Sidney Kimmel Comprehensive Cancer Center, Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America.
PLoS Pathog. 2010 Aug 5;6(8):e1001031. doi: 10.1371/journal.ppat.1001031.
Viral replication efficiency is in large part governed by the ability of viruses to counteract pro-apoptotic signals induced by infection of the host cell. Human herpesvirus 8 (HHV-8) uses several strategies to block the host's innate antiviral defenses via interference with interferon and apoptotic signaling. Contributors include the four viral interferon regulatory factors (vIRFs 1-4), which function in dominant negative fashion to block cellular IRF activities in addition to targeting IRF signaling-induced proteins such as p53 and inhibiting other inducers of apoptosis such as TGFbeta receptor-activated Smad transcription factors. Here we identify direct targeting by vIRF-1 of BH3-only pro-apoptotic Bcl-2 family member Bim, a key negative regulator of HHV-8 replication, to effect its inactivation via nuclear translocation. vIRF-1-mediated relocalization of Bim was identified in transfected cells, by both immunofluorescence assay and western analysis of fractionated cell extracts. Also, co-localization of vIRF-1 and Bim was detected in nuclei of lytically infected endothelial cells. In vitro co-precipitation assays using purified vIRF-1 and Bim revealed direct interaction between the proteins, and Bim-binding residues of vIRF-1 were mapped by deletion and point mutagenesis. Generation and experimental utilization of Bim-refractory vIRF-1 variants revealed the importance of vIRF-1:Bim interaction, specifically, in pro-replication and anti-apoptotic activity of vIRF-1. Furthermore, blocking of the interaction with cell-permeable peptide corresponding to the Bim-binding region of vIRF-1 confirmed the relevance of vIRF-1:Bim association to vIRF-1 pro-replication activity. To our knowledge, this is the first report of an IRF protein that interacts with a Bcl-2 family member and of nuclear sequestration of Bim or any other member of the family as a means of inactivation. The data presented reveal a novel mechanism utilized by a virus to control replication-induced apoptosis and suggest that inhibitory targeting of vIRF-1:Bim interaction may provide an effective antiviral strategy.
病毒复制效率在很大程度上取决于病毒抵抗宿主细胞感染诱导的促凋亡信号的能力。人类疱疹病毒 8 型(HHV-8)利用几种策略通过干扰干扰素和凋亡信号来阻断宿主的先天抗病毒防御。贡献者包括四个病毒干扰素调节因子(vIRF1-4),它们以显性负性方式发挥作用,除了靶向 IRF 信号诱导的蛋白质(如 p53)外,还阻断细胞 IRF 活性,并抑制其他凋亡诱导剂,如 TGFβ受体激活的 Smad 转录因子。在这里,我们确定 vIRF-1 直接靶向 BH3 仅有的促凋亡 Bcl-2 家族成员 Bim,Bim 是 HHV-8 复制的关键负调控因子,通过核易位使其失活。通过免疫荧光测定法和细胞提取物的Western 分析,在转染细胞中鉴定出 vIRF-1 介导的 Bim 的再定位。此外,在裂解感染的内皮细胞的核中检测到 vIRF-1 和 Bim 的共定位。使用纯化的 vIRF-1 和 Bim 进行体外共沉淀测定揭示了蛋白质之间的直接相互作用,并通过缺失和点突变作图确定了 vIRF-1 与 Bim 的结合残基。生成和实验利用 Bim 抗性 vIRF-1 变体揭示了 vIRF-1:Bim 相互作用的重要性,特别是在 vIRF-1 的促复制和抗凋亡活性中。此外,用对应于 vIRF-1 的 Bim 结合区的细胞渗透性肽阻断相互作用证实了 vIRF-1:Bim 关联与 vIRF-1 促复制活性的相关性。据我们所知,这是第一个报道 IRF 蛋白与 Bcl-2 家族成员相互作用以及 Bim 或家族的任何其他成员的核隔离作为失活手段的报告。所提出的数据揭示了病毒控制复制诱导的凋亡的新机制,并表明抑制 vIRF-1:Bim 相互作用的靶向可能提供有效的抗病毒策略。