Protein Machineries Involved in the Attachment of Heme to Cytochrome c: Protein Structures and Molecular Mechanisms

Travaglini-Allocatelli, Carlo

doi:10.1155/2013/505714

Cited by 15 publications

(18 citation statements)

References 144 publications

(239 reference statements)

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“…Catalase coordinates hemin at the ferric ion via a tyrosine residue contained in the proximal hemin-binding motif RLFSYGD (21). Cytochrome c proteins typically contain a CXXCH heme-binding motif where the heme prosthetic group is covalently attached to the cytochrome at the cysteine residues (20). The heme trafficking protein CcmE from E. coli, which trafficks heme to periplasmic cytochrome enzymes, is covalently linked to heme at His130 (30).…”

Section: Discussionmentioning

confidence: 99%

“…Hemin titration of apo-Cj1386 determined that one hemin prosthetic group binds per Cj1386 subunit. Inspection of the Cj1386 protein sequence did not reveal any known hemin-binding motif, such as those characterized for cytochrome (20) and catalase enzymes (21). Therefore, to determine residues involved in hemin binding, the Cj1386 protein sequence was aligned against Cj1386 homologs from different bacterial species to identify conserved residues that potentially were important for hemin binding.…”

Section: Methodsmentioning

confidence: 99%

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Cj1386, an Atypical Hemin-Binding Protein, Mediates Hemin Trafficking to KatA in Campylobacter jejuni

Flint

Stintzi

2015

J Bacteriol

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. While the structure and biochemical properties of catalase enzymes have been well characterized over many decades of research, it remained unclear how catalases acquire hemin. We have previously reported that Cj1386 is essential for ensuring proper hemin content in Campylobacter jejuni catalase (KatA) (A. Flint, Y. Q. Sun, and A. Stintzi, J Bacteriol 194:334 -345, 2012). In this report, an in-depth molecular characterization of Cj1386 was performed to elucidate the mechanistic details of this association. Coimmunoprecipitation assays revealed that KatA-Cj1386 transiently interact in vivo, and UV-visible spectroscopy demonstrated that purified Cj1386 protein binds hemin. Furthermore, hemin titration experiments determined that hemin binds to Cj1386 in a 1:1 ratio with hexacoordinate hemin binding. Mutagenesis of potential hemin-coordinating residues in Cj1386 showed that tyrosine 57 was essential for hemin coordination when Cj1386 was overexpressed in Escherichia coli. The importance of tyrosine 57 in hemin trafficking in vivo was confirmed by introducing the cj1386 Y57A allele into a C. jejuni ⌬cj1386 mutant background. The cj1386 Y57A mutation resulted in increased sensitivity toward H 2 O 2 relative to the wild type, suggesting that KatA was not functional in this strain. In support of this finding, KatA immunoprecipitated from the ⌬cj1386؉cj1386 Y57A mutant had significantly reduced hemin content compared to that of the cj1386 WT background. Overall, these findings indicate that Cj1386 is involved in directly trafficking hemin to KatA and that tyrosine 57 plays a key role in this function.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Cj1386, an Atypical Hemin-Binding Protein, Mediates Hemin Trafficking to KatA in Campylobacter jejuni

Flint

Stintzi

2015

J Bacteriol

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“…System II, or Ccs (cytochrome c synthesis), is present in Gram‐positive bacteria, some β‐ and δ‐proteobacteria, cyanobacteria and in some chloroplasts (Simon and Hederstedt, ). System III is rather simple, containing only one cytochrome c heme lyase (CCHL), and is found mainly in fungal, vertebrate and invertebrate mitochondria (Kranz et al ., ; Travaglini‐Allocatelli, ). Despite the differences, these three systems share some critical properties (Frawley and Kranz, ; Kranz et al ., ; Richard‐Fogal et al ., ; Travaglini‐Allocatelli, ).…”

Section: Introductionmentioning

confidence: 99%

Shewanella oneidensis cytochrome c maturation component CcmI is essential for heme attachment at the non‐canonical motif of nitrite reductase NrfA

