Umezawa Yoshihiro, Kurosu Tetsuya, Akiyama Hiroki, Wu Nang, Nogami Ayako, Nagao Toshikage, Miura Osamu
Department of Hematology, Graduate School of Medical and Dental Sciences, and Graduate School of Biomedical Science, Institute of Biomaterials and Bioengineering, Tokyo Medical and Dental University, Tokyo, Japan.
Oncotarget. 2016 Jul 12;7(28):44448-44461. doi: 10.18632/oncotarget.9844.
DNA-damaging chemotherapeutic agents activate apoptotic pathways in cancer cells. However, they also activate checkpoint mechanisms mainly involving Chk1 and p53 to arrest cell cycle progression, thus abbreviating their cytotoxic effects. We previously found that aberrant tyrosine kinases involved in leukemogenesis, such as BCR/ABL and Jak2-V617F, as well as Jak2 activated by hematopoietic cytokines enhance Chk1-mediated G2/M arrest through the PI3K/Akt/GSK3 pathway to confer resistance to chemotherapeutic agents, which was prevented by inhibition of these kinases or the downstream PI3K/Akt pathway. However, the possible involvement of p53 in regulation of Chk1-mediated G2/M checkpoint has remained to be elucidated. We demonstrate here that a dominant negative mutant of p53, p53-DD, increases Chk1-mediated G2/M checkpoint activation induced by chemotherapeutics and protects it from down regulation by inhibition of Jak2, BCR/ABL, or the PI3K/Akt pathway in hematopoietic model cell lines 32D and BaF3 or their transformants by BCR/ABL. Consistent with this, the p53 activator nutlin-3 synergistically induced apoptosis with chemotherapeutics by inhibiting Chk1-mediated G2/M arrest in these cells, including cells transformed by the T315I mutant of BCR/ABL resistant to various kinase inhibitors in clinical use. Further studies suggest that p53 may inhibit the Chk1 pathway by its transcription-dependent function and through mechanisms involving the proteasomal system, but not the PI3K/Akt/GSK3 pathway. The present study may shed a new light on molecular mechanisms for the therapy resistance of p53-mutated hematological malignancies and would provide valuable information for the development of novel therapeutic strategies against these diseases with dismal prognosis.
DNA损伤性化疗药物可激活癌细胞中的凋亡途径。然而,它们也会激活主要涉及Chk1和p53的检查点机制,以阻止细胞周期进程,从而缩短其细胞毒性作用。我们之前发现,参与白血病发生的异常酪氨酸激酶,如BCR/ABL和Jak2-V617F,以及由造血细胞因子激活的Jak2,通过PI3K/Akt/GSK3途径增强Chk1介导的G2/M期阻滞,从而赋予对化疗药物的抗性,抑制这些激酶或下游PI3K/Akt途径可阻止这种抗性。然而,p53在Chk1介导的G2/M检查点调节中的可能作用仍有待阐明。我们在此证明,p53的显性负性突变体p53-DD可增强化疗药物诱导的Chk1介导的G2/M检查点激活,并保护其免受造血模型细胞系32D和BaF3或其BCR/ABL转化体中Jak2、BCR/ABL或PI3K/Akt途径抑制的下调作用。与此一致的是,p53激活剂nutlin-3通过抑制这些细胞中Chk1介导的G2/M期阻滞,与化疗药物协同诱导凋亡,这些细胞包括对临床使用的各种激酶抑制剂耐药的BCR/ABL T315I突变体转化的细胞。进一步的研究表明,p53可能通过其转录依赖性功能并通过涉及蛋白酶体系统的机制抑制Chk1途径,但不抑制PI3K/Akt/GSK3途径。本研究可能为p53突变的血液系统恶性肿瘤的治疗抗性分子机制提供新的线索,并为开发针对这些预后不良疾病的新型治疗策略提供有价值的信息。