Recessive NLRC4-autoinflammatory disease reveals an ulcerative colitis locus

Annemarie Steiner, Thomas Reygaerts, Alessandra Pontillo, Isabella Ceccherini, Jonas Moecking, Fiona Moghaddas, Sophia Davidson, Francesco Caroli, Alice Grossi, Fabio Fernandes Morato Castro, Jorge Kalil, Florian N. Gohr, Florian Schmidt, Eva Bartok, Thomas Zillinger, Gunther Hartmann, Matthias Geyer, Marco Gattorno, Leonardo Oliveira Mendonca, Seth L. Masters

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    Abstract

    Purpose NLRC4-associated autoinflammatory disease (NLRC4-AID) is an autosomal dominant condition presenting with a range of clinical manifestations which can include macrophage activation syndrome (MAS) and severe enterocolitis. We now report the first homozygous mutation in NLRC4 (c.478G > A, p.A160T) causing autoinflammatory disease with immune dysregulation and find that heterozygous carriers in the general population are at increased risk of developing ulcerative colitis. Methods Circulating immune cells and inflammatory markers were profiled and historical clinical data interrogated. DNA was extracted and sequenced using standard procedures. Inflammasome activation assays for ASC speck formation, pyroptosis, and IL-1 beta/IL-18 secretion confirmed pathogenicity of the mutation in vitro. Genome-wide association of NLRC4 (A160T) with ulcerative colitis was examined using data from the IBD exomes portal. Results A 60-year-old Brazilian female patient was evaluated for recurrent episodes of systemic inflammation from six months of age. Episodes were characterized by recurrent low-grade fever, chills, oral ulceration, uveitis, arthralgia, and abdominal pain, followed by diarrhea with mucus and variable skin rash. High doses of corticosteroids were somewhat effective in controlling disease and anti-IL-1 beta therapy partially controlled symptoms. While on treatment, serum IL-1 beta and IL-18 levels remained elevated. Genetic investigations identified a homozygous mutation in NLRC4 (A160T), inherited in a recessive fashion. Increased ASC speck formation and IL-1 beta/IL-18 secretion confirmed pathogenicity when NLRC4 (A160T) was analyzed in human cell lines. This allele is significantly enriched in patients with ulcerative colitis: OR 2.546 (95% 1.778-3.644), P = 0.01305. Conclusion NLRC4 (A160T) can either cause recessively inherited autoinflammation and immune dysregulation, or function as a heterozygous risk factor for the development of ulcerative colitis.

    Original languageEnglish
    JournalJournal of Clinical Immunology
    Volume42
    Pages (from-to)325-335
    Number of pages11
    ISSN0271-9142
    DOIs
    Publication statusPublished - 2021

    Keywords

    • NLRC4-associated autoinflammatory disease
    • inflammasome
    • ulcerative colitis
    • CAUSES AUTOINFLAMMATION
    • NLRC4 CAUSES
    • MUTATION
    • RECRUITMENT
    • NLRP3

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