Ma Qi, Cavallin Lucas E, Yan Bin, Zhu Shoukang, Duran Elda Margarita, Wang Huili, Hale Laura P, Dong Chunming, Cesarman Ethel, Mesri Enrique A, Goldschmidt-Clermont Pascal J
Vascular Biology Institute, Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
Proc Natl Acad Sci U S A. 2009 May 26;106(21):8683-8. doi: 10.1073/pnas.0812688106. Epub 2009 May 8.
Kaposi's sarcoma (KS) is the major AIDS-associated malignancy. It is characterized by the proliferation of spindle cells, inflammatory infiltrate, and aberrant angiogenesis caused by Kaposi's sarcoma herpesvirus (KSHV) infection. Small GTPase Rac1, an inflammatory signaling mediator triggering reactive oxygen species (ROS) production by NADPH-oxidases, is implicated in carcinogenesis and tumor angiogenesis. Here, we show that expression of a constitutively active Rac1 (RacCA) driven by the alpha-smooth muscle actin promoter in transgenic mice is sufficient to cause KS-like tumors through mechanisms involving ROS-driven proliferation, up-regulation of AKT signaling, and hypoxia-inducible factor 1-alpha-related angiogenesis. RacCA-induced tumors expressed KS phenotypic markers; displayed remarkable transcriptome overlap with KS lesions; and were, like KS, associated with male gender. The ROS scavenging agent N-acetyl-cysteine inhibited angiogenesis and completely abrogated transgenic RacCA tumor formation, indicating a causal role of ROS in tumorigenesis. Consistent with a pathogenic role in KS, immunohistochemical analysis revealed that Rac1 is overexpressed in KSHV(+) spindle cells of AIDS-KS biopsies. Our results demonstrate the direct oncogenicity of Rac1 and ROS and their contribution to a KS-like malignant phenotype, further underscoring the carcinogenic potential of oxidative stress in the context of chronic infection and inflammation. They define the RacCA transgenic mouse as a model suitable for studying the role of oxidative stress in the pathogenesis and therapy of KS, with relevance to other inflammation-related malignancies. Our findings suggest host and viral genes triggering Rac1 or ROS production as key determinants of KS onset and potential KS chemopreventive or therapeutic targets.
卡波西肉瘤(KS)是与艾滋病相关的主要恶性肿瘤。其特征是由卡波西肉瘤疱疹病毒(KSHV)感染引起的梭形细胞增殖、炎症浸润和异常血管生成。小GTP酶Rac1是一种炎症信号介质,可通过NADPH氧化酶触发活性氧(ROS)的产生,与致癌作用和肿瘤血管生成有关。在此,我们表明,在转基因小鼠中,由α-平滑肌肌动蛋白启动子驱动的组成型活性Rac1(RacCA)的表达足以通过涉及ROS驱动的增殖、AKT信号上调和缺氧诱导因子1-α相关血管生成的机制导致KS样肿瘤。RacCA诱导的肿瘤表达KS表型标志物;与KS病变显示出显著的转录组重叠;并且与KS一样,与男性性别有关。ROS清除剂N-乙酰半胱氨酸抑制血管生成并完全消除转基因RacCA肿瘤形成,表明ROS在肿瘤发生中起因果作用。与在KS中的致病作用一致,免疫组织化学分析显示Rac1在艾滋病相关KS活检的KSHV(+)梭形细胞中过表达。我们的结果证明了Rac1和ROS的直接致癌性及其对KS样恶性表型的贡献,进一步强调了在慢性感染和炎症背景下氧化应激的致癌潜力。它们将RacCA转基因小鼠定义为适合研究氧化应激在KS发病机制和治疗中的作用的模型,与其他炎症相关恶性肿瘤相关。我们的发现表明,触发Rac1或ROS产生的宿主和病毒基因是KS发病的关键决定因素以及潜在的KS化学预防或治疗靶点。