Leiden Academic Centre for Drug Research, Leiden University, 2333 CC Leiden, The Netherlands.
Int J Mol Sci. 2022 Sep 4;23(17):10119. doi: 10.3390/ijms231710119.
Hypoxia and HIF signaling drive cancer progression and therapy resistance and have been demonstrated in breast cancer. To what extent breast cancer subtypes differ in their response to hypoxia has not been resolved. Here, we show that hypoxia similarly triggers HIF1 stabilization in luminal and basal A triple negative breast cancer cells and we use high throughput targeted RNA sequencing to analyze its effects on gene expression in these subtypes. We focus on regulation of YAP/TAZ/TEAD targets and find overlapping as well as distinct target genes being modulated in luminal and basal A cells under hypoxia. We reveal a HIF1 mediated, basal A specific response to hypoxia by which TAZ, but not YAP, is phosphorylated at Ser89. While total YAP/TAZ localization is not affected by hypoxia, hypoxia drives a shift of [p-TAZ(Ser89)/p-YAP(Ser127)] from the nucleus to the cytoplasm in basal A but not luminal breast cancer cells. Cell fractionation and YAP knock-out experiments confirm cytoplasmic sequestration of TAZ(Ser89) in hypoxic basal A cells. Pharmacological and genetic interference experiments identify c-Src and CDK3 as kinases involved in such phosphorylation of TAZ at Ser89 in hypoxic basal A cells. Hypoxia attenuates growth of basal A cells and the effect of verteporfin, a disruptor of YAP/TAZ-TEAD-mediated transcription, is diminished under those conditions, while expression of a TAZ-S89A mutant does not confer basal A cells with a growth advantage under hypoxic conditions, indicating that other hypoxia regulated pathways suppressing cell growth are dominant.
缺氧和 HIF 信号通路促进癌症进展和治疗耐药性,在乳腺癌中已有研究证实。然而,不同乳腺癌亚型对缺氧的反应程度仍未得到解决。本研究表明,缺氧同样会引发腔面和基底 A 三阴性乳腺癌细胞中 HIF1 的稳定,我们利用高通量靶向 RNA 测序分析其对这些亚型基因表达的影响。我们重点关注 YAP/TAZ/TEAD 靶基因的调控,发现缺氧条件下腔面和基底 A 细胞中有重叠和独特的靶基因被调节。我们揭示了 HIF1 介导的、基底 A 特异性的缺氧反应,其中 TAZ 而不是 YAP,在 Ser89 被磷酸化。虽然总 YAP/TAZ 定位不受缺氧影响,但缺氧会导致 [p-TAZ(Ser89)/p-YAP(Ser127)]从细胞核转移到细胞质,这仅发生在基底 A 细胞而不是腔面乳腺癌细胞中。细胞分馏和 YAP 敲除实验证实了缺氧条件下基底 A 细胞中 TAZ(Ser89)的细胞质隔离。药理学和遗传干扰实验鉴定出 c-Src 和 CDK3 是缺氧条件下基底 A 细胞中 TAZ 在 Ser89 磷酸化的激酶。缺氧会抑制基底 A 细胞的生长,而在这些条件下,verteporfin(一种破坏 YAP/TAZ-TEAD 介导转录的抑制剂)的效果会减弱,而表达 TAZ-S89A 突变体不会使基底 A 细胞在缺氧条件下获得生长优势,这表明其他受缺氧调节的抑制细胞生长的途径占主导地位。