Adrenocortical carcinoma (ACC) is an aggressive cancer with a poor prognosis. Mitotane,
the only FDA-approved treatment for ACC, targets adrenocortical cells and reduces
cortisol levels. Although it remains the cornerstone of systemic therapy, its overall
impact on long-term outcomes is still a matter of ongoing clinical debate. Drug repurposing
is a cost-effective way to identify new therapies, and defactinib, currently in clinical
trials as part of combination therapies for various solid tumours, may enhance ACC
treatment. We aimed to assess its efficacy in combination with mitotane. We tested
the combination of mitotane and defactinib in H295R, SW13, and mitotane-sensitive
and -resistant HAC15 cells, using functional assays, transcriptomic profiling, 2D
and 3D cultures, bioprinted tissues, and xenografts. We assessed drug interactions
with NMR and toxicity in vivo, as mitotane and defactinib have never been previously
administered together. Genomic data from 228 human ACC and 158 normal adrenal samples
were also analysed. Transcriptomic analysis revealed dysregulation of focal adhesion
along with mitotane-related pathways. Focal adhesion kinase (FAK) signalling was enhanced
in ACC compared to normal adrenal glands, with PTK2 (encoding FAK) upregulated in
44% of tumour samples due to copy number alterations. High FAK signature scores correlated
with worse survival outcomes. FAK inhibition by defactinib, both alone and in combination
with mitotane, showed effective anti-tumour activity in vitro. No toxicity or drug—drug
interactions were observed in vivo. Combination treatment significantly reduced tumour
volume and the number of macrometastases compared to those in the mitotane and control
groups, with defactinib-treated tumours showing increased necrosis in xenografts.
Defactinib combined with conventionally used mitotane shows promise as a novel combination
therapy for ACC and warrants further investigation.