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Solution X-ray scattering combined with computational modeling reveals multiple conformations of covalently bound ubiquitin on PCNA
Journal article   Open access   Peer reviewed

Solution X-ray scattering combined with computational modeling reveals multiple conformations of covalently bound ubiquitin on PCNA

Susan E Tsutakawa, Adam W Van Wynsberghe, Bret D Freudenthal, Christopher P Weinacht, Lokesh Gakhar, M Todd Washington, Zhihao Zhuang, John A Tainer and Ivaylo Ivanov
Proceedings of the National Academy of Sciences - PNAS, Vol.108(43), pp.17672-17677
10/25/2011
DOI: 10.1073/pnas.1110480108
PMCID: PMC3203759
PMID: 22006297
url
https://doi.org/10.1073/pnas.1110480108View
Published (Version of record) Open Access

Abstract

PCNA ubiquitination in response to DNA damage leads to the recruitment of specialized translesion polymerases to the damage locus. This constitutes one of the initial steps in translesion synthesis (TLS)--a critical pathway for cell survival and for maintenance of genome stability. The recent crystal structure of ubiquitinated PCNA (Ub-PCNA) sheds light on the mode of association between the two proteins but also revealed that paradoxically, the ubiquitin surface engaged in PCNA interactions was the same as the surface implicated in translesion polymerase binding. This finding implied a degree of flexibility inherent in the Ub-PCNA complex that would allow it to transition into a conformation competent to bind the TLS polymerase. To address the issue of segmental flexibility, we combined multiscale computational modeling and small angle X-ray scattering. This combined strategy revealed alternative positions for ubiquitin to reside on the surface of the PCNA homotrimer, distinct from the position identified in the crystal structure. Two mutations originally identified in genetic screens and known to interfere with TLS are positioned directly beneath the bound ubiquitin in the alternative models. These computationally derived positions, in an ensemble with the crystallographic and flexible positions, provided the best fit to the solution scattering, indicating that ubiquitin dynamically associated with PCNA and is capable of transitioning between a few discrete sites on the PCNA surface. The finding of new docking sites and the positional equilibrium of PCNA-Ub occurring in solution provide unexpected insight into previously unexplained biological observations.
Macromolecular Substances - chemistry Humans Computational Biology Ubiquitin - chemistry Models, Molecular Protein Binding Scattering, Small Angle Protein Conformation Proliferating Cell Nuclear Antigen - chemistry

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