Escherichia coli K-12 substr. MG1655 Polypeptide: ABC complex for formation and release of holoCcmE - ATP binding subunit

Gene: ccmA Accession Numbers: EG12059 (EcoCyc), b2201, ECK2193

Synonyms: yejW

Regulation Summary Diagram: ?

Regulation summary diagram for ccmA

Component of: ABC complex for formation and release of holoCcmE (extended summary available)

CcmA is the ATP-binding component of the ABC complex responsible for formation and release of holo CcmE, that is, heme containing CcmE. In the absence of CcmA or CcmB, holoCcmE remains bound to CcmC; expression of CcmA and CcmB results in formation of a CcmA2B1C1 complex and release of holoCcmE [Feissner06]. CcmAB is present in the membrane fraction of cells and the purified complex has ATPase activity in vitro; CcmA contains the sequence features of ATP-binding proteins and is predicted to be a cytoplasmic protein [Christensen07].

Citations: [Schulz99]

Gene Citations: [Darwin95, Grove96]

Locations: periplasmic space, cytosol, inner membrane

Map Position: [2,295,043 <- 2,295,666] (49.47 centisomes, 178°)
Length: 624 bp / 207 aa

Molecular Weight of Polypeptide: 23.053 kD (from nucleotide sequence)

Unification Links: ASAP:ABE-0007279 , CGSC:36574 , EchoBASE:EB1989 , EcoGene:EG12059 , EcoliWiki:b2201 , ModBase:P33931 , OU-Microarray:b2201 , PortEco:ccmA , PR:PRO_000022257 , Protein Model Portal:P33931 , RefSeq:NP_416705 , RegulonDB:EG12059 , SMR:P33931 , String:511145.b2201 , UniProt:P33931

Relationship Links: InterPro:IN-FAMILY:IPR003439 , InterPro:IN-FAMILY:IPR003593 , InterPro:IN-FAMILY:IPR005895 , InterPro:IN-FAMILY:IPR017871 , InterPro:IN-FAMILY:IPR027417 , Panther:IN-FAMILY:PTHR24220:SF407 , Pfam:IN-FAMILY:PF00005 , Prosite:IN-FAMILY:PS00211 , Prosite:IN-FAMILY:PS50893 , Prosite:IN-FAMILY:PS51243 , Smart:IN-FAMILY:SM00382

In Paralogous Gene Group: 23 (75 members)

Gene-Reaction Schematic: ?

Gene-Reaction Schematic

Genetic Regulation Schematic: ?

Genetic regulation schematic for ccmA

GO Terms:

Biological Process: GO:0015886 - heme transport Inferred from experiment [Feissner06]
GO:0006810 - transport Inferred by computational analysis [UniProtGOA11, GOA06]
GO:0008152 - metabolic process Inferred by computational analysis [UniProtGOA11, GOA01a]
GO:0017004 - cytochrome complex assembly Inferred by computational analysis [UniProtGOA11, GOA01a]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [Christensen07, Feissner06]
GO:0042623 - ATPase activity, coupled Inferred from experiment [Feissner06, Christensen07]
GO:0000166 - nucleotide binding Inferred by computational analysis [UniProtGOA11]
GO:0005215 - transporter activity Inferred by computational analysis [GOA06, GOA01a]
GO:0005524 - ATP binding Inferred by computational analysis [UniProtGOA11, GOA06, GOA01a]
GO:0015439 - heme-transporting ATPase activity Inferred by computational analysis [GOA01]
GO:0016787 - hydrolase activity Inferred by computational analysis [UniProtGOA11]
GO:0016887 - ATPase activity Inferred by computational analysis [GOA01a]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11a, UniProtGOA11, Christensen07, DiazMejia09]
GO:0043190 - ATP-binding cassette (ABC) transporter complex Inferred from experiment Inferred by computational analysis [GOA06, Feissner06]
GO:0005829 - cytosol Inferred by computational analysis [Christensen07]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11]
GO:0030288 - outer membrane-bounded periplasmic space Inferred by computational analysis [GOA01a]
GO:0031234 - extrinsic component of cytoplasmic side of plasma membrane Inferred by computational analysis [Feissner06]

MultiFun Terms: information transfer protein related chaperoning, repair (refolding)
metabolism biosynthesis of building blocks cofactors, small molecule carriers heme, porphyrine
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes
transport Channel-type Transporters Pyrophosphate Bond (ATP; GTP; P2) Hydrolysis-driven Active Transporters The ATP-binding Cassette (ABC) Superfamily + ABC-type Uptake Permeases ABC superfamily ATP binding cytoplasmic component

