From:  Targeting tumor transition windows

 Tumor transition phases during therapy: biological features, biomarkers, and therapeutic implications.

Transition phaseBiological featuresRepresentative mechanismsCandidate biomarkers and readoutsTherapeutic implications
Therapy-impact phase (early shock response)Acute treatment response; rapid stress signaling; apoptosis in sensitive fraction; early survival programs in a subset [219]DNA damage response; acute reactive oxygen species (ROS) surge; stress kinase activation; proteotoxic stress; early feedback rebound signaling [14]Early ctDNA drop kinetics; acute stress-response transcriptional signatures; phospho-signaling changes; imaging response dynamics (early metabolic change) [220]Identify early nonresponders; exploit immediate stress liabilities; initiate early combinations to prevent entry into tolerance/persistence [14, 220]
Plasticity phaseIncreased phenotypic flexibility; reversible identity shifts; stem-like or slow-cycling programs; lineage instability [38, 174]Transcriptional reprogramming; EMT/MET-like programs; lineage switching; chromatin remodeling; enhancer reconfiguration [221, 222]Single-cell state shifts (scRNA-seq); chromatin accessibility dynamics (scATAC-seq); stemness/lineage signatures; enhancer activity patterns; methylation-based state signatures [139, 221]Limit state exploration; target regulators of reprogramming; prioritize interventions that reduce plasticity and prevent commitment into resistant phenotypes [38, 221]
Persistence phase (drug-tolerant persisters)Small surviving subpopulation; reversible tolerance; quiescent/slow-cycling behavior; minimal-residual-like state; stress-adapted phenotype [12, 84]Epigenetic adaptation; altered proteostasis/UPR; metabolic rewiring; survival pathway dependence; anti-apoptotic programs [18, 223]Detection of rare tolerant states by single-cell profiling; minimal residual disease signals; stress-response expression programs; survival pathway activation profiles; longitudinal ctDNA plateau/slow clearance [84, 220]Target persister dependencies; combine tolerability-targeting with vulnerability targeting; prevent persisters from serving as reservoirs for stable resistance [13, 14]
Vulnerability phase (adaptive fragility)Transitional fragility during reorganization; narrow pathway dependence; high stress burden; incomplete compensatory programs [218]Therapy-induced metabolic stress; signaling rewiring; proteotoxic stress; heightened DNA repair reliance; collateral sensitivity; treatment-induced synthetic lethality [223, 224]Metabolic stress indicators; ROS/redox markers; UPR signatures; dynamic phospho-signaling profiles; DNA repair activation signatures; imaging of hypoxia/metabolic shifts; ctDNA rebound kinetics suggesting adaptation [220, 223]Best window for timed sequential/combination therapy; exploit newly essential pathways; target stress handling, repair dependencies, or compensatory signaling nodes before stabilization [14, 218]
Microenvironmental remodeling phaseTherapy-altered ecology; inflammatory signaling shifts; stromal/immune remodeling; niche support for survival states; spatial heterogeneity of response [225]Hypoxia-driven programs; cytokine signaling; cancer-associated fibroblast (CAF)-mediated protection; immune editing; therapy-induced inflammation; altered vascular/ECM dynamics [226]Spatial imaging changes (perfusion/hypoxia); cytokine/chemokine profiles; immune infiltration signatures; stromal activation markers; spatial transcriptomics readouts [225, 227]Combine tumor-cell targeting with microenvironment-directed strategies; prevent niche-assisted persistence and resistance stabilization; guide region-specific interventions [228, 229]
Stabilization phase (durable resistance)Consolidation of resistant phenotype; reduced reversibility; dominance of resistant clones; stable resistant transcriptional state [171, 230]Secondary target mutations; pathway reactivation mutations; gene amplification; bypass pathway activation; epigenetic “locking”; clonal selection and expansion [151, 231]Resistance mutations in ctDNA; clonal expansion signatures; stable epigenetic/transcriptional resistance programs; persistent imaging evidence of nonresponse; multi-omic confirmation of resistant state [171, 230]Transition windows narrow; resistance becomes durable; requires switching strategies/targets; supports early interception during plasticity/vulnerability phases to delay or prevent stabilization [13, 151]

ctDNA: circulating tumor deoxyribonucleic acid; ECM: extracellular matrix; EMT: epithelial-mesenchymal transition; MET: mesenchymal-epithelial transition; scATAC-seq: single-cell assay for transposase-accessible chromatin using sequencing; scRNA-seq: single-cell ribonucleic acid sequencing; UPR: unfolded protein response.