Sasi Nanda Kumar, Bhutkar Arjun, Lanning Nathan J, MacKeigan Jeffrey P, Weinreich Michael
Laboratory of Genome Integrity and Tumorigenesis, Van Andel Research Institute (VARI), Grand Rapids, MI 49503; Laboratory of Systems Biology, VARI; Graduate Program in Genetics, Michigan State University, East Lansing, MI 48824.
David H. Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
Neoplasia. 2017 May;19(5):439-450. doi: 10.1016/j.neo.2017.03.001. Epub 2017 Apr 25.
DBF4-dependent kinase (DDK) is a two-subunit kinase required for initiating DNA replication at individual origins and is composed of CDC7 kinase and its regulatory subunit DBF4. Both subunits are highly expressed in many diverse tumor cell lines and primary tumors, and this is correlated with poor prognosis. Inhibiting DDK causes apoptosis of tumor cells, but not normal cells, through a largely unknown mechanism. Firstly, to understand why DDK is often overexpressed in tumors, we identified gene expression signatures that correlate with DDK high- and DDK low-expressing lung adenocarcinomas. We found that increased DDK expression is highly correlated with inactivation of RB1-E2F and p53 tumor suppressor pathways. Both CDC7 and DBF4 promoters bind E2F, suggesting that increased E2F activity in RB1 mutant cancers promotes increased DDK expression. Surprisingly, increased DDK expression levels are also correlated with both increased chemoresistance and genome-wide mutation frequencies. Our data further suggest that high DDK levels directly promote elevated mutation frequencies. Secondly, we performed an RNAi screen to investigate how DDK inhibition causes apoptosis of tumor cells. We identified 23 kinases and phosphatases required for apoptosis when DDK is inhibited. These hits include checkpoint genes, G2/M cell cycle regulators, and known tumor suppressors leading to the hypothesis that inhibiting mitotic progression can protect against DDKi-induced apoptosis. Characterization of one novel hit, the LATS2 tumor suppressor, suggests that it promotes apoptosis independently of the upstream MST1/2 kinases in the Hippo signaling pathway.
DBF4依赖激酶(DDK)是一种由两个亚基组成的激酶,是在各个起始点启动DNA复制所必需的,它由CDC7激酶及其调节亚基DBF4组成。这两个亚基在许多不同的肿瘤细胞系和原发性肿瘤中均高表达,且这与预后不良相关。抑制DDK会通过一种很大程度上未知的机制导致肿瘤细胞凋亡,但不会导致正常细胞凋亡。首先,为了理解为何DDK在肿瘤中常常过度表达,我们鉴定了与高表达和低表达DDK的肺腺癌相关的基因表达特征。我们发现DDK表达增加与RB1-E2F和p53肿瘤抑制途径的失活高度相关。CDC7和DBF4的启动子均结合E2F,这表明RB1突变型癌症中E2F活性增加会促进DDK表达增加。令人惊讶的是,DDK表达水平的增加还与化疗耐药性增加和全基因组突变频率增加相关。我们的数据进一步表明,高DDK水平直接促进突变频率升高。其次,我们进行了RNA干扰筛选,以研究DDK抑制如何导致肿瘤细胞凋亡。我们鉴定出了23种在DDK被抑制时凋亡所需的激酶和磷酸酶。这些命中基因包括检查点基因、G2/M细胞周期调节因子以及已知的肿瘤抑制因子,由此得出一个假设,即抑制有丝分裂进程可以预防DDKi诱导的凋亡。对一个新的命中基因——LATS2肿瘤抑制因子的特性分析表明,它在不依赖于Hippo信号通路中上游MST1/2激酶的情况下促进凋亡。