Human Vascularized Macrophage-Islet Organoids to Model Immune-Mediated Pancreatic β cell Pyroptosis upon Viral Infection

Author:

Yang Liuliu,Han Yuling,Zhang Tuo,Dong Xue,Ge Jian,Roy Aadita,Zhu Jiajun,Lu Tiankun,Vandana J. JeyaORCID,de Silva Neranjan,Robertson Catherine C.,Xiang Jenny Z,Pan Chendong,Sun Yanjie,Que Jianwen,Evans Todd,Liu Chengyang,Wang Wei,Naji Ali,Parker Stephen C.J.,Schwartz Robert E.,Chen Shuibing

Abstract

SUMMARYThere is a paucity of human models to study immune-mediated host damage. Here, we utilized the GeoMx spatial multi-omics platform to analyze immune cell changes in COVID-19 pancreatic autopsy samples, revealing an accumulation of proinflammatory macrophages. Single cell RNA-seq analysis of human islets exposed to SARS-CoV-2 or Coxsackievirus B4 (CVB4) viruses identified activation of proinflammatory macrophages and β cell pyroptosis. To distinguish viral versus proinflammatory macrophage-mediated β cell pyroptosis, we developed human pluripotent stem cell (hPSC)-derived vascularized macrophage-islet (VMI) organoids. VMI organoids exhibited enhanced marker expression and function in both β cells and endothelial cells compared to separately cultured cells. Notably, proinflammatory macrophages within VMI organoids induced β cell pyroptosis. Mechanistic investigations highlighted TNFSF12-TNFRSF12A involvement in proinflammatory macrophage-mediated β cell pyroptosis. This study established hPSC- derived VMI organoids as a valuable tool for studying immune cell-mediated host damage and uncovered mechanism of β cell damage during viral exposure.

Publisher

Cold Spring Harbor Laboratory

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