Fan Ming-Hui, Zhu Qiang, Li Hui-Hua, Ra Hyun-Jeong, Majumdar Sonali, Gulick Dexter L, Jerome Jacob A, Madsen Daniel H, Christofidou-Solomidou Melpo, Speicher David W, Bachovchin William W, Feghali-Bostwick Carol, Puré Ellen
From the Pulmonary, Allergy, and Critical Care Division, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
the Molecular and Cellular Pathology Graduate Program, University of North Carolina at Chapel Hill Chapel Hill, North Carolina 27599.
J Biol Chem. 2016 Apr 8;291(15):8070-89. doi: 10.1074/jbc.M115.701433. Epub 2015 Dec 9.
Idiopathic pulmonary fibrosis is a disease characterized by progressive, unrelenting lung scarring, with death from respiratory failure within 2-4 years unless lung transplantation is performed. New effective therapies are clearly needed. Fibroblast activation protein (FAP) is a cell surface-associated serine protease up-regulated in the lungs of patients with idiopathic pulmonary fibrosis as well as in wound healing and cancer. We postulate that FAP is not only a marker of disease but influences the development of pulmonary fibrosis after lung injury. In two different models of pulmonary fibrosis, intratracheal bleomycin instillation and thoracic irradiation, we find increased mortality and increased lung fibrosis in FAP-deficient mice compared with wild-type mice. Lung extracellular matrix analysis reveals accumulation of intermediate-sized collagen fragments in FAP-deficient mouse lungs, consistent within vitrostudies showing that FAP mediates ordered proteolytic processing of matrix metalloproteinase (MMP)-derived collagen cleavage products. FAP-mediated collagen processing leads to increased collagen internalization without altering expression of the endocytic collagen receptor, Endo180. Pharmacologic FAP inhibition decreases collagen internalization as expected. Conversely, restoration of FAP expression in the lungs of FAP-deficient mice decreases lung hydroxyproline content after intratracheal bleomycin to levels comparable with that of wild-type controls. Our findings indicate that FAP participates directly, in concert with MMPs, in collagen catabolism and clearance and is an important factor in resolving scar after injury and restoring lung homeostasis. Our study identifies FAP as a novel endogenous regulator of fibrosis and is the first to show FAP's protective effects in the lung.
特发性肺纤维化是一种以进行性、持续性肺瘢痕形成为特征的疾病,除非进行肺移植,否则患者会在2至4年内死于呼吸衰竭。显然需要新的有效治疗方法。成纤维细胞活化蛋白(FAP)是一种与细胞表面相关的丝氨酸蛋白酶,在特发性肺纤维化患者的肺中以及伤口愈合和癌症中上调。我们推测FAP不仅是疾病的标志物,而且会影响肺损伤后肺纤维化的发展。在两种不同的肺纤维化模型中,即气管内注射博来霉素和胸部照射,我们发现与野生型小鼠相比,FAP缺陷小鼠的死亡率增加且肺纤维化加重。肺细胞外基质分析显示,FAP缺陷小鼠肺中中等大小的胶原片段积累,这与体外研究一致,体外研究表明FAP介导基质金属蛋白酶(MMP)衍生的胶原裂解产物的有序蛋白水解加工。FAP介导的胶原加工导致胶原内化增加,而不改变内吞性胶原受体Endo180的表达。药理学上抑制FAP可如预期那样降低胶原内化。相反,在FAP缺陷小鼠的肺中恢复FAP表达可使气管内注射博来霉素后肺羟脯氨酸含量降低至与野生型对照相当的水平。我们的研究结果表明,FAP与MMP协同直接参与胶原分解代谢和清除,并且是损伤后解决瘢痕和恢复肺稳态的重要因素。我们的研究将FAP确定为纤维化的一种新型内源性调节因子,并且首次表明FAP在肺中的保护作用。