Elghonaimy Eslam A, Ibrahim Sherif A, Youns Amal, Hussein Zeinab, Nouh Mohamed Akram, El-Mamlouk Tahani, El-Shinawi Mohamed, Mostafa Mohamed Mona
Department of Zoology, Faculty of Science, Cairo University, Giza, 12613, Egypt.
Department of Pathology, National Cancer Institute, Cairo University, Giza, 12613, Egypt.
Tumour Biol. 2016 Sep;37(9):12441-12453. doi: 10.1007/s13277-016-5123-x. Epub 2016 Jun 22.
Epithelial-mesenchymal transition (EMT) is an essential process in breast cancer metastasis. The aim of the present study was to determine the role of secretions of tumor-associated leukocytes (TALs) isolated from negative and positive lymph nodes (nLNs and pLNs, respectively) breast cancer patients in regulating EMT mechanism and the associated signaling pathways. We found an increased infiltration of TALs, which was associated with downregulation of E-cadherin and over-expression of vimentin in the breast carcinoma tissues of pLNs as compared to nLNs patients and normal breast tissues obtained from healthy volunteers during mammoplasty. Furthermore, TALs isolated from pLNs breast cancer patients secreted an elevated panel of cytokines by up to 2-5-fold when compared with those isolated from nLNs patients. Secretome of TALs of pLNs possessed higher TARC, IGF-1, IL-3, TNF-β, IL-5, G-CSF, IL-4, and IL-1α with more than a fivefold compared to those of nLNs. Using the human breast cancer cell lines MCF-7 and MDA-MB-231, we found that cytokines secreted by TALs isolated from nLNs and pLNs breast cancer patients promoted EMT via upregulation of TGF-β and vimentin and downregulation of E-cadherin at messenger RNA (mRNA) levels in both cell lines and at protein level in MCF-7. While TGF-β is over-expressed by MDA-MB-231 seeded in media conditioned by secretome of TALs isolated from nLNs and pLNs breast cancer patients. The downstream TGF-β signaling transcription factors, Snail, Slug, and Twist, known to be associated with EMT mechanism were over-expressed by MCF-7 and MDA-MB-231 seeded in media conditioned by secretome of TALs isolated from nLNs and pLNs breast cancer patients. Acquisition of EMT in MCF-7 cells is mechanistically attributed to the activation of EGFR and NF-κB/p65 signaling which are significantly highly expressed by MCF-7 cells seeded in media conditioned by secretome of TALs isolated from pLNs compared to nLNs patients. Overall, this study provides implications of secretome of TALs and activated EGFR and NF-κB/p65 in EMT process that may be considered a therapeutic strategy to inhibit lymph node metastasis in breast cancer patients.
上皮-间质转化(EMT)是乳腺癌转移过程中的一个重要环节。本研究的目的是确定从乳腺癌患者的阴性和阳性淋巴结(分别为nLNs和pLNs)中分离出的肿瘤相关白细胞(TALs)分泌物在调节EMT机制及相关信号通路中的作用。我们发现,与nLNs患者以及隆乳术中从健康志愿者获取的正常乳腺组织相比,pLNs乳腺癌组织中TALs浸润增加,这与E-钙黏蛋白下调和波形蛋白过表达有关。此外,与从nLNs患者中分离出的TALs相比,从pLNs乳腺癌患者中分离出的TALs分泌的细胞因子水平升高了2至5倍。pLNs的TALs分泌组中TARC、IGF-1、IL-3、TNF-β、IL-5、G-CSF、IL-4和IL-1α的含量比nLNs的高出五倍以上。使用人乳腺癌细胞系MCF-7和MDA-MB-231,我们发现从nLNs和pLNs乳腺癌患者中分离出的TALs分泌的细胞因子在mRNA水平上通过上调TGF-β和波形蛋白以及下调E-钙黏蛋白促进了这两种细胞系中的EMT,在MCF-7细胞中还在蛋白质水平上促进了EMT。而接种在由从nLNs和pLNs乳腺癌患者中分离出的TALs分泌组处理过的培养基中的MDA-MB-231细胞中TGF-β过表达。已知与EMT机制相关的下游TGF-β信号转录因子Snail、Slug和Twist在接种于由从nLNs和pLNs乳腺癌患者中分离出的TALs分泌组处理过的培养基中的MCF-7和MDA-MB-231细胞中过表达。MCF-7细胞中EMT的获得在机制上归因于EGFR和NF-κB/p65信号的激活,与接种于由从nLNs患者中分离出的TALs分泌组处理过的培养基中的MCF-7细胞相比,接种于由从pLNs患者中分离出的TALs分泌组处理过的培养基中的MCF-7细胞中这两种信号显著高表达。总体而言,本研究揭示了TALs分泌组以及激活的EGFR和NF-κB/p65在EMT过程中的作用,这可能被视为一种抑制乳腺癌患者淋巴结转移的治疗策略。