MicroRNA mimics can distort physiological microRNA effects on immune checkpoints by triggering an antiviral interferon response

RNA Biol. 2022 Jan;19(1):1305-1315. doi: 10.1080/15476286.2022.2152978.

Abstract

The microRNA-200 family has wide-ranging regulatory functions in cancer development and progression. Above all, it is strongly associated with the epithelial-to-mesenchymal transition (EMT), a process during which cells change their epithelial to a mesenchymal phenotype and acquire invasive characteristics. More recently, miR-200 family members have also been reported to impact the immune evasion of cancer cells by regulating the expression of immunoinhibitory immune checkpoints (ICs) like PD-L1. Therefore, we aimed to comprehensively characterize this miR-200 family as a regulatory interface between EMT and immune evasion mechanisms in biliary tract cancer. Initial correlation analyses and transient overexpression experiments using miRNA mimics suggested miR-200c-3p as a putative regulator of ICs including PD-L1, LGALS9, and IDO1. However, these effects could not be confirmed in stable miR-200c-3p overexpression cell lines, nor in cells transiently transfected with miR-200c-3p mimic from an independent manufacturer. By shifting our efforts towards dissecting the mechanisms leading to these disparate effects, we observed that the initially used miR-200c-3p mimic triggered a double-stranded (ds)RNA-dependent antiviral response. Besides upregulating the ICs, this had substantial cellular consequences including an induction of interferon type I and type III expression, increased levels of intracellular dsRNA sensors, and a significantly altered cellular growth and apoptotic activity.Our study highlights the capability of miRNA mimics to non-specifically induce a dsRNA-mediated antiviral interferon response. Consequently, phenotypic alterations crucially distort physiological miRNA functions and might result in a major misinterpretation of previous and future miRNA studies, especially in the context of IC regulation.

Keywords: MicroRNA mimics; antiviral response; dsRNA sensing; immune checkpoints; interferons; miR-200c-3p; non-specific effects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antiviral Agents / pharmacology
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism
  • Cell Line, Tumor
  • Cell Proliferation
  • Epithelial-Mesenchymal Transition / genetics
  • Gene Expression Regulation, Neoplastic
  • Interferons / genetics
  • Interferons / metabolism
  • MicroRNAs* / metabolism

Substances

  • MicroRNAs
  • Interferons
  • B7-H1 Antigen
  • Antiviral Agents

Grants and funding

FP is supported by a research scholarship of the Austrian Society of Hematology and Medical Oncology (OeGHO). MP is supported by the Austrian Science Fund (FWF; DK-MCD W1226; Austrian Science Fund (FWF).