Essentiality data for ccmA knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 1]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 2]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 3]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 2]
Yes [Feist07, Comment 4]

Last-Curated ? 12-Nov-2014 by Mackie A , Macquarie University

Subunit of: ABC complex for formation and release of holoCcmE

Synonyms: CcmABCDE protoheme IX ABC transporter

Subunit composition of ABC complex for formation and release of holoCcmE = [CcmD][CcmB][CcmA]2[CcmE][CcmC]
         ABC complex for formation and release of holoCcmE - membrane subunit CcmD = CcmD (summary available)
         ABC complex for formation and release of holoCcmE - membrane subunit CcmB = CcmB (summary available)
         ABC complex for formation and release of holoCcmE - ATP binding subunit = CcmA (summary available)
         membrane anchored periplasmic heme chaperone CcmE = CcmE (summary available)
         ABC complex for formation and release of holoCcmE - membrane subunit CcmC = CcmC (summary available)

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 complex 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, thus freeing it for step II of cytochrome c maturation - heme incorporation into cytochrome c apoproteins by the CcmFHG 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 predicted to contain of six transmembrane domains with two cytoplasmic and three periplasmic loops [Goldman98]. A hydrophobic, periplasmically situated surface of CcmC is critical for the binding of heme and its presentation to CcmE [Schulz00]. Two conserved histidine residues - His60 and His184 - are required for holoCcmE formation [Schulz99].

CcmD is a small, cytoplasmically-oriented membrane protein [Schulz00]. CcmD interacts directly with CcmC and CcmE and may function to stabilize the CcmCDE ternary complex [Ahuja05].

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 CcmE has been determined by NMR spectroscopy; the protein has a rigid β-barrel core with a hydrophobic surface for heme binding and is linked to a flexible α helical domain which may function to protect the bound heme [Enggist02].

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+). In the absence of CcmAB (which is required for the release of holoCcmE) a CcmE:heme:CcmC complex can be trapped and purified; CcmE only interacts stably with CcmC when heme is present; heme in the complex is liganded to His60 and His184 of CcmC [Feissner06, RichardFogal10].

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, Schulz98a, Fabianek99, Reid01a, 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]. 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]. Mutants of ccmA lack cytochrome c biogenesis in vivo and are unable to transfer heme from CcmE to apocytochrome c [Christensen07]. 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]. 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 [Schulz98a]. 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, Stevens11]

Citations: [Lee07d, GarciaRubio07, RichardFogal07, Stevens06]

GO Terms:

Biological Process: GO:0015886 - heme transport Inferred from experiment [Schulz99, RichardFogal09]
GO:0017003 - protein-heme linkage Inferred by computational analysis Inferred from experiment [Schulz99, ThonyMeyer95]

Last-Curated ? 10-Nov-2014 by Mackie A , Macquarie University

Enzymatic reaction of: ABC complex for formation and release of holoCcmE

Synonyms: transport of protoheme IX

EC Number:

Transport reaction diagram for ABC complex for formation and release of holoCcmE

This reaction represents step I of cytochrome c synthesis in E. coli K-12. In this reaction reduced heme (the product of aerobic and anaerobic heme synthesis) is moved from the cytosol to the periplasmic face concomitant with binding to apoCcmE. The reaction results in the release of oxidized (Fe3+) holoCcmE. The CcmABCD transporter is not a typical ABC transporter - hydrolysis of ATP is required for release of holoCcmE rather than for active transmembrane transport. The energy source for movment of heme, if required, is not known (see review by [Kranz09]).

Sequence Features

Protein sequence of ABC complex for formation and release of holoCcmE - ATP binding subunit with features indicated

Feature Class Location Common Name Citations Comment
Conserved-Region 4 -> 207  
UniProt: ABC transporter;
Nucleotide-Phosphate-Binding-Region 36 -> 43  
UniProt: ATP; Non-Experimental Qualifier: potential;
Mutagenesis-Variant 42  
alternate sequence K &rarr D results in loss of ATPase actvity in vitro and loss of cytochrome c in vivo
Conserved-Region 129 -> 133 ABC signature motif
Mutagenesis-Variant 132  
alternate sequence G → A prevents release of holoCcmE

Gene Local Context (not to scale): ?

Gene local context diagram

Transcription Units:

Transcription-unit diagram

Transcription-unit diagram

Transcription-unit diagram

Transcription-unit diagram


Peter D. Karp on Wed Jan 18, 2006:
Gene right-end position adjusted based on analysis performed in the 2005 E. coli annotation update [Riley06 ].
10/20/97 Gene b2201 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG12059; confirmed by SwissProt match.


