The Wistar Institute, Philadelphia, United States of America.
Department of Immunology, H. Lee Moffit Cancer and Research Center, Tampa Florida, United States of America.
PLoS Pathog. 2021 Jan 20;17(1):e1009231. doi: 10.1371/journal.ppat.1009231. eCollection 2021 Jan.
Liquid-liquid phase separation (LLPS) can drive formation of diverse and essential macromolecular structures, including those specified by viruses. Kaposi's Sarcoma-Associated Herpesvirus (KSHV) genomes associate with the viral encoded Latency-Associated Nuclear Antigen (LANA) to form stable nuclear bodies (NBs) during latent infection. Here, we show that LANA-NB formation and KSHV genome conformation involves LLPS. Using LLPS disrupting solvents, we show that LANA-NBs are partially disrupted, while DAXX and PML foci are highly resistant. LLPS disruption altered the LANA-dependent KSHV chromosome conformation but did not stimulate lytic reactivation. We found that LANA-NBs undergo major morphological transformation during KSHV lytic reactivation to form LANA-associated replication compartments encompassing KSHV DNA. DAXX colocalizes with the LANA-NBs during latency but is evicted from the LANA-associated lytic replication compartments. These findings indicate the LANA-NBs are dynamic super-molecular nuclear structures that partly depend on LLPS and undergo morphological transitions corresponding to the different modes of viral replication.
液-液相分离(LLPS)可以驱动多种必需的大分子结构的形成,包括病毒指定的结构。卡波济肉瘤相关疱疹病毒(KSHV)基因组与病毒编码的潜伏相关核抗原(LANA)结合,在潜伏感染期间形成稳定的核体(NBs)。在这里,我们表明 LANA-NB 的形成和 KSHV 基因组构象涉及液-液相分离。使用液-液相分离破坏溶剂,我们表明 LANA-NBs 部分被破坏,而 DAXX 和 PML 焦点则具有高度抗性。液-液相分离的破坏改变了 LANA 依赖性 KSHV 染色体构象,但并没有刺激裂解性再激活。我们发现,在 KSHV 裂解性再激活期间,LANA-NBs 发生主要的形态转变,形成包含 KSHV DNA 的 LANA 相关复制区室。在潜伏期间,DAXX 与 LANA-NBs 共定位,但从 LANA 相关的裂解复制区室中逐出。这些发现表明 LANA-NBs 是动态的超分子核结构,部分依赖于液-液相分离,并发生形态转变,对应于不同的病毒复制模式。