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Persistent TOP1 cleavage complexes in drug-tolerant cells drive adaptive resistance to EGFR-targeted therapies in lung cancer

Mathéa Géraud, Rémi Gence, Anne Casanova, Estelle Taranchon-Clermont, Simona Salimbeni, Nesibe Özsu, Maïna Vienne, Célia Delahaye, Elodie Borrull, Amélie Lusque, Mathilde Morisseau, Thomas Filleron, Delphine Pagan, Camille Taha, Agnese Cristini, Julien Mazières, Olivier Calvayrac, Gilles Favre, Anne Pradines, Olivier Sordet

Peer-reviewed journalReal-world use

In the authors' words

Resistance to targeted cancer therapies often arises from drug-tolerant cells, which survive treatment by entering a nonproliferative state. Over time, these cells can acquire mutations that contribute to cell reproliferation, but how nonproliferating drug-tolerant cells accumulate these mutations remains unclear. Here, we show that EGFR inhibition in EGFR -mutated lung cancer transiently down-regulates tyrosyl-DNA phosphodiesterase 1 (TDP1), a repair enzyme that resolves abortive topoisomerase I cleavage complexes (TOP1ccs). In drug-tolerant cells, elevated reactive oxygen species promote TOP1cc trapping, while TDP1 down-regulation impairs their repair, driving TOP1cc accumulation, resistance mutation acquisition, and cell reproliferation. We further find that TDP1 expression is absent in ∼25% of EGFR -mutated lung cancers. In TDP1-deficient cells, combining EGFR inhibition with a sublethal concentration of topotecan, which further increases TOP1ccs, abolishes cell reproliferation. Together, these findings establish persistent TOP1cc accumulation as a driver of therapy-induced mutagenesis linking drug tolerance to adaptive resistance and reveal TDP1 loss as a targetable vulnerability in EGFR-mutated lung cancers.

Main resultThe abstract does not state a limitation.

Appeared: Friday, September 25. Science Advances. Peer-reviewed journal.

DOI: 10.1126/sciadv.aeh9099