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Escherichia coli K-12 substr. MG1655 Polypeptide: membrane anchored periplasmic heme chaperone CcmE



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

Synonyms: yejS

Regulation Summary Diagram: ?

Component of:
CcmEFGH holocytochrome c synthetase (extended summary available)
CcmCDE protoheme IX reservoir complex (summary available)
protoheme IX ABC transporter (extended summary available)

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.

Gene Citations: [Darwin95, Grove96]

Locations: cytosol, inner membrane, periplasmic space

Map Position: [2,292,923 <- 2,293,402] (49.42 centisomes)
Length: 480 bp / 159 aa

Molecular Weight of Polypeptide: 17.698 kD (from nucleotide sequence), 18.0 kD (experimental) [Schulz98 ]

Unification Links: ASAP:ABE-0007271 , CGSC:36587 , EchoBASE:EB1986 , EcoGene:EG12055 , EcoliWiki:b2197 , Mint:MINT-1503318 , ModBase:P69490 , OU-Microarray:b2197 , PortEco:ccmE , PR:PRO_000022261 , Pride:P69490 , Protein Model Portal:P69490 , RefSeq:NP_416701 , RegulonDB:EG12055 , SMR:P69490 , String:511145.b2197 , UniProt:P69490

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

Gene-Reaction Schematic: ?

Genetic Regulation Schematic: ?

GO Terms:

Biological Process: GO:0017003 - protein-heme linkage Inferred from experiment Inferred by computational analysis [GOA06, GOA01, Schulz98]
GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11, GOA01]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [RichardFogal09, Ahuja06, Ahuja05, Ren02]
GO:0020037 - heme binding Inferred from experiment [Schulz98]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11]
Cellular Component: GO:0031237 - intrinsic component of periplasmic side of plasma membrane Inferred from experiment [Schulz98]
GO:0005829 - cytosol Inferred by computational analysis [DiazMejia09]
GO:0005886 - plasma membrane Inferred by computational analysis [UniProtGOA11a, UniProtGOA11, GOA06, GOA01]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11]
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

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

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, Hu05]. 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 [Schulz98]. 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, Schulz98, 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 [Schulz98, 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]

GO Terms:

Biological Process: GO:0017003 - protein-heme linkage Inferred from experiment [Schulz98]
Molecular Function: GO:0020037 - heme binding Inferred from experiment [RichardFogal09]


Subunit of: CcmCDE protoheme IX reservoir complex

Subunit composition of CcmCDE protoheme IX reservoir complex = [CcmD][CcmE][CcmC]
         protoheme IX ABC transporter - membrane subunit CcmD = CcmD (summary available)
         membrane anchored periplasmic heme chaperone CcmE = CcmE (summary available)
         protoheme IX ABC transporter - membrane subunit CcmC = CcmC (summary available)

Component of: protoheme IX ABC transporter (extended summary available)

Summary:
CcmCDE acts as a heme reservoir and releases the heme-bound chaperone, CcmE, upon binding of CcmA2B1 and ATP hydrolysis.

Credits:
Created 13-Dec-2007 by Johnson A , JCVI


Subunit of: protoheme IX ABC transporter

Synonyms: CcmABCDE protoheme IX ABC transporter

Subunit composition of protoheme IX ABC transporter = [(CcmD)(CcmE)(CcmC)][CcmB][CcmA]2
         CcmCDE protoheme IX reservoir complex = (CcmD)(CcmE)(CcmC) (summary available)
                 protoheme IX ABC transporter - membrane subunit CcmD = CcmD (summary available)
                 membrane anchored periplasmic heme chaperone CcmE = CcmE (summary available)
                 protoheme IX ABC transporter - membrane subunit CcmC = CcmC (summary available)
         protoheme IX ABC transporter - membrane subunit CcmB = CcmB (summary available)
         protoheme IX ABC transporter - ATP binding subunit = CcmA (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 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 in order for the covalent attachment of heme cofactor to occur. ccmA, ccmB, ccmC, ccmD, and ccmE are members of an operon whose gene products (CcmA-H) have been shown to be cytoplasmic membrane proteins required for cytochrome c maturation (Cytochrome c maturation proteins). The CcmABCDE protoheme IX ABC transporter has constituents which are members of the ATP-Binding Cassette (ABC) transporter superfamily. Sequence analysis suggests that CcmA is the ATP binding subunit and occurs as a homodimer, and CcmB, CcmC, and CcmD are membrane proteins. CcmE is a membrane-anchored, periplasmic heme chaperone. CcmC, CcmD, and CcmE form a complex for transfer of heme from the cytoplasm through CcmC to be covalently attached to CcmE in the periplasm. CcmD acts to stabilize CcmC and CcmE as a complex in the membrane. In this way the CcmCDE complex acts as a heme reservoir, conserving heme for when it is required for use. Binding of CcmA and CcmB and hydrolysis of ATP result in release of holoCcmE from the complex into the periplasm where heme can be incorporated covalently into cytochrome c apoproteins by the CcmEFGH holocytochrome c synthetase.

