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Nucleic Acids Research Advance Access published online on September 19, 2007
Nucleic Acids Research, doi:10.1093/nar/gkm705
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© 2007 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Structural Biology

Papillomavirus E1 helicase assembly maintains an asymmetric state in the absence of DNA and nucleotide cofactors

Cyril M. Sanders1, Oleg V. Kovalevskiy2,3, Dmytro Sizov3,4, Andrey A. Lebedev3, Michail N. Isupov5 and Alfred A. Antson3,*

1Institute for Cancer Studies, University of Sheffield, Beech Hill Road, Sheffield, S10 2RX, UK, 2Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region, 142290 Russia, 3York Structural Biology Laboratory, Department of Chemistry, University of York, Heslington, York, YO10 5YW, UK 4Taras Shevchenko Kiev State University, Biology Faculty, Virology Department, Glushkova Avenue 2, 03127 Kiev, Ukraine and 5Henry Wellcome Building for Biocatalysis, School of Biosciences, University of Exeter, Stocker Road, Exeter, EX4 4QD, UK

*To whom correspondence should be addressed. Tel: +44 1904328255; Fax: +44 1904328266; Email: fred{at}ysbl.york.ac.uk

Received June 19, 2007. Revised August 25, 2007. Accepted August 26, 2007.

Concerted, stochastic and sequential mechanisms of action have been proposed for different hexameric AAA+ molecular motors. Here we report the crystal structure of the E1 helicase from bovine papillomavirus, where asymmetric assembly is for the first time observed in the absence of nucleotide cofactors and DNA. Surprisingly, the ATP-binding sites adopt specific conformations linked to positional changes in the DNA-binding hairpins, which follow a wave-like trajectory, as observed previously in the E1/DNA/ADP complex. The protein's assembly thus maintains such an asymmetric state in the absence of DNA and nucleotide cofactors, allowing consideration of the E1 helicase action as the propagation of a conformational wave around the protein ring. The data imply that the wave's propagation within the AAA+ domains is not necessarily coupled with a strictly sequential hydrolysis of ATP. Since a single ATP hydrolysis event would affect the whole hexamer, such events may simply serve to rectify the direction of the wave's motion.


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C. M. Sanders
A DNA-binding activity in BPV initiator protein E1 required for melting duplex ori DNA but not processive helicase activity initiated on partially single-stranded DNA
Nucleic Acids Res., April 1, 2008; 36(6): 1891 - 1899.
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