Mi Xiuwei, Duan Yudong, Sun Jiying, Tai Qingliang, Yao Huihui, Meng Lijun, Yang Xiaoshan, Shi Xinyu, Shi Bo, Chen Junjie, Sun Liang, Zhou Diyuan, Xiao Sheng, Yao Yizhou, He Songbing
Department of General Surgery, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215006, China; Advanced Molecular Pathology Institute of Soochow University and SANO, & SANO Medical Laboratories Suzhou, Jiangsu 215000, China.
Department of Orthopedic Surgery, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215006, China.
Pharmacol Res. 2024 Dec;210:107494. doi: 10.1016/j.phrs.2024.107494. Epub 2024 Nov 5.
Despite significant advances in the diagnosis and treatment of colorectal cancer (CRC), the prognosis for late-stage patients remains poor, highlighting the urgent need for new preventive and therapeutic strategies. Recent studies have focused on the ketogenic diet (KD) and its metabolite, β-hydroxybutyrate (BHB), for their tumor-suppressive effects and modulation of inflammatory responses. Using the azoxymethane (AOM) / dextran sulfate sodium (DSS)-induced mouse CRC model, we found that the ketogenic diet and BHB inhibit pro-tumor N2-type tumor-associated neutrophils (TANs) while promoting the polarization of TANs towards the anti-tumor N1 type. This shift in TANs polarization affects tumor growth and metastasis. The underlying mechanism involves BHB acting on the intracellular receptor histone deacetylases 3 (HDAC3), which modulates the activation of the AMOT-YAP/TAZ axis, leading to the inhibition of pro-carcinogenic factor transcription and release. Moreover, clinical cohort data corroborate these findings, showing that CRC patients with elevated BHB levels have significantly lower rates of lymph node involvement, which is associated with a higher infiltration ratio of anti-carcinogenic N1-type TANs in the tumor microenvironment (TME). These results suggest that BHB levels could serve as a prognostic biomarker for CRC. In conclusion, our findings indicate that BHB derived from KD regulates TANs polarization in CRC via the HDAC3-AMOT-YAP/TAZ axis, effectively inhibiting tumor growth and metastasis. These insights establish a novel theoretical basis for employing the KD in the treatment of CRC and for developing cancer adjuvant immunotherapy strategy based on the polarization of neutrophils.
尽管在结直肠癌(CRC)的诊断和治疗方面取得了重大进展,但晚期患者的预后仍然很差,这凸显了对新的预防和治疗策略的迫切需求。最近的研究集中在生酮饮食(KD)及其代谢产物β-羟基丁酸(BHB)上,因为它们具有肿瘤抑制作用和对炎症反应的调节作用。使用氧化偶氮甲烷(AOM)/葡聚糖硫酸钠(DSS)诱导的小鼠CRC模型,我们发现生酮饮食和BHB抑制促肿瘤的N2型肿瘤相关中性粒细胞(TANs),同时促进TANs向抗肿瘤的N1型极化。TANs极化的这种转变影响肿瘤的生长和转移。潜在机制涉及BHB作用于细胞内受体组蛋白去乙酰化酶3(HDAC3),其调节AMOT-YAP/TAZ轴的激活,导致致癌因子转录和释放的抑制。此外,临床队列数据证实了这些发现,表明BHB水平升高的CRC患者淋巴结受累率显著降低,这与肿瘤微环境(TME)中抗癌N1型TANs的较高浸润率相关。这些结果表明BHB水平可作为CRC的预后生物标志物。总之,我们的研究结果表明,KD衍生的BHB通过HDAC3-AMOT-YAP/TAZ轴调节CRC中的TANs极化,有效抑制肿瘤生长和转移。这些见解为将KD用于CRC治疗以及基于中性粒细胞极化开发癌症辅助免疫治疗策略奠定了新的理论基础。