Immunoprecipitation experiments show CcmA, CcmB and CcmC interact directly and form a complex with a stoichiometry of CcmA2B1C1 [Feissner06]. CcmA is an ABC protein which interacts with the membrane proteins, CcmB and CcmC [Linton98]. CcmC also interacts directly with CcmE [Ren01, Feissner06]. CcmC is a membrane protein whose topology has been determined in homologues in other species [Goldman98] to consist of six transmembrane domains with two cytoplasmic and three periplasmic loops. Studies using point mutations of conserved residues suggest that a hydrophobic, periplasmically situated surface of CcmC is critical for the binding of heme and its presentation to CcmE [Schulz00]. The structure of CcmE has been determined by NMR spectroscopy [Enggist02, Vogeli02, Hu05]. 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 [Schulz98]. CcmD has been shown to be a small, cytoplasmically-oriented membrane protein [Schulz00]. CcmD has been shown to interact directly with CcmC and CcmE and stabilize their interaction [Ahuja05].

Purification and characterisation of the complexes of the Ccm pathway has helped elucidate the mechanisms of haem binding and trafficking [RichardFogal09]. Covalent haem attachment to the CcmCDE complex involves oxidation of haem iron (Fe2+ to Fe3+) and released holoCcmE possesses haem in the oxidised state (Fe3+). Haem in the CcmCDE complex is bound using His60 and His184 of CcmC.

ccmA, ccmB, ccmC, ccmD, ccmE, ccmF, ccmG, and ccmH mutants are deficient in the ability to produce c-type cytochromes [ThonyMeyer95, Grove96, Grove96a, ThroneHolst97, Tanapongpipat98, Schulz98, Fabianek99, Reid01, Enggist03, Edeling04, Ahuja06]. Analysis of ccm deletion mutants has suggested that CcmAB are not essential for heme export and covalent attachment to CcmE, the periplasmic heme chaperone, but CcmC is required [Schulz99, Cook00, Schulz00, Ren01]. Mutation deletion studies suggest that a periplasmically-situated hydrophobic surface of CcmC binds heme and presents it to CcmE in the periplasm [Schulz00]. Mutants of ccmA lack cytochrome c biogenesis in vivo and are unable to transfer heme from CcmE to apocytochrome c [Christensen07]. Mutation experiments show that even in the absence of CcmAB, CcmC is able to bind CcmE and heme, but CcmA and CcmB are required for release of holoCcmE from CcmC [Feissner06]. Mutation experiments suggest that CcmC is important in not only the transfer of heme to CcmE but also in heme delivery to apocytochrome c [Ahuja03]. Experiments examining cytochrome c biogenesis when heme production is limited show CcmE acts as a heme reservoir and is able to store heme for future use [Feissner06a]. Deletion mutation and immunoprecipitation studies suggest that CcmE shuttles between CcmC and CcmF for heme transfer to apocytochrome c [Ahuja03]. Overexpression of ccmD elevates CcmC and CcmE levels in the membrane and suppresses the phenotypes of certain CcmC mutants [Schulz00]. A ccmD deletion mutant phenotype can be overcome by overexpression of CcmC and CcmE [Schulz98]. Studies of ccmD deletion mutants have shown that CcmD affects the level of CcmE in the cytoplasmic membrane and is critical for CcmE function [Schulz00] and that it influences the efficiency of the heme transfer process [Ahuja03, Ahuja05].

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, ThonyMeyer00, ThonyMeyer02, Stevens05]

Citations: [Lee07, GarciaRubio07, RichardFogal07, Stevens06]


Enzymatic reaction of: protoheme IX ABC transporter

Synonyms: transport of protoheme IX

EC Number: 3.6.3.41


Sequence Features

Feature Class Location Common Name Attached Group Citations Comment
Transmembrane-Region 9 -> 29    
[UniProt10a]
UniProt: Helical; Signal-anchor for type II membrane protein;; Non-Experimental Qualifier: potential;
Transmembrane-Region 9 -> 30 TMS  
[Enggist02]
 
Mutagenesis-Variant 130    
[Enggist03, UniProt11a]
Alternate sequence: H → C; UniProt: Can still form a covalent bond with heme, but blocks heme release transfer to cytochrome c.
Alternate sequence: H → A; UniProt: Abolishes heme binding.
Amino-Acid-Sites-That-Bind 130 heme-binding site protoheme IX
[Schulz98]
 
Metal-Binding-Site 134    
[UniProt10]
UniProt: Iron (heme axial ligand);


Gene Local Context (not to scale): ?

