Birk Marlène S, Walch Philipp, Baykara Tarik, Sefried Stephanie, Amelang Jan, Buerova Elena, Breuer Ingrid, Vervoorts Jörg, Typas Athanasios, Savitski Mikhail M, Mateus André, Selkrig Joel
Institute of Medical Microbiology, RWTH University Hospital, Aachen 52074, Germany.
European Molecular Biology Laboratory (EMBL), Genome Biology Unit, Meyerhofstrasse 1, Heidelberg 69117, Germany.
Eur J Cell Biol. 2024 Dec;103(4):151448. doi: 10.1016/j.ejcb.2024.151448. Epub 2024 Aug 6.
Intracellular bacterial pathogens hijack the protein machinery of infected host cells to evade their defenses and cultivate a favorable intracellular niche. The intracellular pathogen Salmonella enterica subsp. Typhimurium (STm) achieves this by injecting a cocktail of effector proteins into host cells that modify the activity of target host proteins. Yet, proteome-wide approaches to systematically map changes in host protein function during infection have remained challenging. Here we adapted a functional proteomics approach - Thermal-Proteome Profiling (TPP) - to systematically assess proteome-wide changes in host protein abundance and thermal stability throughout an STm infection cycle. By comparing macrophages treated with live or heat-killed STm, we observed that most host protein abundance changes occur independently of STm viability. In contrast, a large portion of host protein thermal stability changes were specific to infection with live STm. This included pronounced thermal stability changes in proteins linked to mitochondrial function (Acod1/Irg1, Cox6c, Samm50, Vdac1, and mitochondrial respiratory chain complex proteins), as well as the interferon-inducible protein with tetratricopeptide repeats, Ifit1. Integration of our TPP data with a publicly available STm-host protein-protein interaction database led us to discover that the secreted STm effector kinase, SteC, thermally destabilizes and phosphorylates the ribosomal preservation factor Serbp1. In summary, this work emphasizes the utility of measuring protein thermal stability during infection to accelerate the discovery of novel molecular interactions at the host-pathogen interface.
细胞内细菌病原体劫持被感染宿主细胞的蛋白质机制,以逃避其防御并营造有利的细胞内微环境。细胞内病原体鼠伤寒沙门氏菌(STm)通过向宿主细胞注射一组效应蛋白来实现这一点,这些效应蛋白会改变目标宿主蛋白的活性。然而,在感染过程中系统地绘制宿主蛋白功能变化的全蛋白质组方法仍然具有挑战性。在这里,我们采用了一种功能蛋白质组学方法——热蛋白质组分析(TPP)——来系统地评估在整个STm感染周期中宿主蛋白丰度和热稳定性的全蛋白质组变化。通过比较用活的或热灭活的STm处理的巨噬细胞,我们观察到大多数宿主蛋白丰度变化的发生与STm的活力无关。相比之下,很大一部分宿主蛋白热稳定性变化是活的STm感染所特有的。这包括与线粒体功能相关的蛋白质(Acod1/Irg1、Cox6c、Samm50、Vdac1和线粒体呼吸链复合体蛋白)以及具有四肽重复序列的干扰素诱导蛋白Ifit1的显著热稳定性变化。将我们的TPP数据与公开可用的STm-宿主蛋白质-蛋白质相互作用数据库整合,使我们发现分泌的STm效应激酶SteC会使核糖体保护因子Serbp1的热稳定性降低并使其磷酸化。总之,这项工作强调了在感染过程中测量蛋白质热稳定性对于加速发现宿主-病原体界面新分子相互作用的实用性。