Browne Ashley, Tookman Laura A, Ingemarsdotter Carin K, Bouwman Russell D, Pirlo Katrina, Wang Yaohe, McNeish Iain A, Lockley Michelle
Barts Cancer Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom.
Barts Cancer Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom. Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.
Cancer Res. 2015 Jul 15;75(14):2811-21. doi: 10.1158/0008-5472.CAN-14-3761. Epub 2015 May 14.
Adenoviruses have been clinically tested as anticancer therapies but their utility has been severely limited by rapid, systemic cytokine release and consequent inflammatory toxicity. Here, we describe a new approach to tackling these dangerous side effects. Using human ovarian cancer cell lines as well as malignant epithelial cells harvested from the ascites of women with ovarian cancer, we show that tumor cells do not produce cytokines in the first 24 hours following in vitro infection with the oncolytic adenovirus dl922-947. In contrast, dl922-947 does induce inflammatory cytokines at early time points following intraperitoneal delivery in mice with human ovarian cancer intraperitoneal xenografts. In these animals, cytokines originate predominantly in murine tissues, especially in macrophage-rich organs such as the spleen. We use a nonreplicating adenovirus to confirm that early cytokine production is independent of adenoviral replication. Using β3 integrin knockout mice injected intraperitoneally with dl922-947 and β3 null murine peritoneal macrophages, we confirm a role for macrophage cell surface β3 integrin in this dl922-947-induced inflammation. We present new evidence that co-administration of a cyclic RGD-mimetic-specific inhibitor of β3 integrin significantly attenuates the cytokine release and inflammatory hepatic toxicity induced by dl922-947 in an intraperitoneal murine model of ovarian cancer. Importantly, we find no evidence that β3 inhibition compromises viral infectivity and oncolysis in vitro or anticancer efficacy in vivo. By enabling safe, systemic delivery of replicating adenoviruses, this novel approach could have a major impact on the future development of these effective anticancer agents.
腺病毒已作为抗癌疗法进行了临床试验,但其效用因快速的全身性细胞因子释放及随之而来的炎症毒性而受到严重限制。在此,我们描述了一种应对这些危险副作用的新方法。利用人卵巢癌细胞系以及从卵巢癌女性腹水中收集的恶性上皮细胞,我们发现肿瘤细胞在体外感染溶瘤腺病毒dl922 - 947后的最初24小时内不产生细胞因子。相比之下,dl922 - 947在接种人卵巢癌腹腔异种移植物的小鼠腹腔给药后的早期时间点确实会诱导炎症细胞因子产生。在这些动物中,细胞因子主要起源于小鼠组织,尤其是在富含巨噬细胞的器官如脾脏中。我们使用一种非复制型腺病毒来证实早期细胞因子的产生与腺病毒复制无关。通过给β3整合素基因敲除小鼠腹腔注射dl922 - 947以及β3基因缺失的小鼠腹腔巨噬细胞,我们证实了巨噬细胞表面β3整合素在这种由dl922 - 947诱导的炎症中的作用。我们提供了新的证据表明,在卵巢癌腹腔小鼠模型中,联合给予β3整合素的环状RGD模拟特异性抑制剂可显著减轻dl922 - 947诱导的细胞因子释放和炎症性肝毒性。重要的是,我们没有发现证据表明β3抑制会损害体外病毒感染性和溶瘤作用或体内抗癌疗效。通过实现复制型腺病毒的安全全身递送,这种新方法可能会对这些有效抗癌药物的未来发展产生重大影响。