Chung Eun Joo, Hudak Kathryn, Horton Jason A, White Ayla, Scroggins Bradley T, Vaswani Shiva, Citrin Deborah
Radiation Oncology Branch, Center for Cancer Research, National Institutes of Health, Bethesda, Maryland.
Radiat Res. 2014 Sep;182(3):350-62. doi: 10.1667/RR13625.1. Epub 2014 Aug 12.
Radiation fibrosis of the lung is a late toxicity of thoracic irradiation. Epidermal growth factor (EGF) signaling has previously been implicated in radiation lung injury. We hypothesized that TGF-α, an EGF receptor ligand, plays a key role in radiation-induced fibrosis in lung. Mice deficient in transforming growth factor (TGF-α(-/-)) and control C57Bl/6J (C57-WT) mice were exposed to thoracic irradiation in 5 daily fractions of 6 Gy. Cohorts of mice were followed for survival (n ≥ 5 per group) and tissue collection (n = 3 per strain and time point). Collagen accumulation in irradiated lungs was assessed by Masson's trichrome staining and analysis of hydroxyproline content. Cytokine levels in lung tissue were assessed with ELISA. The effects of TGF-α on pneumocyte and fibroblast proliferation and collagen production were analyzed in vitro. Lysyl oxidase (LOX) expression and activity were measured in vitro and in vivo. Irradiated C57-WT mice had a median survival of 24.4 weeks compared to 48.2 weeks for irradiated TGF-α(-/-) mice (P = 0.001). At 20 weeks after irradiation, hydroxyproline content was markedly increased in C57-WT mice exposed to radiation compared to TGF-α(-/-) mice exposed to radiation or unirradiated C57-WT mice (63.0, 30.5 and 37.6 μg/lung, respectively, P = 0.01). C57-WT mice exposed to radiation had dense foci of subpleural fibrosis at 20 weeks after exposure, whereas the lungs of irradiated TGF-α (-/-) mice were largely devoid of fibrotic foci. Lung tissue concentrations of IL-1β, IL-4, TNF-α, TGF-β and EGF at multiple time points after irradiation were similar in C57-WT and TGF-α(-/-) mice. TGF-α in lung tissue of C57-WT mice rose rapidly after irradiation and remained elevated through 20 weeks. TGF-α(-/-) mice had lower basal LOX expression than C57-WT mice. Both LOX expression and LOX activity were increased after irradiation in all mice but to a lesser degree in TGF-α(-/-) mice. Treatment of NIH-3T3 fibroblasts with TGF-α resulted in increases in proliferation, collagen production and LOX activity. These studies identify TGF-α as a critical mediator of radiation-induced lung injury and a novel therapeutic target in this setting. Further, these data implicate TGF-α as a mediator of collagen maturation through a TGF-β independent activation of lysyl oxidase.
放射性肺纤维化是胸部放疗的晚期毒性反应。表皮生长因子(EGF)信号通路先前已被证明与放射性肺损伤有关。我们推测,作为一种EGF受体配体,转化生长因子-α(TGF-α)在放射性肺纤维化中起关键作用。将缺乏转化生长因子(TGF-α(-/-))的小鼠和对照C57Bl/6J(C57-WT)小鼠每天分5次给予6 Gy的胸部照射。对各小鼠队列进行生存情况跟踪(每组n≥5)和组织采集(每个品系和时间点n = 3)。通过Masson三色染色和羟脯氨酸含量分析评估照射后肺组织中的胶原蛋白积累情况。用酶联免疫吸附测定法(ELISA)评估肺组织中的细胞因子水平。在体外分析TGF-α对肺上皮细胞和成纤维细胞增殖及胶原蛋白产生的影响。在体外和体内测量赖氨酰氧化酶(LOX)的表达和活性。照射后的C57-WT小鼠中位生存期为24.4周,而照射后的TGF-α(-/-)小鼠为48.2周(P = 0.001)。照射后20周,与接受照射的TGF-α(-/-)小鼠或未照射的C57-WT小鼠相比,接受照射的C57-WT小鼠肺组织中的羟脯氨酸含量显著增加(分别为63.0、30.5和37.6μg/肺,P = 0.01)。接受照射的C57-WT小鼠在照射后20周出现胸膜下纤维化致密灶,而照射后的TGF-α(-/-)小鼠肺部基本没有纤维化灶。照射后多个时间点,C57-WT小鼠和TGF-α(-/-)小鼠肺组织中白细胞介素-1β(IL-1β)、白细胞介素-4(IL-4)、肿瘤坏死因子-α(TNF-α)、转化生长因子-β(TGF-β)和表皮生长因子(EGF)的浓度相似。照射后,C57-WT小鼠肺组织中的TGF-α迅速升高,并在20周内一直保持在较高水平。TGF-α(-/-)小鼠的基础LOX表达低于C57-WT小鼠。照射后,所有小鼠的LOX表达和活性均增加,但TGF-α(-/-)小鼠增加的程度较小。用TGF-α处理NIH-3T3成纤维细胞会导致细胞增殖、胶原蛋白产生和LOX活性增加。这些研究确定TGF-α是放射性肺损伤的关键介质以及在这种情况下的新型治疗靶点。此外,这些数据表明TGF-α通过独立于TGF-β激活赖氨酰氧化酶而成为胶原蛋白成熟的介质。