Fernández-García Yaiza, Reguera Juan, Busch Carola, Witte Gregor, Sánchez-Ramos Oliberto, Betzel Christian, Cusack Stephen, Günther Stephan, Reindl Sophia
Department of Virology, Bernhard-Nocht-Institute for Tropical Medicine, Hamburg, Germany.
Department of Pharmacology, University of Concepción, Concepción, Chile.
PLoS Pathog. 2016 Jun 14;12(6):e1005635. doi: 10.1371/journal.ppat.1005635. eCollection 2016 Jun.
Andes virus (ANDV) is a human-pathogenic hantavirus. Hantaviruses presumably initiate their mRNA synthesis by using cap structures derived from host cell mRNAs, a mechanism called cap-snatching. A signature for a cap-snatching endonuclease is present in the N terminus of hantavirus L proteins. In this study, we aimed to solve the atomic structure of the ANDV endonuclease and characterize its biochemical features. However, the wild-type protein was refractory to expression in Escherichia coli, presumably due to toxic enzyme activity. To circumvent this problem, we introduced attenuating mutations in the domain that were previously shown to enhance L protein expression in mammalian cells. Using this approach, 13 mutant proteins encompassing ANDV L protein residues 1-200 were successfully expressed and purified. Protein stability and nuclease activity of the mutants was analyzed and the crystal structure of one mutant was solved to a resolution of 2.4 Å. Shape in solution was determined by small angle X-ray scattering. The ANDV endonuclease showed structural similarities to related enzymes of orthobunya-, arena-, and orthomyxoviruses, but also differences such as elongated shape and positively charged patches surrounding the active site. The enzyme was dependent on manganese, which is bound to the active site, most efficiently cleaved single-stranded RNA substrates, did not cleave DNA, and could be inhibited by known endonuclease inhibitors. The atomic structure in conjunction with stability and activity data for the 13 mutant enzymes facilitated inference of structure-function relationships in the protein. In conclusion, we solved the structure of a hantavirus cap-snatching endonuclease, elucidated its catalytic properties, and present a highly active mutant form, which allows for inhibitor screening.
安第斯病毒(ANDV)是一种可感染人类的汉坦病毒。汉坦病毒可能通过利用源自宿主细胞mRNA的帽结构来启动其mRNA合成,这种机制称为帽抢夺。汉坦病毒L蛋白的N端存在帽抢夺内切核酸酶的特征性结构。在本研究中,我们旨在解析ANDV内切核酸酶的原子结构并表征其生化特性。然而,野生型蛋白在大肠杆菌中难以表达,可能是由于其具有毒性酶活性。为了解决这个问题,我们在先前已证明可增强L蛋白在哺乳动物细胞中表达的结构域中引入了减毒突变。使用这种方法,成功表达并纯化了包含ANDV L蛋白第1至200位残基的13种突变蛋白。分析了这些突变体的蛋白质稳定性和核酸酶活性,并解析了其中一种突变体的晶体结构,分辨率达到2.4 Å。通过小角X射线散射确定了其在溶液中的形状。ANDV内切核酸酶与正布尼亚病毒、沙粒病毒和正黏液病毒的相关酶在结构上有相似之处,但也存在差异,如形状细长且活性位点周围有带正电荷的区域。该酶依赖于与活性位点结合的锰,最有效地切割单链RNA底物,不切割DNA,并且可被已知的内切核酸酶抑制剂抑制。结合13种突变酶的原子结构以及稳定性和活性数据,有助于推断该蛋白的结构-功能关系。总之,我们解析了汉坦病毒帽抢夺内切核酸酶的结构,阐明了其催化特性,并展示了一种高活性的突变形式,可用于抑制剂筛选。