Jin

Wan

et al. 2014

Molecular Microbiology

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SummaryShewanella oneidensis is renowned for its respiratory versatility, which is largely due to abundant c-type cytochromes. Maturation of these proteins depends on a Ccm system encoded by genes in an unusual chromosomal arrangement, but the detailed mechanism is not understood. In this study, we identify SO0265 as CcmI, an apocytochrome c chaperone that is important and essential for maturation of c-type cytochromes with the canonical heme binding motif(s) (HBM; CX2CH) and nitrite reductase NrfA carrying a non-canonical CX2CK motif respectively. We show that the N-terminal transmembrane segment of CcmI, CcmI-1, is sufficient for maturation of the former but the entire protein is required for maturation of the latter. Although S. oneidensis possesses a heme lyase, SirEFG, dedicated for non-canonical HBMs, it is specific for SirA, a sulfite reductase with a CX15CH motif. By presenting evidence that the periplasmic portion of CcmI, CcmI-2, interacts with NrfA, we suggest that CcmI also takes the role of Escherichia coli NrfG for chaperoning apo-NrfA for maturation at CX2CK. Moreover, intact CcmI is required for maturation of NrfA, presumably by ensuring that heme attachment at canonical HBMs occurs before apoprotein degradation.

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“…For example, in multiple Bacteroides genomes, a gene for arsenic binding and transfer (arsD) is adjacent to a gene for cytochrome c biogenesis protein. Cytochrome c , produced by a posttranslational process, consists of heme-containing proteins important for cellular energy production and signaling 28,29. Previous reported research on Bacteroides and arsenic appears to be limited to phenotypic characterization of susceptibilities to arsenate in which 25% of strains in the Bacteroides fragilis group, which included Bacteroides thetaiotaomicron , were resistant to 0.01 M arsenate 30.…”

Section: Introductionmentioning

confidence: 99%

Evaluative Profiling of Arsenic Sensing and Regulatory Systems in the Human Microbiome Project Genomes

et al. 2014

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The influence of environmental chemicals including arsenic, a type 1 carcinogen, on the composition and function of the human-associated microbiota is of significance in human health and disease. We have developed a suite of bioinformatics and visual analytics methods to evaluate the availability (presence or absence) and abundance of functional annotations in a microbial genome for seven Pfam protein families: As(III)-responsive transcriptional repressor (ArsR), anion-transporting ATPase (ArsA), arsenical pump membrane protein (ArsB), arsenate reductase (ArsC), arsenical resistance operon transacting repressor (ArsD), water/glycerol transport protein (aquaporins), and universal stress protein (USP). These genes encode function for sensing and/or regulating arsenic content in the bacterial cell. The evaluative profiling strategy was applied to 3,274 genomes from which 62 genomes from 18 genera were identified to contain genes for the seven protein families. Our list included 12 genomes in the Human Microbiome Project (HMP) from the following genera: Citrobacter, Escherichia, Lactobacillus, Providencia, Rhodococcus, and Staphylococcus. Gene neighborhood analysis of the arsenic resistance operon in the genome of Bacteroides thetaiotaomicron VPI-5482, a human gut symbiont, revealed the adjacent arrangement of genes for arsenite binding/transfer (ArsD) and cytochrome c biosynthesis (DsbD_2). Visual analytics facilitated evaluation of protein annotations in 367 genomes in the phylum Bacteroidetes identified multiple genomes in which genes for ArsD and DsbD_2 were adjacently arranged. Cytochrome c, produced by a posttranslational process, consists of heme-containing proteins important for cellular energy production and signaling. Further research is desired to elucidate arsenic resistance and arsenic-mediated cellular energy production in the Bacteroidetes.

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Protein Machineries Involved in the Attachment of Heme to Cytochrome c: Protein Structures and Molecular Mechanisms

Cited by 15 publications

References 144 publications

Cj1386, an Atypical Hemin-Binding Protein, Mediates Hemin Trafficking to KatA in Campylobacter jejuni

Cj1386, an Atypical Hemin-Binding Protein, Mediates Hemin Trafficking to KatA in Campylobacter jejuni

Shewanella oneidensis cytochrome c maturation component CcmI is essential for heme attachment at the non‐canonical motif of nitrite reductase NrfA

Evaluative Profiling of Arsenic Sensing and Regulatory Systems in the Human Microbiome Project Genomes

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