Suman Shubhankar, Moon Bo-Hyun, Thakor Hemang, Fornace Albert J, Datta Kamal
a Department of Biochemistry and Molecular and Cellular Biology and Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC 20057.
Radiat Res. 2014 Sep;182(3):345-9. doi: 10.1667/RR13770.1. Epub 2014 Aug 12.
Low-linear energy transfer (low-LET) γ-ray exposure is a risk factor for colorectal cancer (CRC). Due to their high-LET nature, energetic iron ions found in space are expected to pose greater CRC risks to astronauts undertaking long-duration space missions beyond low Earth orbit. Wild-type p53-induced phosphatase 1 (Wip1) is important for cellular DNA damage response and its abrogation has been shown to inhibit spontaneous intestinal tumorigenesis in APC(Min/+) mice, a well-studied mouse model of human CRC. However, the relationship of Wip1 to radiation-induced intestinal tumorigenesis, especially by energetic iron ions, has not been investigated in APC(Min/+) mice. We have previously reported that there is a greater intestinal tumorigenic potential of iron-ion radiation relative to (137)Cs γ rays, so the purpose of the current study was to investigate whether Wip1 abrogation could influence high-LET dependent intestinal tumorigenesis in APC(Min/+) mice. Intestinal tumor frequency and grade were assessed in APC(Min/+)/Wip1(-/-) mice and results were compared to those in APC(Min/+)/Wip1(+/+) mice after exposure to a mean absorbed dose of 2 Gy from (137)Cs γ rays or 1.6 Gy from 1 GeV/n iron ions. Cellular differentiation and proliferation were also assessed in the intestinal tumors of sham-irradiated and irradiated mice. Decreased tumor frequency and lower tumor grade were observed in APC(Min/+)/Wip1(-/-) relative to APC(Min/+)/Wip1(+/+) mice. Notably, a similar decrease (∼6-fold in both groups) in tumor number was observed in sham-irradiated and γ-irradiated APC(Min/+)/Wip1(-/-) relative to APC(Min/+)/Wip1(+/+) mice. However, tumorigenesis in the energetic iron-ion exposed group was reduced ∼8-fold in APC(Min/+)/Wip1(-/-) relative to APC(Min/+)/Wip1(+/+) mice. A significantly lower proliferation/differentiation index in tumors of iron-ion exposed APC(Min/+)/Wip1(-/-) relative to APC(Min/+)/Wip1(+/+) mice suggests that reduced proliferation and enhanced differentiation as a result of Wip1 abrogation maybe involved. In conclusion, the current study demonstrated that the absence of Wip1 blocked radiation-induced intestinal tumorigenesis irrespective of radiation quality and has implications for developing preventive strategies against the tumorigenic potential of radiation exposure on earth and in outer space.
低线性能量转移(low-LET)γ射线照射是结直肠癌(CRC)的一个风险因素。由于其高线性能量转移特性,在太空中发现的高能铁离子预计会给执行低地球轨道以外的长期太空任务的宇航员带来更大的结直肠癌风险。野生型p53诱导磷酸酶1(Wip1)对细胞DNA损伤反应很重要,并且已证明其缺失可抑制APC(Min/+)小鼠(一种经过充分研究的人类结直肠癌小鼠模型)的自发性肠道肿瘤发生。然而,在APC(Min/+)小鼠中尚未研究Wip1与辐射诱导的肠道肿瘤发生的关系,尤其是高能铁离子诱导的关系。我们之前报道过,相对于(137)Csγ射线,铁离子辐射具有更大的肠道肿瘤发生潜力,因此本研究的目的是调查Wip1缺失是否会影响APC(Min/+)小鼠中依赖高线性能量转移的肠道肿瘤发生。评估了APC(Min/+)/Wip1(-/-)小鼠的肠道肿瘤频率和分级,并将结果与暴露于平均吸收剂量为2 Gy的(137)Csγ射线或1.6 Gy的1 GeV/n铁离子后的APC(Min/+)/Wip1(+/+)小鼠的结果进行比较。还评估了假照射和照射小鼠肠道肿瘤中的细胞分化和增殖情况。相对于APC(Min/+)/Wip1(+/+)小鼠,在APC(Min/+)/Wip1(-/-)小鼠中观察到肿瘤频率降低和肿瘤分级降低。值得注意的是,相对于APC(Min/+)/Wip1(+/+)小鼠,在假照射和γ射线照射的APC(Min/+)/Wip1(-/-)小鼠中观察到肿瘤数量有类似的减少(两组均约为6倍)。然而,相对于APC(Min/+)/Wip1(+/+)小鼠,在高能铁离子暴露组中,APC(Min/+)/Wip1(-/-)小鼠的肿瘤发生减少了约8倍。相对于APC(Min/+)/Wip1(+/+)小鼠,铁离子暴露的APC(Min/+)/Wip1(-/-)小鼠肿瘤中显著更低的增殖/分化指数表明,Wip1缺失导致的增殖减少和分化增强可能与之有关。总之,本研究表明,无论辐射质量如何,Wip1的缺失均可阻断辐射诱导的肠道肿瘤发生,这对于制定针对地球和外层空间辐射暴露致癌潜力的预防策略具有重要意义。