Transcriptomic profiling reveals distinct subsets of immune checkpoint inhibitor induced myositis

Ann Rheum Dis. 2023 Jun;82(6):829-836. doi: 10.1136/ard-2022-223792. Epub 2023 Feb 17.

Abstract

Objectives: Inflammatory myopathy or myositis is a heterogeneous family of immune-mediated diseases including dermatomyositis (DM), antisynthetase syndrome (AS), immune-mediated necrotising myopathy (IMNM) and inclusion body myositis (IBM). Immune checkpoint inhibitors (ICIs) can also cause myositis (ICI-myositis). This study was designed to define gene expression patterns in muscle biopsies from patients with ICI-myositis.

Methods: Bulk RNA sequencing was performed on 200 muscle biopsies (35 ICI-myositis, 44 DM, 18 AS, 54 IMNM, 16 IBM and 33 normal muscle biopsies) and single nuclei RNA sequencing was performed on 22 muscle biopsies (seven ICI-myositis, four DM, three AS, six IMNM and two IBM).

Results: Unsupervised clustering defined three distinct transcriptomic subsets of ICI-myositis: ICI-DM, ICI-MYO1 and ICI-MYO2. ICI-DM included patients with DM and anti-TIF1γ autoantibodies who, like DM patients, overexpressed type 1 interferon-inducible genes. ICI-MYO1 patients had highly inflammatory muscle biopsies and included all patients that developed coexisting myocarditis. ICI-MYO2 was composed of patients with predominant necrotising pathology and low levels of muscle inflammation. The type 2 interferon pathway was activated both in ICI-DM and ICI-MYO1. Unlike the other types of myositis, all three subsets of ICI-myositis patients overexpressed genes involved in the IL6 pathway.

Conclusions: We identified three distinct types of ICI-myositis based on transcriptomic analyses. The IL6 pathway was overexpressed in all groups, the type I interferon pathway activation was specific for ICI-DM, the type 2 IFN pathway was overexpressed in both ICI-DM and ICI-MYO1 and only ICI-MYO1 patients developed myocarditis.

Keywords: autoimmune diseases; dermatomyositis; polymyositis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Intramural

MeSH terms

  • Autoimmune Diseases* / complications
  • Dermatomyositis* / genetics
  • Humans
  • Immune Checkpoint Inhibitors
  • Interferons / genetics
  • Interleukin-6 / metabolism
  • Muscle, Skeletal / pathology
  • Myocarditis* / pathology
  • Myositis* / chemically induced
  • Myositis* / genetics
  • Myositis, Inclusion Body*
  • Transcriptome

Substances

  • Immune Checkpoint Inhibitors
  • Interleukin-6
  • Interferons

Supplementary concepts

  • Antisynthetase syndrome