Swatler, Puccio, et al. used scRNsSeq and flow cytometry to define Treg subsets and analyze heterogeneity and TCR overlap across tissues from 9 tumor types. A common intratumoral Treg signature of 88 genes was defined, and four Treg subsets were further resolved (CCR7+ quiescent; CCR8+ effector; CD161+ Th17-like; intermediate lacking strong functional markers). In NSCLC, CCR8+ effector abundance correlated negatively, and CD161+ Th17-like abundance correlated positively with relapse-free survival. CCR8+ Tregs showed strong tumor localization with clonotype expansion, strong overlap with Tregs in dLN, and some overlap with normal adjacent tissue Tregs and intratumoral Tconv.

Contributed by Ed Fritsch

ABSTRACT: CD4+CD25+FOXP3+ regulatory T cells (Treg) are highly activated in tumors and promote disease progression. Specific, universal targeting of these effector Treg cells is limited by the lack of a conserved signature across human cancers and information on their origin. Here we combine analysis of single-cell RNA-sequencing datasets with spectral flow cytometry and identify a core signature of 88 genes consistently upregulated in intratumoral Treg cells among 9 epithelial cancers. We describe 4 Treg cell subsets – CCR7+ quiescent, CCR8+ effector, CD161+ and intermediate, with distinct tissue distribution, function, differentiation trajectories and molecular drivers. By single-cell T cell receptor sequencing, we observe that protumoral, effector CCR8+ Treg cells exhibit little clonal relationship with other Treg cell subsets inside tumors, but are clonally related to Treg cells in tumor-draining lymph nodes, as well as conventional T cells in tumors. This resource provides insights for development and fine-tuning of CCR8+ Treg cell-targeting therapies in cancer.

Author Info: 1-IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy. 2- Institute of Genetic and Biomedical Research, UoS Milan, National Research Council, Rozzano, Milan, Italy. 3- Departm ent of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy. 4- Discovery Biology, Bristol Myers Squibb Company, Redwood City, California, CA, USA. 5- These authors contributed equally: Julian Swatler, Simone Puccio. e-mail: julian.swatler@humanitasresearch.it; enrico.lugli@humanitasresearch.it