Mitochondria were derived from intracellular bacteria and the mitochondrial intermembrane space is topologically equivalent to the bacterial periplasm. Both compartments contain ATP-independent chaperones involved in the transport of hydrophobic membrane proteins. The mitochondrial TIM (translocase of the mitochondrial inner membrane) 10 complex and the periplasmic chaperone SurA were examined in terms of evolutionary relation, structural similarity, substrate binding specificity and their function in transporting polypeptides for insertion into membranes. The two chaperones are evolutionarily unrelated; structurally, they are also distinct both in their characteristics, as determined by SAXS (small-angle X-ray scattering), and in pairwise structural comparison using the distance matrix alignment (DALILite server). Despite their structural differences, SurA and the TIM10 complex share a common binding specificity in Pepscan assays of substrate proteins. Comprehensive analysis of the binding on a total of 1407 immobilized 13-mer peptides revealed that the TIM10 complex, like SurA, does not bind hydrophobic peptides generally, but that both chaperones display selectivity for peptides rich in aromatic residues and with net positive charge. This common binding specificity was not sufficient for SurA to completely replace TIM10 in yeast cells in vivo. In yeast cells lacking TIM10, when SurA is targeted to the intermembrane space of mitochondria, it binds translocating substrate proteins, but fails to completely transfer the substrate to the translocase in the mitochondrial inner membrane. We suggest that SurA was incapable of presenting substrates effectively to the primitive TOM (translocase of the mitochondrial outer membrane) and TIM complexes in early mitochondria, and was replaced by the more effective small Tim chaperone.
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Research Article|
December 21 2007
Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space
Felicity H. Alcock;
Felicity H. Alcock
*Institute of Molecular Biology and Biotechnology, Foundation of Research and Technology Hellas, PO Box 1385, 71110 Heraklion, Crete, Greece
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J. Günter Grossmann;
J. Günter Grossmann
†Molecular Biophysics Group, CCLRC Daresbury Laboratory, Warrington, Cheshire WA4 4AD, U.K.
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Ian E. Gentle;
Ian E. Gentle
‡Department of Biochemistry and Molecular Biology, University of Melbourne, Parkville 3010, VIC, Australia
§Bio21 Molecular Science and Biotechnology Institute, Parkville 3010, VIC, Australia
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Vladimir A. Likić;
Vladimir A. Likić
§Bio21 Molecular Science and Biotechnology Institute, Parkville 3010, VIC, Australia
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Trevor Lithgow;
Trevor Lithgow
1
‡Department of Biochemistry and Molecular Biology, University of Melbourne, Parkville 3010, VIC, Australia
§Bio21 Molecular Science and Biotechnology Institute, Parkville 3010, VIC, Australia
1Correspondence may be addressed to either of these authors (email tokatlid@imbb.forth.gr or t.lithgow@unimelb.edu.au).
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Kostas Tokatlidis
Kostas Tokatlidis
1
*Institute of Molecular Biology and Biotechnology, Foundation of Research and Technology Hellas, PO Box 1385, 71110 Heraklion, Crete, Greece
∥Department of Materials Science and Technology, University of Crete, PO Box 2208, 71003 Heraklion, Crete, Greece
1Correspondence may be addressed to either of these authors (email tokatlid@imbb.forth.gr or t.lithgow@unimelb.edu.au).
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Publisher: Portland Press Ltd
Received:
July 05 2007
Revision Received:
September 07 2007
Accepted:
September 26 2007
Accepted Manuscript online:
September 26 2007
Online ISSN: 1470-8728
Print ISSN: 0264-6021
© The Authors Journal compilation © 2008 Biochemical Society
2008
Biochem J (2008) 409 (2): 377–387.
Article history
Received:
July 05 2007
Revision Received:
September 07 2007
Accepted:
September 26 2007
Accepted Manuscript online:
September 26 2007
Citation
Felicity H. Alcock, J. Günter Grossmann, Ian E. Gentle, Vladimir A. Likić, Trevor Lithgow, Kostas Tokatlidis; Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space. Biochem J 15 January 2008; 409 (2): 377–387. doi: https://doi.org/10.1042/BJ20070877
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