Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates

Timely removal of DNA recombination intermediates is critical for genome stability. The DNA helicase-topoisomerase complex, Sgs1-Top3-Rmi1 (STR), is the major pathway for processing these intermediates to generate conservative products. However, the mechanisms that promote STR-mediated functions rem...

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Main Authors: Jaclyn N. Bonner, Koyi Choi, Xiaoyu Xue, Nikko P. Torres, Barnabas Szakal, Lei Wei, Bingbing Wan, Meret Arter, Joao Matos, Patrick Sung, Grant W. Brown, Dana Branzei, Xiaolan Zhao
Format: Article
Language:English
Published: Elsevier 2016-07-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124716307409
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spelling doaj-603817206fe94d348474bc7447aa4ea42020-11-25T01:11:33ZengElsevierCell Reports2211-12472016-07-0116236837810.1016/j.celrep.2016.06.015Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination IntermediatesJaclyn N. Bonner0Koyi Choi1Xiaoyu Xue2Nikko P. Torres3Barnabas Szakal4Lei Wei5Bingbing Wan6Meret Arter7Joao Matos8Patrick Sung9Grant W. Brown10Dana Branzei11Xiaolan Zhao12Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USAMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USADepartment of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT 06520, USADonnelly Centre and Department of Biochemistry, University of Toronto, Toronto, ON M5S 3E1, CanadaIFOM, The FIRC of Molecular Oncology, Via Adamello 16, 20139, Milan, ItalyMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USAMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USAInstitute of Biochemistry, Swiss Federal Institute of Technology in Zürich, Otto-Stern-Weg 3, 8093 Zürich, SwitzerlandInstitute of Biochemistry, Swiss Federal Institute of Technology in Zürich, Otto-Stern-Weg 3, 8093 Zürich, SwitzerlandDepartment of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT 06520, USADonnelly Centre and Department of Biochemistry, University of Toronto, Toronto, ON M5S 3E1, CanadaIFOM, The FIRC of Molecular Oncology, Via Adamello 16, 20139, Milan, ItalyMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USATimely removal of DNA recombination intermediates is critical for genome stability. The DNA helicase-topoisomerase complex, Sgs1-Top3-Rmi1 (STR), is the major pathway for processing these intermediates to generate conservative products. However, the mechanisms that promote STR-mediated functions remain to be defined. Here we show that Sgs1 binds to poly-SUMO chains and associates with the Smc5/6 SUMO E3 complex in yeast. Moreover, these interactions contribute to the sumoylation of Sgs1, Top3, and Rmi1 upon the generation of recombination structures. We show that reduced STR sumoylation leads to accumulation of recombination structures, and impaired growth in conditions when these structures arise frequently, highlighting the importance of STR sumoylation. Mechanistically, sumoylation promotes STR inter-subunit interactions and accumulation at DNA repair centers. These findings expand the roles of sumoylation and Smc5/6 in genome maintenance by demonstrating that they foster STR functions in the removal of recombination intermediates.http://www.sciencedirect.com/science/article/pii/S2211124716307409recombination intermediatesprotein sumoylationSmc5/6Sgs1
collection DOAJ
language English
format Article
sources DOAJ
author Jaclyn N. Bonner
Koyi Choi
Xiaoyu Xue
Nikko P. Torres
Barnabas Szakal
Lei Wei
Bingbing Wan
Meret Arter
Joao Matos
Patrick Sung
Grant W. Brown
Dana Branzei
Xiaolan Zhao
spellingShingle Jaclyn N. Bonner
Koyi Choi
Xiaoyu Xue
Nikko P. Torres
Barnabas Szakal
Lei Wei
Bingbing Wan
Meret Arter
Joao Matos
Patrick Sung
Grant W. Brown
Dana Branzei
Xiaolan Zhao
Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
Cell Reports
recombination intermediates
protein sumoylation
Smc5/6
Sgs1
author_facet Jaclyn N. Bonner
Koyi Choi
Xiaoyu Xue
Nikko P. Torres
Barnabas Szakal
Lei Wei
Bingbing Wan
Meret Arter
Joao Matos
Patrick Sung
Grant W. Brown
Dana Branzei
Xiaolan Zhao
author_sort Jaclyn N. Bonner
title Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
title_short Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
title_full Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
title_fullStr Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
title_full_unstemmed Smc5/6 Mediated Sumoylation of the Sgs1-Top3-Rmi1 Complex Promotes Removal of Recombination Intermediates
title_sort smc5/6 mediated sumoylation of the sgs1-top3-rmi1 complex promotes removal of recombination intermediates
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2016-07-01
description Timely removal of DNA recombination intermediates is critical for genome stability. The DNA helicase-topoisomerase complex, Sgs1-Top3-Rmi1 (STR), is the major pathway for processing these intermediates to generate conservative products. However, the mechanisms that promote STR-mediated functions remain to be defined. Here we show that Sgs1 binds to poly-SUMO chains and associates with the Smc5/6 SUMO E3 complex in yeast. Moreover, these interactions contribute to the sumoylation of Sgs1, Top3, and Rmi1 upon the generation of recombination structures. We show that reduced STR sumoylation leads to accumulation of recombination structures, and impaired growth in conditions when these structures arise frequently, highlighting the importance of STR sumoylation. Mechanistically, sumoylation promotes STR inter-subunit interactions and accumulation at DNA repair centers. These findings expand the roles of sumoylation and Smc5/6 in genome maintenance by demonstrating that they foster STR functions in the removal of recombination intermediates.
topic recombination intermediates
protein sumoylation
Smc5/6
Sgs1
url http://www.sciencedirect.com/science/article/pii/S2211124716307409
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