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PMID: 11250894 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA.

The EMBO journal ·Vol. 20 ·No. 6 ·2001-03-15 ·Pages 1281-8

Hell K, Neupert W, Stuart RA

Abstract

Oxa1p is a member of the conserved Oxa1/YidC/Alb3 protein family involved in the membrane insertion of proteins. Oxa1p has been shown previously to directly facilitate the export of the N-terminal domains of membrane proteins across the inner membrane to the intermembrane space of mitochondria. Here we report on a general role of Oxa1p in the membrane insertion of proteins. (i) The function of Oxa1p is not limited to the insertion of membrane proteins that undergo N-terminal tail export; rather, it also extends to the insertion of other polytopic proteins such as the mitochondrially encoded Cox1p and Cox3p proteins. These are proteins whose N-termini are retained in the mitochondrial matrix. (ii) Oxa1p interacts directly with these substrates prior to completion of their synthesis. (iii) The interaction of Oxa1p with its substrates is particularly strong when nascent polypeptide chains are inserted into the inner membrane, suggesting a direct function of Oxa1p in co-translational insertion from the matrix. Taken together, we conclude that the Oxa1 complex represents a general membrane protein insertion machinery in the inner membrane of mitochondria.

MeSH Terms
Carrier Proteins/metabolism Cytochrome b Group/metabolism DNA, Mitochondrial/genetics Electron Transport Complex IV/metabolism Fungal Proteins/metabolism Intracellular Membranes/metabolism Membrane Potentials Membrane Proteins/metabolism Mitochondria/metabolism Protein Biosynthesis Protein Transport Ribosomes/metabolism Yeasts
Chemicals
Carrier Proteins Cytochrome b Group DNA, Mitochondrial Fungal Proteins Membrane Proteins Electron Transport Complex IV
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hell K
Institut fur Physiologische Chemie der Universität München, Goethestrasse 33, D-80336 München, Germany.
Neupert W
Stuart R A
References (28)
28 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Mitochondrial inner membrane bound Pet1402 protein is rapidly imported into mitochondria and affects the integrity of the cytochrome oxidase and ubiquinol-cytochrome c oxidoreductase complexes.
    Biol Chem. 1997 Nov;378(11):1373-9 PMID: 9426197
  3. N-terminal tail export from the mitochondrial matrix. Adherence to the prokaryotic "positive-inside" rule of membrane protein topology.
    J Biol Chem. 1999 Jul 9;274(28):19617-22 PMID: 10391898
  4. YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase.
    EMBO J. 2000 Feb 15;19(4):542-9 PMID: 10675323
  5. Topogenesis of cytochrome oxidase subunit II. Mechanisms of protein export from the mitochondrial matrix.
    J Biol Chem. 1995 Nov 10;270(45):27079-86 PMID: 7592959
  6. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A.
    Science. 1996 May 24;272(5265):1136-44 PMID: 8638158
  7. Mutations affecting a yeast mitochondrial inner membrane protein, pnt1p, block export of a mitochondrially synthesized fusion protein from the matrix.
    Mol Cell Biol. 1999 Oct;19(10):6598-607 PMID: 10490599
  8. Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs.
    EMBO J. 1998 Oct 1;17(19):5796-804 PMID: 9755179
  9. Structure at 2.3 A resolution of the cytochrome bc(1) complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment.
    Structure. 2000 Jun 15;8(6):669-84 PMID: 10873857
  10. Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p.
    EMBO J. 1997 May 1;16(9):2217-26 PMID: 9171337
  11. Making membranes in bacteria.
    Nature. 2000 Aug 10;406(6796):575, 577 PMID: 10949283
  12. Mutations in the membrane anchor of yeast cytochrome c1 compensate for the absence of Oxa1p and generate carbonate-extractable forms of cytochrome c1.
    Genetics. 1998 Oct;150(2):601-11 PMID: 9755193
  13. Isolation and characterization of ribosomes from yeast mitochondria.
    FEBS Lett. 1969 May;3(3):177-181 PMID: 11947000
  14. Oxa1p, an essential component of the N-tail protein export machinery in mitochondria.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2250-5 PMID: 9482871
  15. PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast.
    Mol Gen Genet. 1994 Nov 1;245(3):272-8 PMID: 7816036
  16. Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space.
    FEBS Lett. 1997 Dec 1;418(3):367-70 PMID: 9428747
  17. Topogenesis of inner membrane proteins of mitochondria.
    Trends Biochem Sci. 1996 Jul;21(7):261-7 PMID: 8755248
  18. Identification of Cox20p, a novel protein involved in the maturation and assembly of cytochrome oxidase subunit 2.
    J Biol Chem. 2000 Feb 18;275(7):4571-8 PMID: 10671482
  19. YidC mediates membrane protein insertion in bacteria.
    Nature. 2000 Aug 10;406(6796):637-41 PMID: 10949305
  20. Conservative sorting of F0-ATPase subunit 9: export from matrix requires delta pH across inner membrane and matrix ATP.
    EMBO J. 1995 Jul 17;14(14):3445-51 PMID: 7628445
  21. Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p.
    Mol Biol Cell. 1997 Aug;8(8):1449-60 PMID: 9285818
  22. Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes.
    J Biol Chem. 2000 Jan 21;275(3):1529-32 PMID: 10636840
  23. Nascent Lep inserts into the Escherichia coli inner membrane in the vicinity of YidC, SecY and SecA.
    FEBS Lett. 2000 Jul 7;476(3):229-33 PMID: 10913619
  24. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  25. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis.
    J Mol Biol. 1994 Jun 3;239(2):201-12 PMID: 8196054
  26. ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria.
    Plant Cell. 1997 May;9(5):717-30 PMID: 9165749
  27. The organization of ribosomal granules within mitochondrial structures of aerobic and anaerobic cells of Saccharomyces cerevisae.
    J Cell Biol. 1972 Dec;55(3):721-6 PMID: 4571231
  28. Cloning and characterization of COX18, a Saccharomyces cerevisiae PET gene required for the assembly of cytochrome oxidase.
    J Biol Chem. 2000 May 19;275(20):14898-902 PMID: 10809734
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2001-03-15
Pages
1281-8
Language
English
Region
England
NLM ID
8208664
PMCID
PMC145526
Subset
IM
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