Biochemical requirements for the maturation of mitochondrial c-type cytochromes

Hamel, Patrice; Corvest, Vincent; Giegé, Philippe; Bonnard, Géraldine

doi:10.1016/j.bbamcr.2008.06.017

Cited by 67 publications

(96 citation statements)

References 172 publications

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“…Figure 2 diagrams the thiol proteins (in red) which transfer reducing equivalents from inside the cell to outside. Since some aspects of assembly have been reviewed in the last 5 years (5,9,12,58,70,157), here we focus on selected emerging concepts. Because all proteins in systems I and II are integral membrane proteins, descriptions will be presented in the context of the two-dimensional topologies of the integral membrane proteins in the pathways.…”

Section: Cytochrome C Biogenesis: Three Systems and Some Emerging Spmentioning

confidence: 99%

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

Kranz¹,

Richard-Fogal²,

Taylor

et al. 2009

Microbiol Mol Biol Rev

225

372

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SUMMARY Heme is the prosthetic group for cytochromes, which are directly involved in oxidation/reduction reactions inside and outside the cell. Many cytochromes contain heme with covalent additions at one or both vinyl groups. These include farnesylation at one vinyl in hemes o and a and thioether linkages to each vinyl in cytochrome c (at CXXCH of the protein). Here we review the mechanisms for these covalent attachments, with emphasis on the three unique cytochrome c assembly pathways called systems I, II, and III. All proteins in system I (called Ccm proteins) and system II (Ccs proteins) are integral membrane proteins. Recent biochemical analyses suggest mechanisms for heme channeling to the outside, heme-iron redox control, and attachment to the CXXCH. For system II, the CcsB and CcsA proteins form a cytochrome c synthetase complex which specifically channels heme to an external heme binding domain; in this conserved tryptophan-rich “WWD domain” (in CcsA), the heme is maintained in the reduced state by two external histidines and then ligated to the CXXCH motif. In system I, a two-step process is described. Step 1 is the CcmABCD-mediated synthesis and release of oxidized holoCcmE (heme in the Fe+3 state). We describe how external histidines in CcmC are involved in heme attachment to CcmE, and the chemical mechanism to form oxidized holoCcmE is discussed. Step 2 includes the CcmFH-mediated reduction (to Fe+2) of holoCcmE and ligation of the heme to CXXCH. The evolutionary and ecological advantages for each system are discussed with respect to iron limitation and oxidizing environments.

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Section: Cytochrome C Biogenesis: Three Systems and Some Emerging Spmentioning

confidence: 99%

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

Kranz¹,

Richard-Fogal²,

Taylor

et al. 2009

Microbiol Mol Biol Rev

225

372

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“…For this biochemical process, three different systems have been described Hamel et al, 2009;Kranz et al, 2009;Sanders et al, 2010). The cytochrome c maturation (ccm) system (also called system I) is found in mitochondria of plants and red algae, in archaea, and in different subgroups of bacteria.…”

Section: Function Of Rpf3 In Mitochondria Of Arabidopsis Accession C24mentioning

confidence: 99%

RNA PROCESSING FACTOR3 Is Crucial for the Accumulation of MatureccmCTranscripts in Mitochondria of Arabidopsis Accession Columbia

et al. 2011

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RNA PROCESSING FACTOR1 (RPF1) and RPF2 are pentatricopeptide repeat (PPR) proteins involved in 5# processing of different mitochondrial mRNAs in Arabidopsis (Arabidopsis thaliana). Both factors are highly similar to RESTORERS OF FERTILITY (RF), which are part of cytoplasmic male sterility/restoration systems in various plant species. These findings suggest a predominant role of RF-like PPR proteins in posttranscriptional 5# processing. To further explore the functions of this group of proteins, we examined a number of T-DNA lines carrying insertions in the corresponding PPR genes. This screening identified a nearly complete absence of mature ccmC transcripts in an At1g62930 T-DNA insertion line, a phenotype that could be restored by the introduction of the intact At1g62930 gene into the mutant. The insertion in this nuclear gene, which we now call RPF3, also leads to a severe reduction of the CcmC protein in mitochondria. The analysis of C24/rpf3-1 F2 hybrids lacking functional RPF3 genes revealed that this gene has less influence on the generation of the mature ccmC 5# transcript end derived from a distinct ccmC 5# upstream configuration found in mitochondrial DNAs from C24 and other accessions. These data show that a particular function of an RF-like protein is required only in connection with a distinct mtDNA configuration. Our new results further substantiate the fundamental role of RF-like PPR proteins in the posttranscriptional generation of plant mitochondrial 5# transcript termini.

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“…The human HCCS recognizes both cyt c and cyt c 1 of the membrane cytochrome bc 1 complex III (6,45). Some lower eukaryotes such as Saccharomyces cerevisiae have two related synthases: HCCS that recognizes cyt c and HCC 1 S that recognizes cyt c 1 (8,46).…”

Section: Discussionmentioning

confidence: 99%

Molecular Basis Behind Inability of Mitochondrial Holocytochrome c Synthase to Mature Bacterial Cytochromes

Babbitt

Hsu

Kranz

2016

Journal of Biological Chemistry

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Mitochondrial holocytochrome c synthase (HCCS) is required for cytochrome c (cyt c) maturation and therefore respiration. HCCS efficiently attaches heme via two thioethers to CXXCH of mitochondrial but not bacterial cyt c even though they are functionally conserved. This inability is due to residues in the bacterial cyt c N terminus, but the molecular basis is unknown. Human cyts c with deletions of single residues in ␣ helix-1, which mimic bacterial cyt c, are poorly matured by human HCCS. Focusing on ⌬M13 cyt c, we co-purified this variant with HCCS, demonstrating that HCCS recognizes the bacterial-like cytochrome. Although an HCCS-WT cyt c complex contains two covalent links, HCCS-⌬M13 cyt c contains only one thioether attachment. Using multiple approaches, we show that the single attachment is to the second thiol of C 15 SQC 18 H, indicating that ␣ helix-1 is required for positioning the first cysteine for covalent attachment, whereas the histidine of CXXCH positions the second cysteine. Modeling of the N-terminal structure suggested that the serine residue (of CSQCH) would be anchored where the first cysteine should be in ⌬M13 cyt c. An engineered cyt c with a CQCH motif in the ⌬M13 background is matured at higher levels (2-3-fold), providing further evidence for ␣ helix-1 positioning the first cysteine. Bacterial cyt c biogenesis pathways (Systems I and II) appear to recognize simply the CXXCH motif, not requiring ␣ helix-1. Results here explain mechanistically how HCCS (System III) requires an extended region adjacent to CXXCH for maturation.

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Biochemical requirements for the maturation of mitochondrial c-type cytochromes

Cited by 67 publications

References 172 publications

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

RNA PROCESSING FACTOR3 Is Crucial for the Accumulation of MatureccmCTranscripts in Mitochondria of Arabidopsis Accession Columbia

Molecular Basis Behind Inability of Mitochondrial Holocytochrome c Synthase to Mature Bacterial Cytochromes

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