Frontiers in Oncology
Autophagy as an adaptive resistance mechanism to epigenetic therapy in cancer
By Natalie L. Hakim, John Thomas Gialluisi, Sruthi Sureshkumar and 5 others.
Abstract
Epigenetic therapies can reverse malignant transcriptional programs, but their activity is often constrained by adaptive stress responses that allow cancer cells to survive and recover. Autophagy is a central component of this adaptation. By sustaining metabolic homeostasis, mitochondrial fitness, proteostasis, and lysosomal recycling, autophagy can buffer the cellular injury produced by inhibitors of DNA methyltransferases, histone deacetylases, and bromodomain proteins. These observations provide a strong rationale for combining epigenetic therapies with autophagy inhibition. However, the field has too often equated autophagosome accumulation with increased autophagic flux and treatment-induced autophagy with a functional dependency. Moreover, the lysosomotropic agents used in early clinical studies incompletely inhibit autophagy and exert broader effects on lysosomal biology. Consequently, compelling preclinical activity has not translated into consistent clinical benefit. Here, we critically evaluate the mechanisms through which epigenetic therapies engage autophagy, distinguish correlative markers from causal evidence of resistance, and assess the preclinical and clinical data supporting combination strategies. We also define the major barriers to translation, including inadequate pharmacodynamic assays, a lack of predictive biomarkers, context-dependent effects on tumor and immune cells, and the limited potency and selectivity of current autophagy inhibitors. Defining when, where, and how autophagy becomes a targetable dependency will be essential to translate this compelling biology into an effective precision treatment.



