Prion-like Aggregation of Mitochondrial Antiviral Signaling Protein in Lupus Patients Is Associated With Increased Levels of Type I Interferon

Arthritis Rheumatol. 2016 Nov;68(11):2697-2707. doi: 10.1002/art.39733.

Abstract

Objective: Increased levels of type I interferon (IFN) and type I IFN-regulated genes are found in patients with systemic lupus erythematosus (SLE) and may be central to its pathogenesis. Mitochondrial antiviral signaling protein (MAVS) is a key regulator of type I IFN that undergoes a dramatic prion-like aggregation and self propagates the activation signal from viral RNA to amplify downstream IFN production. We undertook this study to determine whether such MAVS aggregates might play a role in the sustained increased production of type I IFN in SLE.

Methods: Peripheral blood mononuclear cells were isolated and mitochondrial extracts were prepared. MAVS aggregation was detected by semidenatured agarose gel electrophoresis and confirmed by immunofluorescence staining. MAVS-associated signaling proteins were analyzed by Western blotting. MAVS aggregation-associated gene expression signature was analyzed by microarray.

Results: In blood cells from 22 of 67 SLE patients, essentially all MAVS was in a high molecular weight aggregated form. None of 6 rheumatoid arthritis patients and only 3 of 33 healthy controls had abnormal MAVS. Compared to MAVS aggregate-negative patients, MAVS aggregate-positive SLE patients had significantly higher serum levels of IFNβ and significantly increased levels of autoantibodies against Sm and U1 RNP. Gene array data revealed a characteristic gene expression pattern in these patients, with altered expression of genes involved in IFN signaling and membrane trafficking.

Conclusion: Persistent MAVS aggregates may lead to increased type I IFN production and result in unmitigated signals leading to autoimmunity.

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Adult
  • Antibodies, Antinuclear / immunology
  • Arthritis, Rheumatoid / immunology
  • Arthritis, Rheumatoid / metabolism
  • Autoantibodies / immunology
  • Blotting, Western
  • Case-Control Studies
  • Female
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Interferon Type I / immunology
  • Interferon Type I / metabolism*
  • Interferon-beta / immunology
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism*
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology
  • Lupus Erythematosus, Systemic / metabolism*
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Proteins / genetics
  • Middle Aged
  • Mitochondrial Proteins / genetics
  • Protein Aggregation, Pathological / immunology
  • Protein Aggregation, Pathological / metabolism*
  • Receptors, Complement / genetics
  • Ribonucleoprotein, U1 Small Nuclear / immunology
  • Tissue Array Analysis
  • Transcriptome
  • Ubiquitin-Protein Ligases / genetics
  • snRNP Core Proteins / immunology

Substances

  • Adaptor Proteins, Signal Transducing
  • Antibodies, Antinuclear
  • Autoantibodies
  • Intercellular Signaling Peptides and Proteins
  • Interferon Type I
  • MAVS protein, human
  • Membrane Glycoproteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • NLRC3 protein, human
  • NLRX1 protein, human
  • Receptors, Complement
  • Ribonucleoprotein, U1 Small Nuclear
  • complement 1q receptor
  • snRNP Core Proteins
  • Interferon-beta
  • MARCHF5 protein, human
  • Ubiquitin-Protein Ligases