SUMO protease and proteasome recruitment at the nuclear periphery differently affect replication dynamics at arrested forks

Author:

Schirmeisen KamilaORCID,Naiman KarelORCID,Fréon KarineORCID,Besse LaetitiaORCID,Chakraborty ShrenaORCID,Carr Antony M.ORCID,Kramarz KarolORCID,Lambert Sarah AEORCID

Abstract

AbstractNuclear pores complexes (NPCs) are genome organizers, defining a particular nuclear compartment enriched for SUMO protease and proteasome activities, and acting as docking sites for DNA repair. In fission yeast, the anchorage of perturbed replication forks to NPCs is an integral part of the recombination-dependent replication restart mechanism (RDR) that resumes DNA synthesis at terminally dysfunctional forks. By mapping DNA polymerase usage, we report that SUMO protease Ulp1-associated NPCs ensure efficient initiation of restarted DNA synthesis, whereas proteasome-associated NPCs sustain the progression of restarted DNA polymerase. In contrast to Ulp1-dependent events, this last function occurs independently of SUMO chains formation. By analyzing the role of the nuclear basket, the nucleoplasmic extension of the NPC, we reveal that the activities of Ulp1 and the proteasome cannot compensate for each other and affect RDR dynamics in distinct ways. Our work probes the mechanisms by which the NPC environment ensures optimal RDR.Highlights● Ulp1-associated NPCs ensure efficient initiation of restarted DNA synthesis, in a SUMO chain-dependent manner● Proteasome-associated NPCs foster the progression of restarted DNA synthesis, in a SUMO chain-independent manner● The nucleoporin Nup60 promotes the spatial sequestration of Ulp1 at the nuclear periphery● Ulp1 and proteasome activities are differently required for optimal recombination-mediated fork restart.

Publisher

Cold Spring Harbor Laboratory

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