Longitudinal multi-functional analysis identified responses of T cells, B cells, and monocytes as hallmarks of immunotherapy tolerance in patients with merkel cell carcinoma

PLoS One. 2023 Nov 20;18(11):e0293922. doi: 10.1371/journal.pone.0293922. eCollection 2023.

Abstract

Purpose: Merkel cell carcinoma (MCC) is a neuroendocrine carcinoma originating in the skin. Studies are needed to determine the mechanisms of immune escape in patients with MCC, and malignant cell conditions that promote immune evasion.

Methods: We used Single-cell RNA sequencing (scRNA-seq) to determine cellular features associated with MCC disease trajectory. A longitudinal multi-omics study was performed using scRNA-seq data of peripheral blood harvested from four-time points. Six major cell types and fifteen cell subgroups were identified and confirmed their presence by expression of characteristic markers. The expression patterns and specific changes of different cells at different time points were investigated. Subsequently, bulk RNA data was used to validate key findings.

Results: The dynamic characteristics of the cells were identified during the critical period between benign improvement and acquisition of resistance. Combined with the results of the validation cohort, the resistance program expressed in the relapse stage is mainly associated with T cell exhaustion and immune cell crosstalk disorder. Coinciding with immune escape, we also identified a decrease non-classical monocytes and an expansion of classical monocytes with features of high inflammation and immune deficiency.

Conclusion: Changes in cellular status, such as depletion of T cells and dysregulation of B cell proliferation and differentiation, may lead to drug resistance in MCC patients. Meanwhile, the widespread decreased antigen presentation ability and immune disorders caused by deletion of MHC class II gene expression should not be ignored.

MeSH terms

  • Carcinoma, Merkel Cell* / genetics
  • Carcinoma, Merkel Cell* / pathology
  • Humans
  • Immunotherapy / methods
  • Monocytes / pathology
  • Skin Neoplasms* / pathology
  • T-Lymphocytes

Grants and funding

This study was funded by the 2021 Special Fund for Science and Technology Innovation Strategy of Guangdong Province [grant number pdjh2021b0120]; 2020 National Innovation and Entrepreneurship Program for Chinese College Students [grant number 202010572017]; and the 2020 Guangzhou University of Chinese Medicine College Student Innovation and Entrepreneurship Project [grant number 202010572201]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.