Smc5/6’s multifaceted DNA binding capacities stabilize branched DNA structures

Jeremy T-H. Chang, Shibai Li, Emily C. Beckwitt, Thane Than, Cory Haluska, Joshua Chandanani, Michael E. O’Donnell, Xiaolan Zhao () and Shixin Liu ()
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Jeremy T-H. Chang: The Rockefeller University
Shibai Li: Memorial Sloan Kettering Cancer Center
Emily C. Beckwitt: The Rockefeller University
Thane Than: Memorial Sloan Kettering Cancer Center
Cory Haluska: Memorial Sloan Kettering Cancer Center
Joshua Chandanani: The Rockefeller University
Michael E. O’Donnell: The Rockefeller University
Xiaolan Zhao: The Rockefeller University, Weill Cornell Medical College, and Memorial Sloan Kettering Cancer Center
Shixin Liu: The Rockefeller University

Nature Communications, 2022, vol. 13, issue 1, 1-11

Abstract: Abstract Smc5/6 is an evolutionarily conserved SMC complex with roles in DNA replication and repair, as well as in viral DNA restriction. Understanding its multiple functions has been hampered by a lack of mechanistic studies on how the Smc5/6 complex associates with different types of DNA. Here we address this question by simultaneously visualizing the behavior of Smc5/6 on three types of DNA, namely double-stranded (ds) DNA, single-stranded (ss) DNA, and junction DNA formed by juxtaposed ss- and dsDNA, using correlative single-molecule fluorescence and force microscopy. We find that Smc5/6 displays distinct behaviors toward different types of DNA, dynamically associating with dsDNA while stably binding to junction DNA. Mechanistically, both the Nse1-3-4 subcomplex and ATP binding enhance the complex’s dsDNA association. In contrast, Smc5/6’s assembly onto ssDNA emanating from junction DNA, which occurs even in the presence high-affinity ssDNA binders, is aided by Nse1-3-4, but not by ATP. Moreover, we show that Smc5/6 protects junction DNA stability by preventing ssDNA annealing. The multifaceted DNA association behaviors of Smc5/6 provide a framework for understanding its diverse functions in genome maintenance and viral DNA restriction.

Date: 2022
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DOI: 10.1038/s41467-022-34928-9

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