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Smc5/6 functions with Sgs1-Top3-Rmi1 to complete chromosome replication at natural pause sites

Author

Listed:
  • Sumedha Agashe

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Chinnu Rose Joseph

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Teresa Anne Clarisse Reyes

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Demis Menolfi

    (IFOM, the FIRC Institute of Molecular Oncology
    Columbia University)

  • Michele Giannattasio

    (IFOM, the FIRC Institute of Molecular Oncology
    Università degli Studi di Milano)

  • Anja Waizenegger

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Barnabas Szakal

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Dana Branzei

    (IFOM, the FIRC Institute of Molecular Oncology
    Consiglio Nazionale delle Ricerche (IGM-CNR))

Abstract

Smc5/6 is essential for genome structural integrity by yet unknown mechanisms. Here we find that Smc5/6 co-localizes with the DNA crossed-strand processing complex Sgs1-Top3-Rmi1 (STR) at genomic regions known as natural pausing sites (NPSs) where it facilitates Top3 retention. Individual depletions of STR subunits and Smc5/6 cause similar accumulation of joint molecules (JMs) composed of reversed forks, double Holliday Junctions and hemicatenanes, indicative of Smc5/6 regulating Sgs1 and Top3 DNA processing activities. We isolate an intra-allelic suppressor of smc6-56 proficient in Top3 retention but affected in pathways that act complementarily with Sgs1 and Top3 to resolve JMs arising at replication termination. Upon replication stress, the smc6-56 suppressor requires STR and Mus81-Mms4 functions for recovery, but not Srs2 and Mph1 helicases that prevent maturation of recombination intermediates. Thus, Smc5/6 functions jointly with Top3 and STR to mediate replication completion and influences the function of other DNA crossed-strand processing enzymes at NPSs.

Suggested Citation

  • Sumedha Agashe & Chinnu Rose Joseph & Teresa Anne Clarisse Reyes & Demis Menolfi & Michele Giannattasio & Anja Waizenegger & Barnabas Szakal & Dana Branzei, 2021. "Smc5/6 functions with Sgs1-Top3-Rmi1 to complete chromosome replication at natural pause sites," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-22217-w
    DOI: 10.1038/s41467-021-22217-w
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    Cited by:

    1. Chinnu Rose Joseph & Sabrina Dusi & Michele Giannattasio & Dana Branzei, 2022. "Rad51-mediated replication of damaged templates relies on monoSUMOylated DDK kinase," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Laura J. Grange & John J. Reynolds & Farid Ullah & Bertrand Isidor & Robert F. Shearer & Xenia Latypova & Ryan M. Baxley & Antony W. Oliver & Anil Ganesh & Sophie L. Cooke & Satpal S. Jhujh & Gavin S., 2022. "Pathogenic variants in SLF2 and SMC5 cause segmented chromosomes and mosaic variegated hyperploidy," Nature Communications, Nature, vol. 13(1), pages 1-22, December.

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