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Human LUBAC deficiency leads to autoinflammation and immunodeficiency by dysregulation in TNF-mediated cell death

Oda, H.; Manthiram, K.; Pimpale Chavan, P.; Nakabo, S.; Kuehn, H.; Beck, D. B.; Chae, J. J.; Nehrebecky, M.; Ombrello, A.; Romeo, T.; Deuitch, N.; Matthiasardottir, B.; Mullikin, J.; Stoddard, J.; Niemela, J.; Anderton, H.; Lawlor, K. E.; Yoshitomi, H.; Yang, D.; Boehm, M.; Davis, J.; Mudd, P.; Randazzo, D.; Tsai, W. L.; Gadina, M.; Kaplan, M. J.; Toguchida, J.; Mayer, C. T.; Rosenzweig, S. D.; Iwai, K.; Silke, J.; Boisson, B.; Casanova, J.-L.; Rao, A.; Lalaoui, N.; Aksentijevich, I.; Kastner, D. L.

2022-11-14 allergy and immunology
10.1101/2022.11.09.22281431
Show abstract

The linear ubiquitin assembly complex (LUBAC) consists of HOIP, HOIL1 and SHARPIN, and is essential for proper immune responses. Patients with HOIP and HOIL1 deficiencies present with severe immunodeficiency, autoinflammation and glycogen storage. In mice, the loss of Sharpin leads to severe dermatitis due to excessive cell death in keratinocytes. Here we report the first patient with SHARPIN deficiency, manifesting fever, arthritis, colitis, chronic otitis media and hepatic glycogenosis but unexpectedly, not associated with dermatologic manifestations. Mechanistically, fibroblasts and B cells from patients with all three LUBAC deficiencies showed attenuated canonical NF-B response and propensity to apoptosis mediated by TNF superfamily members. Furthermore, the SHARPIN deficient patient showed substantial reduction of adenoidal germinal center B cell development. Treatment of the SHARPIN deficient patient with anti-TNF therapies led to complete clinical and transcriptomic resolution of autoinflammation. These findings underscore the critical role of LUBAC as a gatekeeper for apoptosis-mediated immune dysregulation in humans.

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