DeFilippis Rosa Anna, Fordyce Colleen, Patten Kelley, Chang Hang, Zhao Jianxin, Fontenay Gerald V, Kerlikowske Karla, Parvin Bahram, Tlsty Thea D
Department of Pathology, University of California San Francisco, San Francisco, CA, 94143, USA.
Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, 94143, USA.
Cancer Res. 2014 Sep 15;74(18):5032-5044. doi: 10.1158/0008-5472.CAN-13-3390. Epub 2014 Aug 29.
Telomere malfunction and other types of DNA damage induce an activin A-dependent stress response in mortal nontumorigenic human mammary epithelial cells that subsequently induces desmoplastic-like phenotypes in neighboring fibroblasts. Some characteristics of this fibroblast/stromal response, such as reduced adipocytes and increased extracellular matrix content, are observed not only in tumor tissues but also in disease-free breast tissues at high risk for developing cancer, especially high mammographic density tissues. We found that these phenotypes are induced by repression of the fatty acid translocase CD36, which is seen in desmoplastic and disease-free high mammographic density tissues. In this study, we show that epithelial cells from high mammographic density tissues have more DNA damage signaling, shorter telomeres, increased activin A secretion and an altered DNA damage response compared with epithelial cells from low mammographic density tissues. Strikingly, both telomere malfunction and activin A expression in epithelial cells can repress CD36 expression in adjacent fibroblasts. These results provide new insights into how high mammographic density arises and why it is associated with breast cancer risk, with implications for the definition of novel invention targets (e.g., activin A and CD36) to prevent breast cancer.
端粒功能异常和其他类型的DNA损伤会在终末非致瘤性人乳腺上皮细胞中引发一种依赖激活素A的应激反应,随后在邻近的成纤维细胞中诱导出促结缔组织增生样表型。这种成纤维细胞/基质反应的一些特征,如脂肪细胞减少和细胞外基质含量增加,不仅在肿瘤组织中可见,在患癌风险高的无病乳腺组织中也可见,尤其是乳腺X线摄影密度高的组织。我们发现,这些表型是由脂肪酸转运蛋白CD36的抑制所诱导的,这在促结缔组织增生性和无病的乳腺X线摄影密度高的组织中都有体现。在本研究中,我们表明,与乳腺X线摄影密度低的组织中的上皮细胞相比,乳腺X线摄影密度高的组织中的上皮细胞具有更多的DNA损伤信号、更短的端粒、增加的激活素A分泌以及改变的DNA损伤反应。引人注目的是,上皮细胞中的端粒功能异常和激活素A表达均可抑制相邻成纤维细胞中的CD36表达。这些结果为乳腺X线摄影密度高的成因以及它为何与乳腺癌风险相关提供了新的见解,对预防乳腺癌的新发明靶点(如激活素A和CD36)的定义具有启示意义。