Pereira Joana F S, Bessa Cláudia, Matos Paulo, Jordan Peter
Department of Human Genetics, National Institute of Health 'Dr. Ricardo Jorge', 1649-016 Lisbon, Portugal.
BioISI-Biosystems & Integrative Sciences Institute, Faculty of Sciences, University of Lisbon, 1749-016 Lisbon, Portugal.
Cancers (Basel). 2022 Mar 9;14(6):1393. doi: 10.3390/cancers14061393.
An inflammatory microenvironment is a tumour-promoting condition that provides survival signals to which cancer cells respond with gene expression changes. One example is the alternative splicing variant Rat Sarcoma Viral Oncogene Homolog (Ras)-Related C3 Botulinum Toxin Substrate 1 (RAC1)B, which we previously identified in a subset of V-Raf Murine Sarcoma Viral Oncogene Homolog B (BRAF)-mutated colorectal tumours. RAC1B was also increased in samples from inflammatory bowel disease patients or in an acute colitis mouse model. Here, we used an epithelial-like layer of polarized Caco-2 or T84 colorectal cancer (CRC) cells in co-culture with fibroblasts, monocytes or macrophages and analysed the effect on RAC1B expression in the CRC cells by RT-PCR, Western blot and confocal fluorescence microscopy. We found that the presence of cancer-associated fibroblasts and M1 macrophages induced the most significant increase in RAC1B levels in the polarized CRC cells, accompanied by a progressive loss of epithelial organization. Under these conditions, we identified interleukin (IL)-6 as the main trigger for the increase in RAC1B levels, associated with Signal Transducer and Activator of Transcription (STAT)3 activation. IL-6 neutralization by a specific antibody abrogated both RAC1B overexpression and STAT3 phosphorylation in polarized CRC cells. Our data identify that pro-inflammatory extracellular signals from stromal cells can trigger the overexpression of tumour-related RAC1B in polarized CRC cells. The results will help to understand the tumour-promoting effect of inflammation and identify novel therapeutic strategies.
炎症微环境是一种促进肿瘤生长的条件,它提供生存信号,癌细胞会通过基因表达变化对这些信号作出反应。一个例子是可变剪接变体鼠肉瘤病毒癌基因同源物(Ras)相关的C3肉毒杆菌毒素底物1(RAC1)B,我们之前在一部分V-Raf鼠肉瘤病毒癌基因同源物B(BRAF)突变的结直肠癌肿瘤中鉴定到了它。在炎症性肠病患者的样本或急性结肠炎小鼠模型中,RAC1B也有所增加。在这里,我们将极化的Caco-2或T84结肠癌细胞的上皮样层与成纤维细胞、单核细胞或巨噬细胞共培养,并通过逆转录聚合酶链反应(RT-PCR)、蛋白质免疫印迹法和共聚焦荧光显微镜分析对结肠癌细胞中RAC1B表达的影响。我们发现,癌症相关成纤维细胞和M1巨噬细胞的存在会导致极化结肠癌细胞中RAC1B水平最显著的升高,同时伴随着上皮组织结构的逐渐丧失。在这些条件下,我们确定白细胞介素(IL)-6是RAC1B水平升高的主要触发因素,这与信号转导子和转录激活子(STAT)3的激活有关。用特异性抗体中和IL-6可消除极化结肠癌细胞中RAC1B的过表达和STAT3的磷酸化。我们的数据表明,来自基质细胞的促炎细胞外信号可触发极化结肠癌细胞中肿瘤相关RAC1B的过表达。这些结果将有助于理解炎症促进肿瘤生长的作用,并确定新的治疗策略。