Dominant-negative NFKBIA mutation promotes IL-1β production causing hepatic disease with severe immunodeficiency.
Tan EE., Hopkins RA., Lim CK., Jamuar SS., Ong C., Thoon KC., Koh MJ., Shin EM., Lian DW., Weerasooriya M., Lee CZ., Soetedjo AAP., Lim CS., Au VB., Chua E., Lee HY., Jones LA., James SS., Kaliaperumal N., Kwok J., Tan ES., Thomas B., Wu LX., Ho L., Fairhurst AM., Ginhoux F., Teo AK., Zhang YL., Ong KH., Yu W., Venkatesh B., Tergaonkar V., Reversade B., Chin KC., Tan AM., Liew WK., Connolly JE.
Although IKK-β has previously been shown as a negative regulator of IL-1β secretion in mice, this role has not been proven in humans. Genetic studies of NF-κB signaling in humans with inherited diseases of the immune system have not demonstrated the relevance of the NF-κB pathway in suppressing IL-1β expression. Here, we report an infant with a clinical pathology comprising neutrophil-mediated autoinflammation and recurrent bacterial infections. Whole-exome sequencing revealed a de novo heterozygous missense mutation of NFKBIA, resulting in a L34P IκBα variant that severely repressed NF-κB activation and downstream cytokine production. Paradoxically, IL-1β secretion was elevated in the patient's stimulated leukocytes, in her induced pluripotent stem cell-derived macrophages, and in murine bone marrow-derived macrophages containing the L34P mutation. The patient's hypersecretion of IL-1β correlated with activated neutrophilia and liver fibrosis with neutrophil accumulation. Hematopoietic stem cell transplantation reversed neutrophilia, restored a resting state in neutrophils, and normalized IL-1β release from stimulated leukocytes. Additional therapeutic blockade of IL-1 ameliorated liver damage, while decreasing neutrophil activation and associated IL-1β secretion. Our studies reveal a previously unrecognized role of human IκBα as an essential regulator of canonical NF-κB signaling in the prevention of neutrophil-dependent autoinflammatory diseases. These findings also highlight the therapeutic potential of IL-1 inhibitors in treating complications arising from systemic NF-κB inhibition.