Simerzin Alina, Ackerman Emily E, Fujimaki Kotaro, Kohler Rainer H, Iwamoto Yoshiko, Heltberg Mathias S, Jambhekar Ashwini, Weissleder Ralph, Lahav Galit
Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115.
Center for Systems Biology, Massachusetts General Hospital, Boston, MA 02114.
Mol Biol Cell. 2025 Jun 1;36(6):br16. doi: 10.1091/mbc.E24-09-0394. Epub 2025 Apr 9.
The tumor suppressor protein p53 plays a key role in the cellular response to DNA damage. In response to DNA double-strand breaks (DSB), cultured cells exhibit oscillations of p53 levels, which impact gene expression and cell fate. The dynamics of p53 in vivo have only been studied in fixed tissues or using reporters for p53's transcriptional activity. Here we established breast tumors expressing a fluorescent reporter for p53 levels and employed intravital imaging to quantify its dynamics in response to DSB in vivo. Our findings revealed large heterogeneity among individual cells, with most cells exhibiting a single prolonged pulse. We then tested how p53 dynamics might change under high cell confluency, one factor that differs between cell culture and tissues. We revealed that highly confluent cultured breast cancer cells also show one broad p53 pulse instead of oscillations. Through mathematical modeling, sensitivity analysis, and live-cell imaging, we identified low levels of the phosphatase Wip1, a transcriptional target and negative regulator of p53, as a key contributor to these dynamics. Because high cell confluency better reflects the microenvironment of tissues, the impact of cell confluency on p53 dynamics may have important consequences for cancerous tissues responding to DNA damage-inducing therapies.
肿瘤抑制蛋白p53在细胞对DNA损伤的反应中起关键作用。响应DNA双链断裂(DSB)时,培养的细胞会表现出p53水平的振荡,这会影响基因表达和细胞命运。p53在体内的动态变化仅在固定组织中或使用p53转录活性的报告基因进行过研究。在此,我们建立了表达p53水平荧光报告基因的乳腺肿瘤,并采用活体成像技术来量化其在体内对DSB反应的动态变化。我们的研究结果揭示了单个细胞之间存在很大的异质性,大多数细胞表现出单个延长的脉冲。然后,我们测试了在高细胞汇合度(细胞培养和组织之间的一个不同因素)下p53动态变化可能如何改变。我们发现高度汇合的培养乳腺癌细胞也显示出一个宽泛的p53脉冲而不是振荡。通过数学建模、敏感性分析和活细胞成像,我们确定磷酸酶Wip1(p53的转录靶点和负调节因子)的低水平是这些动态变化的关键因素。由于高细胞汇合度能更好地反映组织的微环境,细胞汇合度对p53动态变化的影响可能对癌组织对DNA损伤诱导疗法的反应具有重要意义。