Peng Zhang, Jinrong Ma, Yi Ching Esther Wan, Chenxi Li, Lijuan Liu, Mengmeng He, Ning Zhang, Yanfen Ma, Jian Hu, Liyuan Zhao, Ziwei Zhong, Xiao Lei, Jin Gong, Ting Zeng, JunPeng Ma, Yanyan Da, Zhiyong Zhou, Jin Yang, Xiaoqin Wang, Tian Gong, Chengsheng Zhang
Aerobic glycolysis and lactate have been shown to modulate tumor microenvironment (TME) and disease progression. Lactate-mediated histone lysine lactylation (Kla) is a newly recognized epigenetic modification whose biological function remains poorly understood. Here, through integrated bioinformatic and experimental analyses, we demonstrate that glycolysis-derived lactate induces histone H3 lysine 18 lactylation (H3K18la) and up-regulates the expression of chemokine C-X-C motif Ligand 1 (CXCL1), thereby recruiting neutrophils and inducing immunosuppression in pancreatic cancer. Moreover, our data suggest that p300/CBP-associated factor (PCAF) functions as a histone lactyltransferase that transcriptionally activates CXCL1 expression. Finally, we reveal that combinational treatment with bromosporine (a PCAF inhibitor) and anti-PD-1 antibody exhibits a synergistic antitumor effect on both subcutaneous and orthotopic tumor models of pancreatic cancer. Taken together, our study not only identifies a mechanism by which the aerobic glycolysis-induced Lactate-PCAF-H3K18la-CXCL1 pathway mediates neutrophil infiltration and immunosuppression, but also develops a potential therapeutic strategy for pancreatic cancer. Increased glycolysis in pancreatic cancer promotes immune escape by altering the tumor microenvironment. Here, the authors show that lactate-driven histone lactylation via PCAF increases CXCL1 expression, recruiting neutrophils and enabling immunosuppression, and PCAF inhibition improves anti-PD-1 therapy in pancreatic cancer mouse models.