The tumor suppressor TP53 is the most frequently mutated gene in cancer and associated to poor prognosis and chemoresistance. We have previously identified the mutant p53-targeting compound APR-246 that is currently tested in a Phase III clinical trial in myelodysplastic syndrome.
APR-246 reactivates mutant p53 to a wild type-like functional protein capable of inducing p53 downstream targets and eventually cell death. APR-246 is non-enzymatically converted to its active product methylene quinclidinone (MQ) which binds to cysteine residues in p53 and promotes refolding. APR-246 also exhibits pro-oxidant activity as MQ binds and inactivates important antioxidants such as glutathione and thioredoxin reductase, which both are essential for the cellular defense against oxidative and electrophilic stress.
Multidrug resistance protein 1 (MRP1/ABCC1) plays an important role in efflux of unconjugated and glutathione-conjugated drugs, and thereby reduces drug accumulation and enhances tumor cell resistance. As MQ readily conjugates to glutathione, we hypothesized that MRP1 could be involved in the efflux of APR-246 and/or MQ from cells. Indeed, inhibition or knockdown of MRP1 leads to intracellular 14C-accumulation after 14C- APR-246 treatment in tumor cell lines of various origin. Additionally, treatment with MRP1 inhibitors shifted intra- and extracellular thiol status. The compound accumulation and thiol status shift caused profound synergistic cell death upon combination treatment with APR-246 and MRP1 inhibition in cancer cell lines of various origins while normal fibroblasts were unaffected at similar concentrations. Missense mutant p53 expressing cell lines had the highest synergistic response. MRP1 inhibition also lowered the threshold of anti-tumor activity of APR-246 in xenograft tumor models in mice. LC-MS analysis revealed that cellular APR-246 levels were unchanged after MRP1 inhibition while MQ conjugated to glutathione (GS-MQ) accumulated. Furthermore, we showed that MQ conjugation is readily reversible which suggests that GS-MQ could serve as a drug reservoir, increasing the availability of MQ for targeting of mutant p53.