ABC transporter-mediated release of a haem chaperone allows cytochrome c biogenesis

Mol Microbiol. 2006 Jul;61(1):219-31. doi: 10.1111/j.1365-2958.2006.05221.x.

Abstract

Although organisms from all kingdoms have either the system I or II cytochrome c biogenesis pathway, it has remained a mystery as to why these two distinct pathways have developed. We have previously shown evidence that the system I pathway has a higher affinity for haem than system II for cytochrome c biogenesis. Here, we show the mechanism by which the system I pathway can utilize haem at low levels. The mechanism involves an ATP-binding cassette (ABC) transporter that is required for release of the periplasmic haem chaperone CcmE to the last step of cytochrome c assembly. This ABC transporter is composed of the ABC subunit CcmA, and two membrane proteins, CcmB and CcmC. In the absence of CcmA or CcmB, holo(haem)CcmE binds to CcmC in a stable dead-end complex, indicating high affinity binding of haem to CcmC. Expression of CcmA and CcmB facilitates formation of the CcmA2B1C1 complex and ATP-dependent release of holoCcmE. We propose that the CcmA2B1C1 complex represents a new subgroup within the ABC transporter superfamily that functions to release a chaperone.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism*
  • Apoproteins / metabolism
  • Bacterial Outer Membrane Proteins / genetics
  • Bacterial Outer Membrane Proteins / metabolism*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Biological Transport
  • Cytochrome c Group / biosynthesis*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Heme / metabolism*
  • Hemeproteins / biosynthesis
  • Hemeproteins / genetics
  • Hemeproteins / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Models, Biological
  • Molecular Chaperones / metabolism*
  • Plasmids / genetics
  • Recombinant Fusion Proteins / metabolism

Substances

  • ATP-Binding Cassette Transporters
  • Apoproteins
  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins
  • CcmA protein, bacteria
  • CcmB protein, E coli
  • CcmC protein, bacteria
  • CcmE protein, E coli
  • Cytochrome c Group
  • Escherichia coli Proteins
  • Hemeproteins
  • Membrane Proteins
  • Molecular Chaperones
  • Recombinant Fusion Proteins
  • Heme