Immunosuppressive Traits of the Hybrid Epithelial/Mesenchymal Phenotype

Front Immunol. 2021 Dec 15:12:797261. doi: 10.3389/fimmu.2021.797261. eCollection 2021.

Abstract

Recent preclinical and clinical data suggests enhanced metastatic fitness of hybrid epithelial/mesenchymal (E/M) phenotypes, but mechanistic details regarding their survival strategies during metastasis remain unclear. Here, we investigate immune-evasive strategies of hybrid E/M states. We construct and simulate the dynamics of a minimalistic regulatory network encompassing the known associations among regulators of EMT (epithelial-mesenchymal transition) and PD-L1, an established immune-suppressor. Our simulations for the network consisting of SLUG, ZEB1, miR-200, CDH1 and PD-L1, integrated with single-cell and bulk RNA-seq data analysis, elucidate that hybrid E/M cells can have high levels of PD-L1, similar to those seen in cells with a full EMT phenotype, thus obviating the need for cancer cells to undergo a full EMT to be immune-evasive. Specifically, in breast cancer, we show the co-existence of hybrid E/M phenotypes, enhanced resistance to anti-estrogen therapy and increased PD-L1 levels. Our results underscore how the emergent dynamics of interconnected regulatory networks can coordinate different axes of cellular fitness during metastasis.

Keywords: PD-L1; epithelial- mesenchymal transition (EMT); hybrid epithelial/mesenchymal; immune evasion; multistability.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Antineoplastic Agents, Hormonal / therapeutic use
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / immunology*
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cadherins / genetics
  • Cadherins / metabolism
  • Computer Simulation
  • Drug Resistance, Neoplasm
  • Epithelial-Mesenchymal Transition / immunology*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Gene Regulatory Networks
  • Humans
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Models, Biological
  • Neoplasm Metastasis
  • Phenotype
  • Signal Transduction
  • Snail Family Transcription Factors / genetics
  • Snail Family Transcription Factors / metabolism
  • Tamoxifen / therapeutic use
  • Tumor Escape / immunology*
  • Tumor Microenvironment / immunology*
  • Zinc Finger E-box-Binding Homeobox 1 / genetics
  • Zinc Finger E-box-Binding Homeobox 1 / metabolism

Substances

  • Antigens, CD
  • Antineoplastic Agents, Hormonal
  • B7-H1 Antigen
  • CD274 protein, human
  • CDH1 protein, human
  • Cadherins
  • MIRN200 microRNA, human
  • MicroRNAs
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • ZEB1 protein, human
  • Zinc Finger E-box-Binding Homeobox 1
  • Tamoxifen