Requirement of Mucosa-Associated Lymphoid Tissue Lymphoma Translocation Protein 1 Protease Activity for Fcγ Receptor-Induced Arthritis, but Not Fcγ Receptor-Mediated Platelet Elimination, in Mice

Arthritis Rheumatol. 2020 Jun;72(6):919-930. doi: 10.1002/art.41204. Epub 2020 Apr 26.

Abstract

Objective: Fcγ receptors (FcγR) play important roles in both protective and pathogenic immune responses. The assembly of the CBM signalosome encompassing caspase recruitment domain-containing protein 9, B cell CLL/lymphoma 10, and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1) is required for optimal FcγR-induced canonical NF-κB activation and proinflammatory cytokine release. This study was undertaken to clarify the relevance of MALT-1 protease activity in FcγR-driven events and evaluate the therapeutic potential of selective MALT-1 protease inhibitors in FcγR-mediated diseases.

Methods: Using genetic and pharmacologic disruption of MALT-1 scaffolding and enzymatic activity, we assessed the relevance of MALT-1 function in murine and human primary myeloid cells upon stimulation with immune complexes (ICs) and in murine models of autoantibody-driven arthritis and immune thrombocytopenic purpura (ITP).

Results: MALT-1 protease function is essential for optimal FcγR-induced production of proinflammatory cytokines by various murine and human myeloid cells stimulated with ICs. In contrast, MALT-1 protease inhibition did not affect the Syk-dependent, FcγR-mediated production of reactive oxygen species or leukotriene B4 . Notably, pharmacologic MALT-1 protease inhibition in vivo reduced joint inflammation in the murine K/BxN serum-induced arthritis model (mean area under the curve for paw swelling of 45.42% versus 100% in control mice; P = 0.0007) but did not affect platelet depletion in a passive model of ITP.

Conclusion: Our findings indicate a specific contribution of MALT-1 protease activity to FcγR-mediated events and suggest that MALT-1 protease inhibitors have therapeutic potential in a subset of FcγR-driven inflammatory disorders.

MeSH terms

  • Animals
  • Antigen-Antibody Complex / metabolism
  • Arthritis, Experimental / immunology*
  • Arthritis, Rheumatoid / immunology*
  • Blood Platelets / metabolism
  • Cytokines / immunology
  • Disease Models, Animal
  • Humans
  • Mice
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / immunology*
  • Myeloid Cells / metabolism
  • Receptors, IgG / immunology*

Substances

  • Antigen-Antibody Complex
  • Cytokines
  • Receptors, IgG
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein