Dacheux Mélanie A, Lee Sue Chin, Shin Yoojin, Norman Derek D, Lin Kuan-Hung, E Shuyu, Yue Junming, Benyó Zoltán, Tigyi Gábor J
Department of Physiology, College of Medicine, University of Tennessee Health Science Center (UTHSC), Memphis, TN 38163, USA.
Department of Pathology and Laboratory Medicine, College of Medicine, University of Tennessee Health Science Center (UTHSC), Memphis, TN 38163, USA.
Cancers (Basel). 2022 Mar 21;14(6):1586. doi: 10.3390/cancers14061586.
Although metastases are the principal cause of cancer-related deaths, the molecular aspects of the role of stromal cells in the establishment of the metastatic niche remain poorly understood. One of the most prevalent sites for cancer metastasis is the lungs. According to recent research, lung stromal cells such as bronchial epithelial cells and resident macrophages secrete autotaxin (ATX), an enzyme with lysophospholipase D activity that promotes cancer progression. In fact, several studies have shown that many cell types in the lung stroma could provide a rich source of ATX in diseases. In the present study, we sought to determine whether ATX derived from alveolar type II epithelial (ATII) pneumocytes could modulate the progression of lung metastasis, which has not been evaluated previously. To accomplish this, we used the B16-F10 syngeneic melanoma model, which readily metastasizes to the lungs when injected intravenously. Because B16-F10 cells express high levels of ATX, we used the CRISPR-Cas9 technology to knock out the ATX gene in B16-F10 cells, eliminating the contribution of tumor-derived ATX in lung metastasis. Next, we used the inducible Cre/loxP system (Sftpc-CreERT2/Enpp2fl/fl) to generate conditional knockout (KO) mice in which ATX is specifically deleted in ATII cells (i.e., Sftpc-KO). Injection of ATX-KO B16-F10 cells into Sftpc-KO or Sftpc-WT control littermates allowed us to investigate the specific contribution of ATII-derived ATX in lung metastasis. We found that targeted KO of ATX in ATII cells significantly reduced the metastatic burden of ATX-KO B16-F10 cells by 30% (unpaired t-test, p = 0.028) compared to Sftpc-WT control mice, suggesting that ATX derived from ATII cells could affect the metastatic progression. We detected upregulated levels of cytokines such as IFNγ (unpaired t-test, p < 0.0001) and TNFα (unpaired t-test, p = 0.0003), which could favor the increase in infiltrating CD8+ T cells observed in the tumor regions of Sftpc-KO mice. Taken together, our results highlight the contribution of host ATII cells as a stromal source of ATX in the progression of melanoma lung metastasis.
尽管转移是癌症相关死亡的主要原因,但基质细胞在转移小生境形成中所起作用的分子机制仍知之甚少。癌症转移最常见的部位之一是肺部。根据最近的研究,支气管上皮细胞和驻留巨噬细胞等肺基质细胞会分泌自分泌运动因子(ATX),这是一种具有溶血磷脂酶D活性的酶,可促进癌症进展。事实上,多项研究表明,肺基质中的许多细胞类型在疾病中都可能是ATX的丰富来源。在本研究中,我们试图确定源自II型肺泡上皮(ATII)肺细胞的ATX是否能调节肺转移的进程,此前尚未对此进行评估。为了实现这一目标,我们使用了B16-F10同基因黑色素瘤模型,该模型静脉注射后很容易转移到肺部。由于B16-F10细胞表达高水平的ATX,我们使用CRISPR-Cas9技术敲除B16-F10细胞中的ATX基因,消除肿瘤源性ATX在肺转移中的作用。接下来,我们使用诱导型Cre/loxP系统(Sftpc-CreERT2/Enpp2fl/fl)生成条件性敲除(KO)小鼠,其中ATX在ATII细胞中被特异性删除(即Sftpc-KO)。将ATX-KO B16-F10细胞注射到Sftpc-KO或Sftpc-WT对照同窝小鼠体内,使我们能够研究源自ATII的ATX在肺转移中的具体作用。我们发现,与Sftpc-WT对照小鼠相比,ATII细胞中ATX的靶向敲除显著降低了ATX-KO B16-F10细胞30%的转移负担(未配对t检验,p = 0.028),这表明源自ATII细胞的ATX可能影响转移进程。我们检测到细胞因子如IFNγ(未配对t检验,p < 0.0001)和TNFα(未配对t检验,p = 0.0003)的水平上调,这可能有助于Sftpc-KO小鼠肿瘤区域中浸润的CD8+ T细胞增加。综上所述,我们的结果突出了宿主ATII细胞作为黑色素瘤肺转移进程中ATX的基质来源所起的作用。