CcmE accumulates [Schulz98a, Reid98, Ren02]. A paralogue of CcmF in E. coli, NrfE, has been shown to function in the ligation of heme to the heme-binding site of the pentaheme c-type cytochrome NrfA [Eaves98]. Deletion mutation studies suggest that CcmF and CcmH form part of a heme lyase complex required to transfer heme from CcmE to the C-X-X-C-H heme-binding domains of apocytochromes c [Grove96a], and that only the N-terminal domain of CcmH containing a conserved C-X-X-C redox motif was required for cytochrome-c maturation [Fabianek99]. CcmH mutants could be complemented by addition of 2-mercapto-ethanesulfonic acid suggesting CcmH maintains the heme-binding sites of apocytochromes c in reduced form for heme ligation [Fabianek99]. CcmG mutants are unable to reduce the disulfide bonds of cytochromes c for attachment of heme [Fabianek98, Reid98, Ahuja06], but were not significantly affected in general redox reactions in the periplasm [Reid01]. Purified CcmG mutants were used to determine the kinetics of disulfide exchange between CcmG and DsbD revealing electron transfer from DsbD to CcmG [Stirnimann05] rather than to CcmH or a CcmH-CcmG mixed disulfide as suggested by other experiments [Reid01]. Homologues of CcmG contain a conserved C-X-X-C redox-active motif [Fabianek97] which is important for cytochrome c maturation [Fabianek98]. The C-X-X-C motif is characteristic of thioredoxin (TRX)-like proteins which are capable of reverting disulfide bonds to dithiols [Edeling04]. The redox activity of CcmG differs from that of TRX in that it is highly specific for cytochrome c maturation.

Expression of ccmABCDEFGH occurs from the napF promoter or from the ccmA promoter, and there is also a weak promoter within ccmD that enables transcription of downstream genes [Grove96, Tanapongpipat98].

Reviews: [ThonyMeyer97, Kranz98, Fabianek00, ThonyMeyer00, Stevens05, SkorkoGlonekv05, Stevens11]

Citations: [Stevens06, Harvat05, Li01, IobbiNivol94, Mavridou12]

Gene-Reaction Schematic: ?

GO Terms:

Biological Process: GO:0017003 - protein-heme linkage Inferred from experiment [Schulz98a]
Molecular Function: GO:0020037 - heme binding Inferred from experiment [RichardFogal09]


Subunit of CcmEFGH holocytochrome c synthetase: membrane anchored periplasmic heme chaperone CcmE

Synonyms: YejS

Gene: ccmE Accession Numbers: EG12055 (EcoCyc), b2197, ECK2189

Locations: cytosol, inner membrane, periplasmic space

Sequence Length: 159 AAs

Molecular Weight: 17.698 kD (from nucleotide sequence)

Molecular Weight: 18.0 kD (experimental) [Schulz98a]

GO Terms:

Biological Process: GO:0017003 - protein-heme linkage Inferred from experiment Inferred by computational analysis [GOA06, GOA01a, Schulz98a]
GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11a, GOA01a]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [RichardFogal09, Ahuja06, Ahuja05, Ren02]
GO:0020037 - heme binding Inferred from experiment [Schulz98a]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11a]
Cellular Component: GO:0031237 - intrinsic component of periplasmic side of plasma membrane Inferred from experiment [Schulz98a]
GO:0005829 - cytosol Inferred by computational analysis [DiazMejia09]
GO:0005886 - plasma membrane Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, GOA06, GOA01a]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11a]
GO:0030288 - outer membrane-bounded periplasmic space

MultiFun Terms: information transfer protein related chaperoning, repair (refolding)
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes

Unification Links: EcoliWiki:b2197 , Mint:MINT-1503318 , ModBase:P69490 , PR:PRO_000022261 , Pride:P69490 , Protein Model Portal:P69490 , RefSeq:NP_416701 , SMR:P69490 , String:511145.b2197 , UniProt:P69490

Relationship Links: InterPro:IN-FAMILY:IPR004329 , InterPro:IN-FAMILY:IPR012340 , PDB:Structure:1SR3 , Pfam:IN-FAMILY:PF03100

Summary:
CcmE is the periplasmic heme chaperone responsible for shuttling heme from the CcmABCDE protoheme IX ABC transport complex to the CcmEFGH holocytochrome c synthetase for attachment to c-type cytochromes.

Essentiality data for ccmE knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 1]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 2]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 1]

Subunit of CcmEFGH holocytochrome c synthetase: cytochrome c-type biogenesis protein

Synonyms: YejR, CcmF

Gene: ccmF Accession Numbers: EG12054 (EcoCyc), b2196, ECK2188

Locations: inner membrane

Sequence Length: 647 AAs

Molecular Weight: 71.389 kD (from nucleotide sequence)

GO Terms:

Biological Process: GO:0015886 - heme transport Inferred by computational analysis [GOA01a]
GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11a, GOA01a]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [RichardFogal09, Ren02]
GO:0015232 - heme transporter activity Inferred by computational analysis [GOA01a]
GO:0020037 - heme binding Inferred by computational analysis [GOA01a]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, DiazMejia09, Daley05, Rapp04]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a, GOA01a]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11a]

