Kumar Ashwani, Toledo Jose C, Patel Rakesh P, Lancaster Jack R, Steyn Adrie J C
Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11568-73. doi: 10.1073/pnas.0705054104. Epub 2007 Jul 3.
A fundamental challenge to the study of oxidative stress responses of Mycobacterium tuberculosis (Mtb) is to understand how the protective host molecules are sensed and relayed to control bacilli gene expression. The genetic response of Mtb to hypoxia and NO is controlled by the sensor kinases DosS and DosT and the response regulator DosR through activation of the dormancy/NO (Dos) regulon. However, the regulatory ligands of DosS and DosT and the mechanism of signal sensing were unknown. Here, we show that both DosS and DosT bind heme as a prosthetic group and that DosS is rapidly autooxidized to attain the met (Fe3+) form, whereas DosT exists in the O2-bound (oxy) form. EPR and UV-visible spectroscopy analysis showed that O2, NO, and CO are ligands of DosS and DosT. Importantly, we demonstrate that the oxidation or ligation state of the heme iron modulates DosS and DosT autokinase activity and that ferrous DosS, and deoxy DosT, show significantly increased autokinase activity compared with met DosS and oxy DosT. Our data provide direct proof that DosS functions as a redox sensor, whereas DosT functions as a hypoxia sensor, and that O2, NO, and CO are modulatory ligands of DosS and DosT. Finally, we identified a third potential dormancy signal, CO, that induces the Mtb Dos regulon. We conclude that Mtb has evolved finely tuned redox and hypoxia-mediated sensing strategies for detecting O2, NO, and CO. Data presented here establish a paradigm for understanding the mechanism of bacilli persistence.
对结核分枝杆菌(Mtb)氧化应激反应进行研究面临的一个基本挑战是了解保护性宿主分子是如何被感知并传递以控制杆菌基因表达的。Mtb对缺氧和一氧化氮(NO)的遗传反应由传感激酶DosS和DosT以及反应调节因子DosR通过激活休眠/NO(Dos)调控子来控制。然而,DosS和DosT的调节配体以及信号传感机制尚不清楚。在此,我们表明DosS和DosT都结合血红素作为辅基,并且DosS会迅速自动氧化以达到高铁(Fe3+)形式,而DosT以与氧气结合的(氧合)形式存在。电子顺磁共振(EPR)和紫外可见光谱分析表明,氧气、NO和一氧化碳(CO)是DosS和DosT的配体。重要的是,我们证明血红素铁的氧化或连接状态调节DosS和DosT的自激酶活性,并且亚铁形式的DosS和脱氧形式的DosT与高铁形式的DosS和氧合形式的DosT相比,自激酶活性显著增加。我们的数据提供了直接证据,证明DosS作为氧化还原传感器发挥作用,而DosT作为缺氧传感器发挥作用,并且氧气、NO和CO是DosS和DosT的调节配体。最后,我们鉴定出了第三种潜在的休眠信号CO,它可诱导Mtb的Dos调控子。我们得出结论,Mtb已经进化出精细调节的氧化还原和缺氧介导的传感策略来检测氧气、NO和CO。此处呈现的数据为理解杆菌持续性机制建立了一个范例。