Current standard-of-care for the aggressive, triple negative breast cancer (TNBC) subtype involves preoperative drug regimens incorporating microtubule targeting agents (MTAs), a compound class that aims to inhibit cell proliferation and invasion by disrupting microtubule dynamics. However, these frontline agents ignore the finely-tuned balance that exists between the actin and microtubule cytoskeletons. Compensatory effects mediated by the actin cytoskeleton in response to MTAs have been shown to drive metastasis and drug-resistance, factors that ultimately limit the response to MTAs and likely underlie poor patient outcomes. Here, we assess whether TNBC cells can be sensitized to clinically-approved MTAs by co-targeting and disrupting actin-microtubule crosstalk.
Actomyosin complexes comprising nonmuscle myosin-2 (NM-2) motors generate the contractile forces essential for cell adhesion, migration and division, and represent an established point of crosstalk between the two cytoskeletal networks. However, the few NM-2 destabilizing compounds identified to date have shown limited anti-tumorigenic potential. Using biochemical approaches, we have now identified and characterized a commercially available small molecule that instead directly binds and activates NM-2 motors, which we refer to as Myosin-2 Motor Activator (M-2MA). Within tumour cells, M-2MA stabilizes a contractile phenotype and reduces both proliferation and invasion in a 3D setting. As a combination therapy, M-2MA exhibits strong synergistic effects with a subset of MTAs, enhancing their ability to induce apoptosis throughout the entire cell cycle.
Using M-2MA as a first-in-class molecule, we have exploited a large-scale, chemically diverse screen (Bryce et al., 2019, Cell Systems) to identify further compounds that induce similar F-actin phenotypes. Of the 39 compounds identified, 33 enhance the efficacy of clinically-approved MTAs, 10 display MTA synergy profiles consistent with M-2MA and 3 are effective at nanomolar doses. Together, these data demonstrate that disrupting cytoskeletal crosstalk may represent a powerful and viable therapeutic approach to enhance the sensitivity of tumour cells to standard-of-care treatment.