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

Author

Listed:
  • Jeremy T-H. Chang

    (The Rockefeller University
    The Rockefeller University, Weill Cornell Medical College, and Memorial Sloan Kettering Cancer Center)

  • 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
    Memorial Sloan Kettering Cancer Center)

  • Shixin Liu

    (The Rockefeller University
    The Rockefeller University, Weill Cornell Medical College, and Memorial Sloan Kettering Cancer Center)

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.

Suggested Citation

  • Jeremy T-H. Chang & Shibai Li & Emily C. Beckwitt & Thane Than & Cory Haluska & Joshua Chandanani & Michael E. O’Donnell & Xiaolan Zhao & Shixin Liu, 2022. "Smc5/6’s multifaceted DNA binding capacities stabilize branched DNA structures," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34928-9
    DOI: 10.1038/s41467-022-34928-9
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    References listed on IDEAS

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    1. Aaron Alt & Hung Q. Dang & Owen S. Wells & Luis M. Polo & Matt A. Smith & Grant A. McGregor & Thomas Welte & Alan R. Lehmann & Laurence H. Pearl & Johanne M. Murray & Antony W. Oliver, 2017. "Specialized interfaces of Smc5/6 control hinge stability and DNA association," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
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