Nguyen Hung N, Jeong Yunju, Kim Yunhye, Kamiya Mari, Kim Yaunghyun, Athar Humra, Castaldi Peter J, Hersh Craig P, Menon Jaivardhan A, Wong Jessie, Chan Ian, Oldham William M, Padera Robert F, Sharma Nirmal S, Sholl Lynette M, Vivero Marina, Watts Gerald F M, Knipe Rachel S, Black Katharine E, Hariri Lida P, Yun Jeong H, Merriam Louis T, Yuan Ke, Kim Edy Y, Brenner Michael B
Department of Medicine, Division of Rheumatology, Inflammation and Immunity, Brigham and Women's Hospital, Boston, MA 02115.
Harvard Medical School, Boston, MA 02115.
Proc Natl Acad Sci U S A. 2024 Dec 10;121(50):e2401899121. doi: 10.1073/pnas.2401899121. Epub 2024 Dec 5.
Fibrosis drives end-organ damage in many diseases. However, clinical trials targeting individual upstream activators of fibroblasts, such as TGFβ, have largely failed. Here, we target the leukemia inhibitory factor receptor (LIFR) as an "autocrine master amplifier" of multiple upstream activators of lung fibroblasts. In idiopathic pulmonary fibrosis (IPF), the most common fibrotic lung disease, we found that lung myofibroblasts had high LIF expression, and the fibroblasts in fibroblastic foci coexpressed LIF and LIFR. In IPF, fibroblastic foci are the "leading edge" of fibrosis and a key site of disease pathogenesis. TGFβ1, one of the principal drivers of fibrosis, up-regulated LIF expression in IPF fibroblasts. We found that TGFβ1, IL-4, and IL-13 stimulations of fibroblasts require the LIF-LIFR axis to evoke a strong fibrogenic effector response in fibroblasts. In vitro antibody blockade of LIFR on IPF lung fibroblasts reduced the induction of profibrotic genes after TGFβ1 stimulation. Silencing LIF and LIFR reduced profibrotic fibroblast activation following TGFβ1, IL-4, and IL-13 stimulations. We also demonstrated that LIFR amplified profibrotic stimuli in precision-cut lung slices from IPF patients. These LIFR signals were transduced via JAK2, and STAT1 in IPF lung fibroblasts. Together, we find that LIFR drives an autocrine circuit that amplifies and sustains pathogenic activation of IPF fibroblasts. Targeting a single, downstream master amplifier on fibroblasts, like LIFR, is an alternative therapeutic strategy that simultaneously attenuates the profibrotic effects of multiple upstream stimuli.
纤维化在许多疾病中导致终末器官损伤。然而,针对成纤维细胞单个上游激活因子(如转化生长因子β,TGFβ)的临床试验大多以失败告终。在此,我们将白血病抑制因子受体(LIFR)作为肺成纤维细胞多种上游激活因子的“自分泌主放大器”进行研究。在最常见的纤维化肺病——特发性肺纤维化(IPF)中,我们发现肺肌成纤维细胞有高表达的LIF,且纤维母细胞灶中的成纤维细胞共表达LIF和LIFR。在IPF中,纤维母细胞灶是纤维化的“前沿”和疾病发病机制的关键部位。TGFβ1是纤维化的主要驱动因子之一,可上调IPF成纤维细胞中的LIF表达。我们发现,TGFβ1、白细胞介素-4(IL-4)和白细胞介素-13对成纤维细胞的刺激需要LIF-LIFR轴才能在成纤维细胞中引发强烈的促纤维化效应反应。在体外,对IPF肺成纤维细胞的LIFR进行抗体阻断可减少TGFβ1刺激后促纤维化基因的诱导。沉默LIF和LIFR可降低TGFβ1、IL-4和IL-13刺激后促纤维化的成纤维细胞活化。我们还证明,LIFR在IPF患者的精密肺切片中放大了促纤维化刺激。这些LIFR信号通过JAK2和IPF肺成纤维细胞中的信号转导子和转录激活子1(STAT1)进行转导。我们共同发现,LIFR驱动一个自分泌回路,放大并维持IPF成纤维细胞的致病性激活。靶向成纤维细胞上单一的下游主放大器,如LIFR,是一种替代治疗策略,可同时减弱多种上游刺激的促纤维化作用。