Montespan Charlotte, Marvin Shauna A, Austin Sisley, Burrage Andrew M, Roger Benoit, Rayne Fabienne, Faure Muriel, Campell Edward M, Schneider Carola, Reimer Rudolph, Grünewald Kay, Wiethoff Christopher M, Wodrich Harald
MFP CNRS UMR 5234, Microbiologie Fondamentale et Pathogénicité, Université de Bordeaux, Bordeaux, France.
Department of Microbiology and Immunology, Loyola University Chicago Stritch School of Medicine, Maywood, Illinois, United States of America.
PLoS Pathog. 2017 Feb 13;13(2):e1006217. doi: 10.1371/journal.ppat.1006217. eCollection 2017 Feb.
Cells employ active measures to restrict infection by pathogens, even prior to responses from the innate and humoral immune defenses. In this context selective autophagy is activated upon pathogen induced membrane rupture to sequester and deliver membrane fragments and their pathogen contents for lysosomal degradation. Adenoviruses, which breach the endosome upon entry, escape this fate by penetrating into the cytosol prior to autophagosome sequestration of the ruptured endosome. We show that virus induced membrane damage is recognized through Galectin-8 and sequesters the autophagy receptors NDP52 and p62. We further show that a conserved PPxY motif in the viral membrane lytic protein VI is critical for efficient viral evasion of autophagic sequestration after endosomal lysis. Comparing the wildtype with a PPxY-mutant virus we show that depletion of Galectin-8 or suppression of autophagy in ATG5-/- MEFs rescues infectivity of the PPxY-mutant virus while depletion of the autophagy receptors NDP52, p62 has only minor effects. Furthermore we show that wildtype viruses exploit the autophagic machinery for efficient nuclear genome delivery and control autophagosome formation via the cellular ubiquitin ligase Nedd4.2 resulting in reduced antigenic presentation. Our data thus demonstrate that a short PPxY-peptide motif in the adenoviral capsid permits multi-layered viral control of autophagic processes during entry.
细胞会采取主动措施来限制病原体的感染,甚至在先天免疫和体液免疫防御做出反应之前就会这样做。在这种情况下,病原体诱导的膜破裂会激活选择性自噬,以隔离并将膜碎片及其病原体内容物输送到溶酶体进行降解。腺病毒进入时会突破内体,通过在内体破裂被自噬体隔离之前渗透到细胞质中而逃避这种命运。我们发现,病毒诱导的膜损伤通过半乳糖凝集素-8被识别,并隔离自噬受体NDP52和p62。我们进一步表明,病毒膜裂解蛋白VI中一个保守的PPxY基序对于内体裂解后病毒有效逃避自噬隔离至关重要。通过将野生型病毒与PPxY突变病毒进行比较,我们发现,在ATG5-/- 小鼠胚胎成纤维细胞中,半乳糖凝集素-8的缺失或自噬的抑制可挽救PPxY突变病毒的感染性,而自噬受体NDP52、p62的缺失只有轻微影响。此外,我们还表明,野生型病毒利用自噬机制实现有效的核基因组传递,并通过细胞泛素连接酶Nedd4.2控制自噬体形成,从而减少抗原呈递。因此,我们的数据表明,腺病毒衣壳中的一个短PPxY肽基序允许病毒在进入过程中对自噬过程进行多层次控制。