Department of Immunology and Microbiology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA.
Infect Immun. 2022 Jan 25;90(1):e0048121. doi: 10.1128/IAI.00481-21. Epub 2021 Nov 8.
Endoplasmic reticulum (ER) stress is intimately linked with inflammation in response to pathogenic infections. ER stress occurs when cells experience a buildup of misfolded or unfolded protein during times of perturbation, such as infections, which facilitates the unfolded protein response (UPR). The UPR involves multiple host pathways in an attempt to reestablish homeostasis, which oftentimes leads to inflammation and cell death if unresolved. The UPR is activated to help resolve some bacterial infections, and the IRE1α pathway is especially critical in mediating inflammation. To understand the role of the IRE1α pathway of the UPR during enteric bacterial infection, we employed Citrobacter rodentium to study host-pathogen interactions in intestinal epithelial cells and the murine gastrointestinal (GI) tract. C. rodentium is an enteric mouse pathogen that is similar to the human pathogens enteropathogenic and enterohemorrhagic Escherichia coli (EPEC and EHEC, respectively), for which we have limited small-animal models. Here, we demonstrate that both C. rodentium and EPEC induced the UPR in intestinal epithelial cells. UPR induction during C. rodentium infection correlated with the onset of inflammation in bone marrow-derived macrophages (BMDMs). Our previous work implicated IRE1α and NOD1/2 in ER stress-induced inflammation, which we observed were also required for proinflammatory gene induction during C. rodentium infection. C. rodentium induced IRE1α-dependent inflammation in mice, and inhibiting IRE1α led to a dysregulated inflammatory response and delayed clearance of C. rodentium. This study demonstrates that ER stress aids inflammation and clearance of C. rodentium through a mechanism involving the IRE1α-NOD1/2 axis.
内质网(ER)应激与病原感染引起的炎症密切相关。当细胞在扰动时(如感染)经历错误折叠或未折叠蛋白的积累时,就会发生 ER 应激,这有助于未折叠蛋白反应(UPR)。UPR 涉及多个宿主途径,试图重新建立体内平衡,如果未解决,这通常会导致炎症和细胞死亡。UPR 被激活以帮助解决一些细菌感染,IRE1α 途径在介导炎症方面尤为关键。为了了解 UPR 的 IRE1α 途径在肠细菌感染中的作用,我们使用柠檬酸杆菌来研究肠道上皮细胞和鼠胃肠道中的宿主-病原体相互作用。柠檬酸杆菌是一种肠道鼠病原体,类似于人类病原体肠致病性和肠出血性大肠杆菌(分别为 EPEC 和 EHEC),我们对其的小型动物模型有限。在这里,我们证明柠檬酸杆菌和 EPEC 均可诱导肠道上皮细胞中的 UPR。柠檬酸杆菌感染期间 UPR 的诱导与骨髓来源的巨噬细胞(BMDM)中炎症的发生相关。我们之前的工作表明 IRE1α 和 NOD1/2 在 ER 应激诱导的炎症中起作用,我们观察到它们在柠檬酸杆菌感染期间诱导促炎基因表达也需要它们。柠檬酸杆菌在小鼠中诱导 IRE1α 依赖性炎症,抑制 IRE1α 导致炎症反应失调和柠檬酸杆菌清除延迟。这项研究表明,通过涉及 IRE1α-NOD1/2 轴的机制,内质网应激有助于柠檬酸杆菌的炎症和清除。