Popa Crina, Coll Núria S, Valls Marc, Sessa Guido
Genetics Department, Universitat de Barcelona, Barcelona, Catalonia, Spain.
Centre for Research in Agricultural Genomics (CSIC-IRTA-UAB-UB), Bellaterra, Catalonia, Spain.
PLoS Pathog. 2016 Feb 25;12(2):e1005360. doi: 10.1371/journal.ppat.1005360. eCollection 2016 Feb.
Type III effectors (T3E) are key virulence proteins that are injected by bacterial pathogens inside the cells of their host to subvert cellular processes and contribute to disease. The budding yeast Saccharomyces cerevisiae represents an important heterologous system for the functional characterisation of T3E proteins in a eukaryotic environment. Importantly, yeast contains eukaryotic processes with low redundancy and are devoid of immunity mechanisms that counteract T3Es and mask their function. Expression in yeast of effectors from both plant and animal pathogens that perturb conserved cellular processes often resulted in robust phenotypes that were exploited to elucidate effector functions, biochemical properties, and host targets. The genetic tractability of yeast and its amenability for high-throughput functional studies contributed to the success of this system that, in recent years, has been used to study over 100 effectors. Here, we provide a critical view on this body of work and describe advantages and limitations inherent to the use of yeast in T3E research. "Favourite" targets of T3Es in yeast are cytoskeleton components and small GTPases of the Rho family. We describe how mitogen-activated protein kinase (MAPK) signalling, vesicle trafficking, membrane structures, and programmed cell death are also often altered by T3Es in yeast and how this reflects their function in the natural host. We describe how effector structure-function studies and analysis of candidate targeted processes or pathways can be carried out in yeast. We critically analyse technologies that have been used in yeast to assign biochemical functions to T3Es, including transcriptomics and proteomics, as well as suppressor, gain-of-function, or synthetic lethality screens. We also describe how yeast can be used to select for molecules that block T3E function in search of new antibacterial drugs with medical applications. Finally, we provide our opinion on the limitations of S. cerevisiae as a model system and its most promising future applications.
III型效应蛋白(T3E)是关键的毒力蛋白,由细菌病原体注入宿主细胞内,以破坏细胞过程并导致疾病。出芽酵母酿酒酵母是在真核环境中对T3E蛋白进行功能表征的重要异源系统。重要的是,酵母含有冗余度低的真核过程,并且没有对抗T3E并掩盖其功能的免疫机制。来自植物和动物病原体的效应蛋白在酵母中的表达会扰乱保守的细胞过程,通常会导致明显的表型,这些表型被用于阐明效应蛋白的功能、生化特性和宿主靶点。酵母的遗传易处理性及其适用于高通量功能研究的特性促成了该系统的成功,近年来,该系统已用于研究100多种效应蛋白。在这里,我们对这一系列工作提供批判性观点,并描述在T3E研究中使用酵母所固有的优点和局限性。酵母中T3E的“偏好”靶点是细胞骨架成分和Rho家族的小GTP酶。我们描述了丝裂原活化蛋白激酶(MAPK)信号传导、囊泡运输、膜结构和程序性细胞死亡在酵母中如何也经常被T3E改变,以及这如何反映它们在天然宿主中的功能。我们描述了如何在酵母中进行效应蛋白结构-功能研究以及对候选靶向过程或途径的分析。我们批判性地分析了已在酵母中用于赋予T3E生化功能的技术,包括转录组学和蛋白质组学,以及抑制子、功能获得或合成致死筛选。我们还描述了如何利用酵母筛选能够阻断T3E功能的分子,以寻找具有医学应用的新型抗菌药物。最后,我们对酿酒酵母作为模型系统的局限性及其最有前景的未来应用发表了看法。