Zhang Yibi, Wang Xiaodong, Gu Yinmin, Liu Tongfeng, Zhao Xujie, Cheng Shuwen, Duan Liqiang, Huang Chang, Wu Songzhe, Gao Shan
School of Biomedical Engineering (Suzhou), Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China.
Key Laboratory of Bio-medical Diagnostics, Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences, Suzhou 215163, China.
Proc Natl Acad Sci U S A. 2025 Jan 28;122(4):e2420005122. doi: 10.1073/pnas.2420005122. Epub 2025 Jan 23.
Heterogeneous roles of complement C3 have been implicated in tumor metastasis and are highly context dependent. However, the underlying mechanisms linking C3 to tumor metastasis remain elusive in renal cell carcinoma (RCC). Here, we demonstrate that C3 of RCC cell-derived extracellular vesicles (EVs) contributes to metastasis via polarizing tumor-associated macrophages (TAMs) into the immunosuppressive phenotype and recruiting polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs). Mechanistically, EV C3 induces the secretion of CCL2 and CXCL1 by lung macrophages and subsequently enhances TAM polarization and PMN-MDSC recruitment. Notably, targeting the CCL2/CCR2 or CXCL1/CXCR2 axis with the inhibitors RS504393 or Navarixin, respectively, effectively suppresses lung metastasis induced by RCC-derived C3 in a mouse model. Clinically, RCC patients with high expression of C3 demonstrate poor prognosis. Collectively, our findings reveal that tumor-derived EV C3 induces an immunosuppressive tumor microenvironment via TAMs, and thus promoting RCC metastasis.
补体C3的异质性作用与肿瘤转移有关,且高度依赖于具体环境。然而,在肾细胞癌(RCC)中,将C3与肿瘤转移联系起来的潜在机制仍不清楚。在此,我们证明RCC细胞衍生的细胞外囊泡(EVs)中的C3通过将肿瘤相关巨噬细胞(TAMs)极化为免疫抑制表型并募集多形核髓源性抑制细胞(PMN-MDSCs)来促进转移。从机制上讲,EV C3诱导肺巨噬细胞分泌CCL2和CXCL1,随后增强TAM极化和PMN-MDSC募集。值得注意的是,分别用抑制剂RS504393或Navarixin靶向CCL2/CCR2或CXCL1/CXCR2轴,可有效抑制小鼠模型中RCC衍生的C3诱导的肺转移。临床上,C3高表达的RCC患者预后较差。总体而言,我们的研究结果表明,肿瘤衍生的EV C3通过TAMs诱导免疫抑制性肿瘤微环境,从而促进RCC转移。