MultiFun Terms: cell structure membrane
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes

Unification Links: DIP:DIP-9256N , EcoliWiki:b2196 , EcoO157Cyc:CCMF-MONOMER , Mint:MINT-225079 , PR:PRO_000022262 , Protein Model Portal:P33927 , RefSeq:NP_416700 , String:511145.b2196 , UniProt:P33927

Relationship Links: InterPro:IN-FAMILY:IPR002541 , InterPro:IN-FAMILY:IPR003567 , InterPro:IN-FAMILY:IPR003568 , Pfam:IN-FAMILY:PF01578 , Prints:IN-FAMILY:PR01410 , Prints:IN-FAMILY:PR01411

Summary:
CcmF is a membrane protein component of the CcmEFGH holocytochrome c synthetase.

Essentiality data for ccmF knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 3]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 1]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 2]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 1]

Subunit of CcmEFGH holocytochrome c synthetase: CcmG

Synonyms: YejQ, thioredoxin-like protein, cytochrome c biogenesis, DsbE

Gene: ccmG Accession Numbers: EG12053 (EcoCyc), b2195, ECK2187

Locations: inner membrane, periplasmic space

Sequence Length: 185 AAs

Molecular Weight: 20.809 kD (from nucleotide sequence)

GO Terms:

Biological Process: GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11a, GOA01a]
GO:0045454 - cell redox homeostasis Inferred by computational analysis [GOA01a]
GO:0055114 - oxidation-reduction process Inferred by computational analysis [GOA01a]
Molecular Function: GO:0015036 - disulfide oxidoreductase activity Inferred by computational analysis [GOA01a]
GO:0016491 - oxidoreductase activity Inferred by computational analysis [GOA01a]
Cellular Component: GO:0005886 - plasma membrane Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, Fabianek98]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11a]
GO:0030288 - outer membrane-bounded periplasmic space Inferred by computational analysis [GOA01a, DiazMejia09, Fabianek98]

MultiFun Terms: cell structure membrane
information transfer protein related chaperoning, repair (refolding)
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes

Unification Links: DIP:DIP-48446N , EcoliWiki:b2195 , ModBase:P0AA86 , PR:PRO_000022483 , Protein Model Portal:P0AA86 , RefSeq:NP_416699 , SMR:P0AA86 , String:511145.b2195 , UniProt:P0AA86

Relationship Links: InterPro:IN-FAMILY:IPR004799 , InterPro:IN-FAMILY:IPR012336 , InterPro:IN-FAMILY:IPR013740 , InterPro:IN-FAMILY:IPR017937 , PDB:Structure:1Z5Y , PDB:Structure:2B1K , PDB:Structure:2B1L , PDB:Structure:2G0F , PDB:Structure:3K8N , Pfam:IN-FAMILY:PF08534 , Prosite:IN-FAMILY:PS00194 , Prosite:IN-FAMILY:PS51352

Summary:
CcmG is a membrane protein component of the CcmEFGH holocytochrome c synthetase.

Essentiality data for ccmG knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 3]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 1]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 2]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 1]

Subunit of CcmEFGH holocytochrome c synthetase: CcmH

Synonyms: YejP, cytochrome c biogenesis protein CcmH

Gene: ccmH Accession Numbers: EG12052 (EcoCyc), b2194, ECK2186

Locations: inner membrane

Sequence Length: 350 AAs

Molecular Weight: 39.089 kD (from nucleotide sequence)

GO Terms:

Biological Process: GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11a]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [RichardFogal09, Ren02]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11a]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, DiazMejia09, Daley05]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11a]

MultiFun Terms: cell structure membrane
information transfer protein related chaperoning, repair (refolding)
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes

Unification Links: DIP:DIP-48146N , EcoliWiki:b2194 , Mint:MINT-225097 , ModBase:P0ABM9 , PR:PRO_000022263 , Protein Model Portal:P0ABM9 , RefSeq:NP_416698 , SMR:P0ABM9 , String:511145.b2194 , UniProt:P0ABM9

Relationship Links: InterPro:IN-FAMILY:IPR005616 , InterPro:IN-FAMILY:IPR011990 , InterPro:IN-FAMILY:IPR013026 , InterPro:IN-FAMILY:IPR019734 , Pfam:IN-FAMILY:PF03918 , Prosite:IN-FAMILY:PS50005 , Prosite:IN-FAMILY:PS50293

Summary:
CcmH is a membrane protein component of the CcmEFGH holocytochrome c synthetase.

The crystal structure of this subunit has been determined to 1.65 Å resolution [Ahuja08].

