Periplasmic chaperone/usher machineries are used for assembly of filamentous adhesion organelles of Gram-negative pathogens in a process that has been suggested to be driven by folding energy. Structures of mutant chaperone–subunit complexes revealed a final folding transition (condensation of the subunit hydrophobic core) on the release of organelle subunit from the chaperone–subunit pre-assembly complex and incorporation into the final fibre structure. However, in view of the large interface between chaperone and subunit in the pre-assembly complex and the reported stability of this complex, it is difficult to understand how final folding could release sufficient energy to drive assembly. In the present paper, we show the X-ray structure for a native chaperone–fibre complex that, together with thermodynamic data, shows that the final folding step is indeed an essential component of the assembly process. We show that completion of the hydrophobic core and incorporation into the fibre results in an exceptionally stable module, whereas the chaperone–subunit pre-assembly complex is greatly destabilized by the high-energy conformation of the bound subunit. This difference in stabilities creates a free energy potential that drives fibre formation.
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Research Article|
July 26 2005
Resolving the energy paradox of chaperone/usher-mediated fibre assembly
Anton V. Zavialov;
Anton V. Zavialov
1
*Department of Molecular Biology, Uppsala Biomedical Center, Swedish University of Agricultural Sciences, Box 590, SE-753 24 Uppsala, Sweden
1Correspondence may be addressed to either of these authors (email anton.zavialov@molbio.slu.se or stefan.knight@molbio.slu.se).
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Vladimir M. Tischenko;
Vladimir M. Tischenko
2
†Institute of Biological Instrumentation, 142292 Pushchino, Russian Federation
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Laura J. Fooks;
Laura J. Fooks
‡Microbiology Division, School of Animal and Microbial Sciences, University of Reading, Reading RG6 6AJ, U.K.
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Bjørn O. Brandsdal;
Bjørn O. Brandsdal
3
§Department of Cell and Molecular Biology, Uppsala Biomedical Center, Uppsala University, Box 596, SE-751 24 Uppsala, Sweden
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Johan Åqvist;
Johan Åqvist
§Department of Cell and Molecular Biology, Uppsala Biomedical Center, Uppsala University, Box 596, SE-751 24 Uppsala, Sweden
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Vladimir P. Zav'yalov;
Vladimir P. Zav'yalov
∥Department of Molecular and Microbial Biology, George Mason University Manassas, VA 20110, U.S.A.
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Sheila Macintyre;
Sheila Macintyre
‡Microbiology Division, School of Animal and Microbial Sciences, University of Reading, Reading RG6 6AJ, U.K.
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Stefan D. Knight
Stefan D. Knight
1
*Department of Molecular Biology, Uppsala Biomedical Center, Swedish University of Agricultural Sciences, Box 590, SE-753 24 Uppsala, Sweden
1Correspondence may be addressed to either of these authors (email anton.zavialov@molbio.slu.se or stefan.knight@molbio.slu.se).
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Publisher: Portland Press Ltd
Received:
March 11 2005
Accepted:
March 31 2005
Accepted Manuscript online:
March 31 2005
Online ISSN: 1470-8728
Print ISSN: 0264-6021
The Biochemical Society, London
2005
Biochem J (2005) 389 (3): 685–694.
Article history
Received:
March 11 2005
Accepted:
March 31 2005
Accepted Manuscript online:
March 31 2005
Citation
Anton V. Zavialov, Vladimir M. Tischenko, Laura J. Fooks, Bjørn O. Brandsdal, Johan Åqvist, Vladimir P. Zav'yalov, Sheila Macintyre, Stefan D. Knight; Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem J 1 August 2005; 389 (3): 685–694. doi: https://doi.org/10.1042/BJ20050426
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