Login / Signup

Inherited PD-1 deficiency underlies tuberculosis and autoimmunity in a child.

Masato OgishiRui YangCaner AytekinDavid LanglaisMathieu BourgeyTaushif KhanFatima Al AliMahbuba RahmanOttavia M DelmonteMaya ChrabiehPeng ZhangConor GruberSimon J PelhamAndrás N SpaanJérémie RosainWei-Te LeiScott DrutmanMatthew D HellmannMargaret K CallahanMatthew J AdamowPhillip WongJedd D WolchokGeetha RaoCindy S MaYuka NakajimaTomonori YaguchiKenji ChamotoSamuel C WilliamsJean François EmileFlore RozenbergMichael S GlickmanFranck RapaportGaspard KernerGarrett AllingtonIlhan TezcanDeniz Çağdaş AyvazFerda O HosnutFigen DoguAydan IkinciogullariV Koneti RaoLeena KainulainenVivien BéziatJacinta BustamanteSilvia VilarinhoRichard P LiftonBertrand BoissonLaurent AbelDusan BogunovicNico MarrLuigi Daniele NotarangeloStuart G TangyeTasuku HonjoPhilippe GrosStéphanie Boisson-DupuisJean Laurent Casanova
Published in: Nature medicine (2021)
The pathophysiology of adverse events following programmed cell death protein 1 (PD-1) blockade, including tuberculosis (TB) and autoimmunity, remains poorly characterized. We studied a patient with inherited PD-1 deficiency and TB who died of pulmonary autoimmunity. The patient's leukocytes did not express PD-1 or respond to PD-1-mediated suppression. The patient's lymphocytes produced only small amounts of interferon (IFN)-γ upon mycobacterial stimuli, similarly to patients with inborn errors of IFN-γ production who are vulnerable to TB. This phenotype resulted from a combined depletion of Vδ2+ γδ T, mucosal-associated invariant T and CD56bright natural killer lymphocytes and dysfunction of other T lymphocyte subsets. Moreover, the patient displayed hepatosplenomegaly and an expansion of total, activated and RORγT+ CD4-CD8- double-negative αβ T cells, similar to patients with STAT3 gain-of-function mutations who display lymphoproliferative autoimmunity. This phenotype resulted from excessive amounts of STAT3-activating cytokines interleukin (IL)-6 and IL-23 produced by activated T lymphocytes and monocytes, and the STAT3-dependent expression of RORγT by activated T lymphocytes. Our work highlights the indispensable role of human PD-1 in governing both antimycobacterial immunity and self-tolerance, while identifying potentially actionable molecular targets for the diagnostic and therapeutic management of TB and autoimmunity in patients on PD-1 blockade.
Keyphrases