Poghosyan Susanna, Frenkel Nicola, van den Bent Lotte, Raats Danielle, Spaapen Tessa, Laoukili Jamila, Borel Rinkes Inne, Kranenburg Onno, Hagendoorn Jeroen
Laboratory for Translational Oncology and Department of Surgical Oncology, Division of Imaging and Cancer, University Medical Center Utrecht and Utrecht University, Heidelberglaan 100, 3584CX, Utrecht, The Netherlands.
Br J Cancer. 2025 Jan;132(1):69-80. doi: 10.1038/s41416-024-02892-4. Epub 2024 Nov 9.
The formation of lung metastasis as part of the progression of colon cancer is a poorly understood process. Theoretically, liver metastases could seed lung metastases.
To assess the contribution of the liver lymphatic vasculature to metastatic spread to the lungs, we generated murine liver-metastasis-derived organoids overexpressing vascular endothelial growth factor (VEGF)-C. The organoids were reimplanted into the mouse liver for tumour generation and onward metastasis.
Liver metastases from patients with concomitant lung metastases showed higher expression of VEGF-C, lymphatic vessel hyperplasia, and tumour cell invasion into lymphatic vessels when compared to those without lung metastases. Reimplantation of VEGF-C overexpressing organoids into the mouse liver showed that VEGF-C caused peritumoral lymphatic vessel hyperplasia, lymphatic tumour cell invasion, and lung metastasis formation. This change in metastatic organotropism was accompanied by reduced expression of WNT-driven adult stem cell markers, and increased expression of fetal stem cell markers and NOTCH pathway genes. Further NOTCH pathway inhibition with γ-secretase inhibitor (DAPT) in vivo results in a slight reduction in lung metastases and a decrease in lymphatic hyperplasia and invasion in VEGF-C-overexpressing tumours.
Collectively, these data indicate that VEGF-C can drive onward metastasis from the liver to the lung and suggest that targeting VEGF-C/NOTCH pathways may impair the progression of colorectal cancer.
作为结肠癌进展一部分的肺转移形成过程尚不清楚。理论上,肝转移可能引发肺转移。
为评估肝脏淋巴脉管系统对肺转移扩散的作用,我们构建了过表达血管内皮生长因子(VEGF)-C的源自小鼠肝转移的类器官。将这些类器官重新植入小鼠肝脏以生成肿瘤并继续发生转移。
与无肺转移的患者相比,伴有肺转移的患者肝转移灶中VEGF-C表达更高、淋巴管增生以及肿瘤细胞侵入淋巴管。将过表达VEGF-C的类器官重新植入小鼠肝脏显示,VEGF-C导致肿瘤周围淋巴管增生、淋巴管肿瘤细胞浸润及肺转移形成。这种转移器官趋向性的改变伴随着WNT驱动的成体干细胞标志物表达降低,以及胎儿干细胞标志物和NOTCH通路基因表达增加。体内用γ-分泌酶抑制剂(DAPT)进一步抑制NOTCH通路导致肺转移略有减少,且VEGF-C过表达肿瘤中淋巴管增生和浸润减少。
总体而言,这些数据表明VEGF-C可驱动从肝脏到肺的进一步转移,并提示靶向VEGF-C/NOTCH通路可能会损害结直肠癌的进展。