Department of Immunology, School of Medicine, University of Connecticut Health Center, 263 Farmington Ave., Farmington, CT, 06030, USA.
The Eighth Clinical Medical College of Guangzhou University of Chinese Medicine, Foshan Hospital of Traditional Chinese Medicine, Foshan, Guangdong, 528000, China.
Cancer Gene Ther. 2024 Jul;31(7):1007-1017. doi: 10.1038/s41417-024-00796-2. Epub 2024 Jun 19.
Activation of Gasdermin D (GSDMD) results in its cleavage, oligomerization, and subsequent formation of plasma membrane pores, leading to a form of inflammatory cell death denoted as pyroptosis. The roles of GSDMD in inflammation and immune responses to infection are well documented. However, whether GSDMD also plays a role in sporadic cancer development, especially that in the gut epithelium, remains unknown. Here, we show that GSDMD is activated in colorectal tumors of both human and mouse origins. Ablation of GSDMD in a mouse model of sporadic colorectal cancer resulted in reduced tumor formation in the colon and rectum, suggesting a tumor-promoting role of the protein in the gut. Both antibiotic-mediated depletion of gut microbiota and pharmacological inhibition of NLRP3 inflammasome reduced the activation of GSDMD. Loss of GSDMD resulted in reduced infiltration of immature myeloid cells, and increased numbers of macrophages in colorectal tumors. Activation of GSDMD is also accompanied by the aggregation of the endosomal sorting complex required for transport (ESCRT) membrane repair proteins on the membrane of colorectal tumor cells, suggesting that active membrane repairment may prevent pyroptosis induced by the formation of GSDMD pore in tumor cells. Our results show that gut microbiota/NLRP3-mediated activation of GSDMD promotes the development of colorectal tumors, and supports the use of NLRP3 inhibitors to treat colon cancer.
Gasdermin D (GSDMD) 的激活导致其切割、寡聚化,随后形成质膜孔,导致一种称为细胞焦亡的炎症细胞死亡形式。GSDMD 在炎症和对感染的免疫反应中的作用已有充分记录。然而,GSDMD 是否也在散发性癌症的发展中发挥作用,特别是在肠道上皮中,尚不清楚。在这里,我们表明 GSDMD 在人类和小鼠来源的结直肠肿瘤中被激活。在散发性结直肠癌的小鼠模型中敲除 GSDMD 会导致结肠和直肠中的肿瘤形成减少,表明该蛋白在肠道中具有促进肿瘤的作用。肠道微生物群的抗生素耗竭和 NLRP3 炎性体的药理学抑制均可降低 GSDMD 的激活。GSDMD 的缺失导致不成熟髓样细胞在结直肠肿瘤中的浸润减少,而巨噬细胞数量增加。GSDMD 的激活还伴随着内体分选复合物必需的运输 (ESCRT) 膜修复蛋白在结直肠肿瘤细胞膜上的聚集,表明活性膜修复可能防止 GSDMD 孔在肿瘤细胞中形成引起的细胞焦亡。我们的结果表明,肠道微生物群/NLRP3 介导的 GSDMD 激活促进了结直肠肿瘤的发展,并支持使用 NLRP3 抑制剂治疗结肠癌。