Transcription Units:

Notes:

History:
10/20/97 Gene b2197 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG12055; confirmed by SwissProt match.


References

Ahuja03: Ahuja U, Thony-Meyer L (2003). "Dynamic features of a heme delivery system for cytochrome C maturation." J Biol Chem 278(52);52061-70. PMID: 14532274

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

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

Christensen07: Christensen O, Harvat EM, Thony-Meyer L, Ferguson SJ, Stevens JM (2007). "Loss of ATP hydrolysis activity by CcmAB results in loss of c-type cytochrome synthesis and incomplete processing of CcmE." FEBS J 274(9);2322-32. PMID: 17419738

Cook00: Cook GM, Poole RK (2000). "Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association." Microbiology 2000;146 ( Pt 2);527-36. PMID: 10708391

Darwin95: Darwin AJ, Stewart V (1995). "Nitrate and nitrite regulation of the Fnr-dependent aeg-46.5 promoter of Escherichia coli K-12 is mediated by competition between homologous response regulators (NarL and NarP) for a common DNA-binding site." J Mol Biol 1995;251(1);15-29. PMID: 7643383

DiazMejia09: Diaz-Mejia JJ, Babu M, Emili A (2009). "Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome." FEMS Microbiol Rev 33(1);66-97. PMID: 19054114

Eaves98: Eaves DJ, Grove J, Staudenmann W, James P, Poole RK, White SA, Griffiths I, Cole JA (1998). "Involvement of products of the nrfEFG genes in the covalent attachment of haem c to a novel cysteine-lysine motif in the cytochrome c552 nitrite reductase from Escherichia coli." Mol Microbiol 28(1);205-16. PMID: 9593308

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

Enggist02: Enggist E, Thony-Meyer L, Guntert P, Pervushin K (2002). "NMR structure of the heme chaperone CcmE reveals a novel functional motif." Structure 10(11);1551-7. PMID: 12429096

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

Fabianek97: Fabianek RA, Huber-Wunderlich M, Glockshuber R, Kunzler P, Hennecke H, Thony-Meyer L (1997). "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 272(7);4467-73. PMID: 9020171

Fabianek98: Fabianek RA, 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(7);1947-50. PMID: 9537397

Fabianek99: Fabianek RA, 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(2);92-100. PMID: 9914305

Feissner06: Feissner RE, Richard-Fogal CL, Frawley ER, Kranz RG (2006). "ABC transporter-mediated release of a haem chaperone allows cytochrome c biogenesis." Mol Microbiol 61(1);219-31. PMID: 16824107

Feissner06a: Feissner RE, Richard-Fogal CL, Frawley ER, Loughman JA, Earley KW, Kranz RG (2006). "Recombinant cytochromes c biogenesis systems I and II and analysis of haem delivery pathways in Escherichia coli." Mol Microbiol 60(3);563-77. PMID: 16629661

GarciaRubio07: Garcia-Rubio I, Braun M, Gromov I, Thony-Meyer L, Schweiger A (2007). "Axial coordination of heme in ferric CcmE chaperone characterized by EPR spectroscopy." Biophys J 92(4);1361-73. PMID: 17142277

GOA01: 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."

Goldman98: Goldman BS, Beck DL, Monika EM, Kranz RG (1998). "Transmembrane heme delivery systems." Proc Natl Acad Sci U S A 95(9);5003-8. PMID: 9560218

Grove96: Grove J, Tanapongpipat S, Thomas G, Griffiths L, Crooke H, 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 1996;19(3);467-81. PMID: 8830238

Grove96a: Grove J, Busby S, Cole J (1996). "The role of the genes nrf EFG and ccmFH in cytochrome c biosynthesis in Escherichia coli." Mol Gen Genet 1996;252(3);332-41. PMID: 8842153

Harvat05: Harvat EM, Stevens JM, Redfield C, Ferguson SJ (2005). "Functional characterization of the C-terminal domain of the cytochrome c maturation protein CcmE." J Biol Chem 280(44);36747-53. PMID: 16129669

Harvat09: Harvat EM, Redfield C, Stevens JM, Ferguson SJ (2009). "Probing the Heme-Binding Site of the Cytochrome c Maturation Protein CcmE (dagger)." Biochemistry. PMID: 19178152

