Department of Molecular and Cellular Biochemistry, College of Medicine, The Ohio State University, Columbus, Ohio, United States of America.
PLoS One. 2013 Aug 16;8(8):e71533. doi: 10.1371/journal.pone.0071533. eCollection 2013.
Tumor fibroblasts are active partners in tumor progression, but the genes and pathways that mediate this collaboration are ill-defined. Previous work demonstrates that Ets2 function in stromal cells significantly contributes to breast tumor progression. Conditional mouse models were used to study the function of Ets2 in both mammary stromal fibroblasts and epithelial cells. Conditional inactivation of Ets2 in stromal fibroblasts in PyMT and ErbB2 driven tumors significantly reduced tumor growth, however deletion of Ets2 in epithelial cells in the PyMT model had no significant effect. Analysis of gene expression in fibroblasts revealed a tumor- and Ets2-dependent gene signature that was enriched in genes important for ECM remodeling, cell migration, and angiogenesis in both PyMT and ErbB2 driven-tumors. Consistent with these results, PyMT and ErbB2 tumors lacking Ets2 in fibroblasts had fewer functional blood vessels, and Ets2 in fibroblasts elicited changes in gene expression in tumor endothelial cells consistent with this phenotype. An in vivo angiogenesis assay revealed the ability of Ets2 in fibroblasts to promote blood vessel formation in the absence of tumor cells. Importantly, the Ets2-dependent gene expression signatures from both mouse models were able to distinguish human breast tumor stroma from normal stroma, and correlated with patient outcomes in two whole tumor breast cancer data sets. The data reveals a key function for Ets2 in tumor fibroblasts in signaling to endothelial cells to promote tumor angiogenesis. The results highlight the collaborative networks that orchestrate communication between stromal cells and tumor cells, and suggest that targeting tumor fibroblasts may be an effective strategy for developing novel anti-angiogenic therapies.
肿瘤成纤维细胞是肿瘤进展的活跃伙伴,但介导这种协作的基因和途径尚不清楚。先前的工作表明,Ets2 在基质细胞中的功能显著促进了乳腺癌的进展。使用条件性小鼠模型研究了 Ets2 在乳腺基质成纤维细胞和上皮细胞中的功能。在 PyMT 和 ErbB2 驱动的肿瘤中,条件性敲除基质成纤维细胞中的 Ets2 显著降低了肿瘤生长,但在 PyMT 模型中上皮细胞中 Ets2 的缺失没有显著影响。对成纤维细胞中基因表达的分析揭示了一个肿瘤和 Ets2 依赖性的基因特征,该特征在 PyMT 和 ErbB2 驱动的肿瘤中富含与细胞外基质重塑、细胞迁移和血管生成相关的重要基因。与这些结果一致的是,缺乏 Ets2 的 PyMT 和 ErbB2 肿瘤中的功能性血管较少,而 Ets2 在成纤维细胞中引起的肿瘤内皮细胞基因表达变化与这种表型一致。体内血管生成测定显示,缺乏肿瘤细胞的情况下,Ets2 在成纤维细胞中能够促进血管形成。重要的是,来自两种小鼠模型的 Ets2 依赖性基因表达特征能够区分人乳腺癌肿瘤基质与正常基质,并与两个全肿瘤乳腺癌数据集中的患者预后相关。这些数据揭示了 Ets2 在肿瘤成纤维细胞中向内皮细胞发出信号以促进肿瘤血管生成的关键功能。研究结果突出了协调基质细胞和肿瘤细胞之间通讯的协作网络,并表明靶向肿瘤成纤维细胞可能是开发新型抗血管生成疗法的有效策略。