Chunwei Li , Lili Zhu , Yaqi Yang , Tengfei Zhang , Chengxin Chen , Yixing Zhang , Wenxuan Ji , Xiaoran Duan , Wenhua Xue , Lifeng Li , Jie Zhao
{"title":"在肺腺癌中,过表达 FBP1 可通过抑制糖酵解和促进 IL33 的分泌来增强树突状细胞的活化和成熟。","authors":"Chunwei Li , Lili Zhu , Yaqi Yang , Tengfei Zhang , Chengxin Chen , Yixing Zhang , Wenxuan Ji , Xiaoran Duan , Wenhua Xue , Lifeng Li , Jie Zhao","doi":"10.1016/j.bbadis.2024.167559","DOIUrl":null,"url":null,"abstract":"<div><div>Fructose 1,6-diphosphatase 1 (FBP1) is an enzyme involved in gluconeogenesis and glycolysis inhibition. Dendritic cells (DCs) are antigen-presenting cells, and antigens presented to T cells activate the immune response. FBP1 inhibits the development of several tumors, and high FBP1 expression inhibits the proliferation, migration, and invasion of lung cancer cells. However, the mechanism through which FBP1 mediates the tumor immune microenvironment is unclear. This study mainly analyzed the role of FBP1 in regulating the function of DCs through metabolic reprogramming and immune microenvironment using in vitro and in vivo experiments. The positive association of FBP1 with DCs was found by bioinformatic analysis. The in vitro experiments revealed that the extracellular acidification rate and lactate level were lower in the FBP1 overexpression cells than in the control cells and that the lower lactate level reduced the inhibition of DC function. In addition, high FBP1 expression promoted the secretion of IL33 by activating the cGAS/STING/NF-κB/IL33 pathway, which was identified and verified via high-throughput sequencing and in vitro experiments. FBP1 activated the cGAS/STING pathway by increasing the degree of DNA damage, as revealed by the level of γH2AX and comet assay. IL33 enhanced the expression of the DC costimulatory molecules CD86 and HLA-DR as well as that of the functional factor IL-1β. The results demonstrated that FBP1 promoted the activation and maturation of DCs by inhibiting glycolysis and promoting the secretion of IL33 as well as by further activating the function of CD8<sup>+</sup>T cells. Finally, the humanized immune system mouse models confirmed the above role of FBP1. Thus, FBP1 may serve as a new target to cure lung adenocarcinoma, and IL33 may improve the efficiency of immune therapy in lung adenocarcinoma.</div></div>","PeriodicalId":8821,"journal":{"name":"Biochimica et biophysica acta. 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FBP1 inhibits the development of several tumors, and high FBP1 expression inhibits the proliferation, migration, and invasion of lung cancer cells. However, the mechanism through which FBP1 mediates the tumor immune microenvironment is unclear. This study mainly analyzed the role of FBP1 in regulating the function of DCs through metabolic reprogramming and immune microenvironment using in vitro and in vivo experiments. The positive association of FBP1 with DCs was found by bioinformatic analysis. The in vitro experiments revealed that the extracellular acidification rate and lactate level were lower in the FBP1 overexpression cells than in the control cells and that the lower lactate level reduced the inhibition of DC function. In addition, high FBP1 expression promoted the secretion of IL33 by activating the cGAS/STING/NF-κB/IL33 pathway, which was identified and verified via high-throughput sequencing and in vitro experiments. 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引用次数: 0
摘要
果糖 1,6-二磷酸酶 1(FBP1)是一种参与糖元生成和糖酵解抑制的酶。树突状细胞(DC)是抗原递呈细胞,递呈给 T 细胞的抗原可激活免疫反应。FBP1 可抑制多种肿瘤的发展,FBP1 的高表达可抑制肺癌细胞的增殖、迁移和侵袭。然而,FBP1介导肿瘤免疫微环境的机制尚不清楚。本研究主要通过体外和体内实验分析了FBP1通过代谢重编程和免疫微环境调节DCs功能的作用。通过生物信息学分析发现,FBP1 与 DCs 呈正相关。体外实验发现,FBP1过表达细胞的细胞外酸化率和乳酸水平低于对照细胞,乳酸水平的降低减少了对DC功能的抑制。此外,FBP1的高表达还通过激活cGAS/STING/NF-κB/IL33通路促进了IL33的分泌。γH2AX水平和彗星试验显示,FBP1通过增加DNA损伤程度激活了cGAS/STING通路。IL33 可增强 DC 拟合分子 CD86 和 HLA-DR 以及功能因子 IL-1β 的表达。结果表明,FBP1 通过抑制糖酵解和促进 IL33 的分泌以及进一步激活 CD8+T 细胞的功能,促进了 DC 的活化和成熟。最后,人源化免疫系统小鼠模型证实了 FBP1 的上述作用。因此,FBP1可作为治疗肺腺癌的新靶点,而IL33可提高肺腺癌免疫疗法的效率。
Overexpression of FBP1 enhances dendritic cell activation and maturation by inhibiting glycolysis and promoting the secretion of IL33 in lung adenocarcinoma
Fructose 1,6-diphosphatase 1 (FBP1) is an enzyme involved in gluconeogenesis and glycolysis inhibition. Dendritic cells (DCs) are antigen-presenting cells, and antigens presented to T cells activate the immune response. FBP1 inhibits the development of several tumors, and high FBP1 expression inhibits the proliferation, migration, and invasion of lung cancer cells. However, the mechanism through which FBP1 mediates the tumor immune microenvironment is unclear. This study mainly analyzed the role of FBP1 in regulating the function of DCs through metabolic reprogramming and immune microenvironment using in vitro and in vivo experiments. The positive association of FBP1 with DCs was found by bioinformatic analysis. The in vitro experiments revealed that the extracellular acidification rate and lactate level were lower in the FBP1 overexpression cells than in the control cells and that the lower lactate level reduced the inhibition of DC function. In addition, high FBP1 expression promoted the secretion of IL33 by activating the cGAS/STING/NF-κB/IL33 pathway, which was identified and verified via high-throughput sequencing and in vitro experiments. FBP1 activated the cGAS/STING pathway by increasing the degree of DNA damage, as revealed by the level of γH2AX and comet assay. IL33 enhanced the expression of the DC costimulatory molecules CD86 and HLA-DR as well as that of the functional factor IL-1β. The results demonstrated that FBP1 promoted the activation and maturation of DCs by inhibiting glycolysis and promoting the secretion of IL33 as well as by further activating the function of CD8+T cells. Finally, the humanized immune system mouse models confirmed the above role of FBP1. Thus, FBP1 may serve as a new target to cure lung adenocarcinoma, and IL33 may improve the efficiency of immune therapy in lung adenocarcinoma.
期刊介绍:
BBA Molecular Basis of Disease addresses the biochemistry and molecular genetics of disease processes and models of human disease. This journal covers aspects of aging, cancer, metabolic-, neurological-, and immunological-based disease. Manuscripts focused on using animal models to elucidate biochemical and mechanistic insight in each of these conditions, are particularly encouraged. Manuscripts should emphasize the underlying mechanisms of disease pathways and provide novel contributions to the understanding and/or treatment of these disorders. Highly descriptive and method development submissions may be declined without full review. The submission of uninvited reviews to BBA - Molecular Basis of Disease is strongly discouraged, and any such uninvited review should be accompanied by a coverletter outlining the compelling reasons why the review should be considered.