The transition from ductal carcinoma in situ (DCIS) to invasive ductal carcinoma (IDC) is an evolutionary bottleneck where progression occurs only in 30% of patients but the molecular processes marking this transition remain poorly understood. We have previously profiled the immune system in normal breast tissue, DCIS and IDC and have found increasing immunosuppression with progression, suggesting that immune escape is characteristic of the transition from DCIS to IDC.
We investigated how the immune system can shape this evolutionary trajectory by assessing matched cases of pure DCIS and recurrent IDC using whole exome sequencing, RNA sequencing, and cyclic immunofluorescence.
Phenotypic characterisation revealed similar or lower lymphocytic infiltration in IDC compared to DCIS, and a higher proportion of B cells commonly found within tertiary lymphoid structures. Topological analysis demonstrated a higher proportion of Tregs within close proximity of tumor cells in IDC, consistent with increasing immunosuppression.
Tumor genetic profiles showed that copy number aberrations are early events conserved in this transition. CNAs associated with reduced immune infiltration include 1q amplification which may occur as early as DCIS, and IDO1 amplification found predominantly in IDC. In contrast, the emergence of pathologic mutations is a constant evolutionary process under selection, with very few events common to both DCIS and IDC. Conserved mutations lying the PTEN/PIK3CA axis were predicted to be neoantigens, yet were not eliminated.
The mutational and thus neoantigen presenting landscape can be shaped by the immune system, in contrast to copy number aberrations which are more immunologically silent but can contribute to immunosuppression. Immune evasion and the unchecked acquisition of mutations is one way of overcoming this evolutionary bottleneck, leading to the emergence of invasive disease.