Clonal circulating tumor cell mobilization following chimeric antigen receptor T-cell therapy in metastatic castration-resistant prostate cancer
Abstract
Abstract Background Metastatic castration-resistant prostate cancer (mCRPC) is an aggressive, treatment-refractory stage of disease with limited treatment options and poor prognosis. Chimeric antigen receptor (CAR)-T cell therapy has demonstrated success in hematological malignancies. However, responses in solid tumors remain variable, underscoring the need for improved real-time monitoring of tumor biology and therapeutic response. Methods In this exploratory, retrospective analysis within a CAR-T clinical trial (NCT03873805), we characterized the circulatory tumor landscape of mCRPC using a high-resolution, single-cell, enrichment-free liquid biopsy platform integrating phenotypic and genomic profiling of circulating tumor cells (CTCs) and other rare cells. Longitudinal peripheral blood (PB) and bone marrow aspirate (BMA) samples were collected from eight patients (four clinical responders, four non-responders) before lymphodepletion (LD), before infusion, and after therapy. Fluorescent whole-slide imaging was used to identify rare cell phenotypes, and single-cell whole-genome copy-number variation profiling was performed to assess clonal identity. Results LD mobilized CTCs from bone marrow into PB, altering compartmental cellularity regardless of response. Single-cell genomic analysis identified clonally altered CTC populations with response-aligned dynamics: responders demonstrated post-infusion clonal reduction, whereas non-responders exhibited persistence across time points and compartments. Clonal tumor populations frequently spanned epithelial and immune-like CTC phenotypes, indicating phenotypic heterogeneity within shared lineages. Conclusions This proof-of-concept study demonstrates the feasibility of longitudinal, enrichment-free single-cell liquid biopsy to monitor clonal heterogeneity, compartmental redistribution, and treatment-associated cellular dynamics during CAR-T therapy in mCRPC.