Hu05: Hu K, Vogeli B, Pervushin K (2005). "Side-chain H and C resonance assignment in protonated/partially deuterated proteins using an improved 3D(13)C-detected HCC-TOCSY." J Magn Reson 174(2);200-8. PMID: 15862235

IobbiNivol94: Iobbi-Nivol C, Crooke H, Griffiths L, Grove J, Hussain H, Pommier J, Mejean V, Cole JA (1994). "A reassessment of the range of c-type cytochromes synthesized by Escherichia coli K-12." FEMS Microbiol Lett 1994;119(1-2);89-94. PMID: 8039676

Joyce06: Joyce AR, Reed JL, White A, Edwards R, Osterman A, Baba T, Mori H, Lesely SA, Palsson BO, Agarwalla S (2006). "Experimental and computational assessment of conditionally essential genes in Escherichia coli." J Bacteriol 188(23);8259-71. PMID: 17012394

Kranz98: Kranz R, Lill R, Goldman B, Bonnard G, Merchant S (1998). "Molecular mechanisms of cytochrome c biogenesis: three distinct systems." Mol Microbiol 29(2);383-96. PMID: 9720859

Lee07: Lee JH, Harvat EM, Stevens JM, Ferguson SJ, Saier MH (2007). "Evolutionary origins of members of a superfamily of integral membrane cytochrome c biogenesis proteins." Biochim Biophys Acta 1768(9);2164-81. PMID: 17706591

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

Linton98: Linton KJ, Higgins CF (1998). "The Escherichia coli ATP-binding cassette (ABC) proteins." Mol Microbiol 1998;28(1);5-13. PMID: 9593292

Mavridou12: Mavridou DA, Ferguson SJ, Stevens JM (2012). "The interplay between the disulfide bond formation pathway and cytochrome c maturation in Escherichia coli." FEBS Lett 586(12);1702-7. PMID: 22569094

Ouyang03: Ouyang N, Chen WY, Li Q, Gao YG, Hu HY, Xia ZX (2003). "Crystallization and preliminary crystallographic studies of Escherichia coli CcmG/DsbE protein." Acta Crystallogr D Biol Crystallogr 59(Pt 9);1674-5. PMID: 12925810

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

Rapp04: Rapp M, Drew D, Daley DO, Nilsson J, Carvalho T, Melen K, De Gier JW, Von Heijne G (2004). "Experimentally based topology models for E. coli inner membrane proteins." Protein Sci 13(4);937-45. PMID: 15044727

Reid01: Reid E, Cole J, Eaves DJ (2001). "The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly." Biochem J 355(Pt 1);51-8. PMID: 11256948

Reid98: Reid E, Eaves DJ, Cole JA (1998). "The CcmE protein from Escherichia coli is a haem-binding protein." FEMS Microbiol Lett 166(2);369-75. PMID: 9770295

Ren01: Ren Q, Thony-Meyer L (2001). "Physical interaction of CcmC with heme and the heme chaperone CcmE during cytochrome c maturation." J Biol Chem 276(35);32591-6. PMID: 11384983

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

RichardFogal07: Richard-Fogal CL, Frawley ER, Feissner RE, Kranz RG (2007). "Heme concentration dependence and metalloporphyrin inhibition of the system I and II cytochrome c assembly pathways." J Bacteriol 189(2);455-63. PMID: 17085564

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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Other References Related to Gene Regulation

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McNicholas02: McNicholas PM, Gunsalus RP (2002). "The molybdate-responsive Escherichia coli ModE transcriptional regulator coordinates periplasmic nitrate reductase (napFDAGHBC) operon expression with nitrate and molybdate availability." J Bacteriol 184(12);3253-9. PMID: 12029041

Partridge09: Partridge JD, Bodenmiller DM, Humphrys MS, Spiro S (2009). "NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility." Mol Microbiol 73(4);680-94. PMID: 19656291

Pruss01: Pruss BM, Liu X, Hendrickson W, Matsumura P (2001). "FlhD/FlhC-regulated promoters analyzed by gene array and lacZ gene fusions." FEMS Microbiol Lett 2001;197(1);91-7. PMID: 11287152

Stewart03: Stewart V, Bledsoe PJ, Williams SB (2003). "Dual overlapping promoters control napF (periplasmic nitrate reductase) operon expression in Escherichia coli K-12." J Bacteriol 185(19);5862-70. PMID: 13129959

Stewart03a: Stewart V, Bledsoe PJ (2003). "Synthetic lac operator substitutions for studying the nitrate- and nitrite-responsive NarX-NarL and NarQ-NarP two-component regulatory systems of Escherichia coli K-12." J Bacteriol 185(7);2104-11. PMID: 12644479


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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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