Ye Jiayu, Baer John M, Faget Douglas V, Morikis Vasilios A, Ren Qihao, Melam Anupama, Delgado Ana Paula, Luo Xianmin, Bagchi Satarupa Mullick, Belle Jad I, Campos Edward, Friedman Michael, Veis Deborah J, Knudsen Erik S, Witkiewicz Agnieszka K, Powers Scott, Longmore Gregory D, DeNardo David G, Stewart Sheila A
Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri.
Department of Medicine, Washington University School of Medicine, St. Louis, Missouri.
Cancer Discov. 2024 Jul 1;14(7):1302-1323. doi: 10.1158/2159-8290.CD-23-0426.
The tumor microenvironment (TME) profoundly influences tumorigenesis, with gene expression in the breast TME capable of predicting clinical outcomes. The TME is complex and includes distinct cancer-associated fibroblast (CAF) subtypes whose contribution to tumorigenesis remains unclear. Here, we identify a subset of myofibroblast CAFs (myCAF) that are senescent (senCAF) in mouse and human breast tumors. Utilizing the MMTV-PyMT;INK-ATTAC (INK) mouse model, we found that senCAF-secreted extracellular matrix specifically limits natural killer (NK) cell cytotoxicity to promote tumor growth. Genetic or pharmacologic senCAF elimination unleashes NK cell killing, restricting tumor growth. Finally, we show that senCAFs are present in HER2+, ER+, and triple-negative breast cancer and in ductal carcinoma in situ (DCIS) where they predict tumor recurrence. Together, these findings demonstrate that senCAFs are potently tumor promoting and raise the possibility that targeting them by senolytic therapy could restrain breast cancer development. Significance: senCAFs limit NK cell-mediated killing, thereby contributing to breast cancer progression. Thus, targeting senCAFs could be a clinically viable approach to limit tumor progression. See related article by Belle et al., p. 1324.
肿瘤微环境(TME)对肿瘤发生有着深远影响,乳腺TME中的基因表达能够预测临床结果。TME很复杂,包括不同的癌症相关成纤维细胞(CAF)亚型,其对肿瘤发生的作用尚不清楚。在这里,我们在小鼠和人类乳腺肿瘤中鉴定出了一部分衰老的肌成纤维细胞CAF(myCAF,即衰老CAF,senCAF)。利用MMTV-PyMT;INK-ATTAC(INK)小鼠模型,我们发现senCAF分泌的细胞外基质会特异性地限制自然杀伤(NK)细胞的细胞毒性,从而促进肿瘤生长。通过基因或药物手段消除senCAF可释放NK细胞的杀伤作用,限制肿瘤生长。最后,我们表明senCAF存在于HER2阳性、雌激素受体(ER)阳性和三阴性乳腺癌以及导管原位癌(DCIS)中,在这些肿瘤中它们可预测肿瘤复发。总之,这些发现表明senCAF具有强大的促肿瘤作用,并增加了通过衰老细胞溶解疗法靶向它们来抑制乳腺癌发展的可能性。意义:senCAF限制NK细胞介导的杀伤作用,从而促进乳腺癌进展。因此,靶向senCAF可能是一种临床上可行的限制肿瘤进展的方法。见Belle等人的相关文章,第1324页。