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

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

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

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

Feist07: Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BO (2007). "A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information." Mol Syst Biol 3;121. PMID: 17593909

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

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

GOA01: GOA, MGI (2001). "Gene Ontology annotation based on Enzyme Commission mapping." Genomics 74;121-128.

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."

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

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

Kranz09: Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER (2009). "Cytochrome c biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control." Microbiol Mol Biol Rev 73(3);510-28, Table of Contents. PMID: 19721088

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

Lee07d: 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

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

Reid01a: 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

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

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

RichardFogal10: Richard-Fogal C, Kranz RG (2010). "The CcmC:heme:CcmE complex in heme trafficking and cytochrome c biosynthesis." J Mol Biol 401(3);350-62. PMID: 20599545

Riley06: Riley M, Abe T, Arnaud MB, Berlyn MK, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett G, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL (2006). "Escherichia coli K-12: a cooperatively developed annotation snapshot--2005." Nucleic Acids Res 34(1);1-9. PMID: 16397293

Schulz00: Schulz H, Pellicioli EC, Thony-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(6);1379-88. PMID: 10998170

Schulz98a: Schulz H, Hennecke H, Thony-Meyer L (1998). "Prototype of a heme chaperone essential for cytochrome c maturation." Science 281(5380);1197-200. PMID: 9712585

Schulz99: Schulz H, Fabianek RA, Pellicioli EC, Hennecke H, Thony-Meyer L (1999). "Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB." Proc Natl Acad Sci U S A 1999;96(11);6462-7. PMID: 10339610

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

Stevens11: Stevens JM, Mavridou DA, Hamer R, Kritsiligkou P, Goddard AD, Ferguson SJ (2011). "Cytochrome c biogenesis System I." FEBS J 278(22);4170-8. PMID: 21958041

Tanapongpipat98: Tanapongpipat S, Reid E, Cole JA, Crooke H (1998). "Transcriptional control and essential roles of the Escherichia coli ccm gene products in formate-dependent nitrite reduction and cytochrome c synthesis." Biochem J 334 ( Pt 2);355-65. PMID: 9716493

ThonyMeyer00: Thony-Meyer L (2000). "Haem-polypeptide interactions during cytochrome c maturation." Biochim Biophys Acta 1459(2-3);316-24. PMID: 11004446

ThonyMeyer02: Thony-Meyer L (2002). "Cytochrome c maturation: a complex pathway for a simple task?." Biochem Soc Trans 30(4);633-8. PMID: 12196152

ThonyMeyer95: Thony-Meyer L, Fischer F, Kunzler P, Ritz D, Hennecke H (1995). "Escherichia coli genes required for cytochrome c maturation." J Bacteriol 177(15);4321-6. PMID: 7635817

ThonyMeyer97: Thony-Meyer L (1997). "Biogenesis of respiratory cytochromes in bacteria." Microbiol Mol Biol Rev 1997;61(3);337-76. PMID: 9293186

ThroneHolst97: Throne-Holst M, Thony-Meyer L, Hederstedt L (1997). "Escherichia coli ccm in-frame deletion mutants can produce periplasmic cytochrome b but not cytochrome c." FEBS Lett 410(2-3);351-5. PMID: 9237661

UniProt09: UniProt Consortium (2009). "UniProt version 15.8 released on 2009-10-01 00:00:00." Database.

UniProt10: UniProt Consortium (2010). "UniProt version 2010-07 released on 2010-06-15 00:00:00." Database.

UniProtGOA11: UniProt-GOA (2011). "Gene Ontology annotation based on manual assignment of UniProtKB keywords in UniProtKB/Swiss-Prot entries."

UniProtGOA11a: UniProt-GOA (2011). "Gene Ontology annotation based on the manual assignment of UniProtKB Subcellular Location terms in UniProtKB/Swiss-Prot entries."

Other References Related to Gene Regulation

Choe93: Choe M, Reznikoff WS (1993). "Identification of the regulatory sequence of anaerobically expressed locus aeg-46.5." J Bacteriol 1993;175(4);1165-72. PMID: 8432709

Darwin98: Darwin AJ, Ziegelhoffer EC, Kiley PJ, Stewart V (1998). "Fnr, NarP, and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro." J Bacteriol 1998;180(16);4192-8. PMID: 9696769

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

Report Errors or Provide Feedback
Please cite the following article in publications resulting from the use of EcoCyc: Nucleic Acids Research 41:D605-12 2013
Page generated by SRI International Pathway Tools version 19.0 on Mon Oct 5, 2015, BIOCYC14A.