Essentiality data for ccmH knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 3]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 1]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 2]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 1]

References

Ahuja05: Ahuja U, Thony-Meyer L (2005). "CcmD is involved in complex formation between CcmC and the heme chaperone CcmE during cytochrome c maturation." J Biol Chem 280(1);236-43. PMID: 15513913

Ahuja06: Ahuja U, Thony-Meyer L (2006). "The membrane anchors of the heme chaperone CcmE and the periplasmic thioredoxin CcmG are functionally important." FEBS Lett 580(1);216-22. PMID: 16364305

Ahuja08: Ahuja U, Rozhkova A, Glockshuber R, Thony-Meyer L, Einsle O (2008). "Helix swapping leads to dimerization of the N-terminal domain of the c-type cytochrome maturation protein CcmH from Escherichia coli." FEBS Lett 582(18);2779-86. PMID: 18625227

Allen05: Allen JW, Leach N, Ferguson SJ (2005). "The histidine of the c-type cytochrome CXXCH haem-binding motif is essential for haem attachment by the Escherichia coli cytochrome c maturation (Ccm) apparatus." Biochem J 389(Pt 2);587-92. PMID: 15801911

Allen08: Allen JW, Sawyer EB, Ginger M, Barker PD, Ferguson SJ (2008). "Variant c-type cytochromes as probes of the substrate specificity of the E. coli cytochrome c maturation (Ccm) apparatus." Biochem J. PMID: 19090787

Baba06: Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006). "Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection." Mol Syst Biol 2;2006.0008. PMID: 16738554

Daley05: Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G (2005). "Global topology analysis of the Escherichia coli inner membrane proteome." Science 308(5726);1321-3. PMID: 15919996

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Edeling02: Edeling MA, Guddat LW, Fabianek RA, Thony-Meyer L, Martin JL (2002). "Structure of CcmG/DsbE at 1.14 A resolution: high-fidelity reducing activity in an indiscriminately oxidizing environment." Structure (Camb) 10(7);973-9. PMID: 12121652

Edeling04: Edeling MA, Ahuja U, Heras B, Thony-Meyer L, Martin JL (2004). "The acidic nature of the CcmG redox-active center is important for cytochrome c maturation in Escherichia coli." J Bacteriol 186(12);4030-3. PMID: 15175318

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Enggist03: Enggist E, Schneider MJ, Schulz H, Thony-Meyer L (2003). "Biochemical and mutational characterization of the heme chaperone CcmE reveals a heme binding site." J Bacteriol 185(1);175-83. PMID: 12486054

Fabianek00: Fabianek RA, Hennecke H, Thony-Meyer L (2000). "Periplasmic protein thiol:disulfide oxidoreductases of Escherichia coli." FEMS Microbiol Rev 2000;24(3);303-16. PMID: 10841975

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Gerdes03: Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD, Somera AL, Kyrpides NC, Anderson I, Gelfand MS, Bhattacharya A, Kapatral V, D'Souza M, Baev MV, Grechkin Y, Mseeh F, Fonstein MY, Overbeek R, Barabasi AL, Oltvai ZN, Osterman AL (2003). "Experimental determination and system level analysis of essential genes in Escherichia coli MG1655." J Bacteriol 185(19);5673-84. PMID: 13129938

GOA01a: GOA, DDB, FB, MGI, ZFIN (2001). "Gene Ontology annotation through association of InterPro records with GO terms."

GOA06: GOA, SIB (2006). "Electronic Gene Ontology annotations created by transferring manual GO annotations between orthologous microbial proteins."

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Li01: Li Q, Hu HY, Wang WQ, Xu GJ (2001). "Structural and redox properties of the leaderless DsbE (CcmG) protein: both active-site cysteines of the reduced form are involved in its function in the Escherichia coli periplasm." Biol Chem 382(12);1679-86. PMID: 11843181

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Ouyang06: Ouyang N, Gao YG, Hu HY, Xia ZX (2006). "Crystal structures of E. coli CcmG and its mutants reveal key roles of the N-terminal beta-sheet and the fingerprint region." Proteins 65(4);1021-31. PMID: 17019698

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Ren02: 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(10);7657-63. PMID: 11744735

RichardFogal09: Richard-Fogal CL, Frawley ER, Bonner ER, Zhu H, San Francisco B, Kranz RG (2009). "A conserved haem redox and trafficking pathway for cofactor attachment." EMBO J 28(16);2349-59. PMID: 19629033

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SkorkoGlonekv05: Skorko-Glonekv J, Sobiecka A (2005). "[Periplasmatic disulfide oxidoreductases from bacterium Escherichia coli--their structure and function]." Postepy Biochem 51(4);459-67. PMID: 16676581

Stevens05: Stevens JM, Uchida T, Daltrop O, Ferguson SJ (2005). "Covalent cofactor attachment to proteins: cytochrome c biogenesis." Biochem Soc Trans 33(Pt 4);792-5. PMID: 16042600

Stevens06: Stevens JM, Uchida T, Daltrop O, Kitagawa T, Ferguson SJ (2006). "Dynamic ligation properties of the Escherichia coli heme chaperone CcmE to non-covalently bound heme." J Biol Chem 281(10);6144-51. PMID: 16373344

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Stirnimann05: Stirnimann CU, Rozhkova A, Grauschopf U, Grutter MG, Glockshuber R, Capitani G (2005). "Structural basis and kinetics of DsbD-dependent cytochrome c maturation." Structure 13(7);985-93. PMID: 16004871

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Please cite the following article in publications resulting from the use of EcoCyc: Nucleic Acids Research 41:D605-12 2013
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