Single-cell landscape of peripheral immune response in patients with anti-melanoma differentiation-associated gene 5 dermatomyositis

Rheumatology (Oxford). 2024 Aug 1;63(8):2284-2294. doi: 10.1093/rheumatology/kead597.

Abstract

Objective: Anti-melanoma differentiation-associated gene 5 (Anti-MDA5)-positive DM is a rare but life-threatening autoimmune disorder that is associated with a high risk of developing rapidly progressive interstitial lung disease. Current empirical therapies offer limited benefit in terms of patient survival, as little is known about the aetiology of anti-MDA5 DM. To best understand its immune landscape, we applied single-cell RNA sequencing (scRNA-seq) to peripheral blood samples from DM patients and healthy controls.

Methods: Peripheral blood mononuclear cells (PBMCs) from eight DM patients (including three distinct subtypes of DM) and two healthy donors were sequenced using the 10X Genomics platform. Additional scRNA-seq data for four healthy donors were incorporated for further bioinformatic analysis.

Results: Aberrantly increased proportions of CD14+ monocytes and plasma cells were observed in anti-MDA5 DM PBMC samples. Moreover, we found an overactivated type I IFN response and antiviral immunity in both innate and adaptive immune cells derived from anti-MDA5 DM patients that was positively correlated with disease severity. Importantly, a unique subset of CD14+ monocytes that highly expressed IFN alpha-inducible protein 27 (IFI27), a biomarker for viral infection, and IFN induced with helicase C domain 1 (IFIH1, which encodes MDA5) was specifically identified in anti-MDA5 DM samples for the first time.

Conclusion: Our study has illustrated the peripheral immune cell atlas of a number of DM subtypes, has provided compelling evidence for a viral infection-derived origin for anti-MDA5 DM, and has indicated potential targets for innovative therapeutic interventions.

Keywords: IFI27; MDA5; PBMC; antiviral immunity; dermatomyositis; interferon; single-cell RNA sequencing.

MeSH terms

  • Adult
  • Aged
  • Autoantibodies / blood
  • Autoantibodies / immunology
  • Case-Control Studies
  • Dermatomyositis* / blood
  • Dermatomyositis* / genetics
  • Dermatomyositis* / immunology
  • Female
  • Humans
  • Immunity, Innate
  • Interferon-Induced Helicase, IFIH1* / genetics
  • Interferon-Induced Helicase, IFIH1* / immunology
  • Leukocytes, Mononuclear* / immunology
  • Leukocytes, Mononuclear* / metabolism
  • Lipopolysaccharide Receptors
  • Male
  • Middle Aged
  • Monocytes / immunology
  • Plasma Cells / immunology
  • Single-Cell Analysis*

Substances

  • Interferon-Induced Helicase, IFIH1
  • IFIH1 protein, human
  • Lipopolysaccharide Receptors
  • Autoantibodies