Replication stress is the main driver of genome instability in early cancer development and is recognized as a hallmark of cancer. Actin is a cytoskeletal protein that polymerizes from monomeric to filamentous form (F-actin) to provide cells with mechanical support, transport pathways, and a driving force for movement. While actin is traditionally considered a cytoplasmic protein, nuclear actin polymerization was recently identified to contribute to double strand break repair.
Here we used a suite of imaging tools to identify that nuclear F-actin plays a prominent role in the replication stress response in human cells. Consistent with replication stress, live and fixed imaging assays revealed that pharmacological inhibition of actin polymerization resulted in S-phase elongation, altered replication dynamics, and chromosome segregation errors. Using live and super resolution imaging we also found that replication stress resulted in ATR, IPMK and mTOR-dependent nuclear F-actin, which altered nuclear architecture by promoting nuclear ellipticity and expanding the nuclear volume to counteract membrane deformation induced by replication stress. Additionally, we developed novel analytical tools for live cell-imaging that revealed nuclear F-actin promoted the mobility of stalled replication foci within the nuclear volume. This incresed motility included the directed movement of stalled replication foci along actin fibres to the nuclear periphery. Inhibiting ATR, mTOR or actin polymerization, suppressed F-actin dependent alteration of nuclear architecture in response to replication stress and prevented the restart of stalled replication forks. Finally, inhibiting actin polymerization slowed resolution of ATR-dependent DNA damage response signalling in response to replication stress.
Cumulatively, these data reveal a novel pathway regulated by ATR and mTOR, where F-actin dependent forces shape nuclear architecture in response to replication stress to maintain genome stability. A current pre-print of the manuscript describing these data is availble on bioRxiv at: https://doi.org/10.1101/451708