Francois Asvi Arora, Yin Xiaoke, Oka Shinichi, Sadoshima Junichi, Mayr Manuel, Eaton Philip
William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, EC1M 6BQ, UK.
National Heart and Lung Institute, Imperial College London, London, SW7 2AZ, UK.
Sci Rep. 2025 May 3;15(1):15554. doi: 10.1038/s41598-025-00665-4.
Reactive protein cysteine thiols are critical to sensing and transducing oxidant signals, often by induction of disulfide bonds that alter their activity or interactions. Identifying such redox active proteins nowadays is mostly achieved using thiol redox proteomics with such datasets increasingly available. Subsequently, we are challenged with determining how changes in the redox state of a protein of interest alters its activity or interactions and how this affects physiology or disease progression including in vivo scenarios. Such studies necessitate the measurement of how the protein redox state changes with health or disease-related interventions, with it not always being practicable to resort back to resource-intensive proteomics to achieve this. In some proteins, oxidation to a disulfide state causes a non-reducing gel-shift, but this is mostly not the case and so other efficient approaches are required to index changes in redox state. Here we assessed the utility of immobilized, solid-phase phenylarsine oxide (PAO-Sepharose) as a tool for indexing the thiol redox state of candidate proteins in cardiac samples from in vivo interventions associated with oxidative stress. PAO-Sepharose, which binds proteins with proximal reduced thiol pairs but not when they form a disulfide, was also used to identify proteins that that are oxidised in isolated perfused mouse hearts exposed to hydrogen peroxide or diamide using proteomics. This together with complementary studies using a cardiac-specific FLAG-Thioredoxin-1C35S-HA transgenic 'trap-mutant' mouse model allowed identification of heart proteins susceptible to oxidant-induced disulfide bond formation using proteomics. Thus, two in vitro approaches identified putative cardiac thiol redox sensor proteins that were then assessed with in vivo follow-up studies for their susceptibility to oxidation during endotoxemia induced by lipopolysaccharide or type I diabetes induced by streptozotocin in mice. Of five proteins selected for further analysis by PAO-Sepharose binding, two, namely apoptotic protease activating factor 1 interacting protein (APIP) and γ-glutamylcyclotransferase (GGCT), displayed significantly lower affinity capture from hearts from lipopolysaccharide- or streptozotocin-treated mice, consistent with oxidation of their vicinal thiols. We conclude that PAO-Sepharose is an effective and accessible tool for identifying oxidant-sensitive protein thiols in both ex vivo and in vivo models of oxidative stress. As increasing numbers of thiol redox proteins are identified, PAO-Sepharose binding is an efficient method to determine if they change their oxidation state during interventions relevant to health and disease.
反应性蛋白半胱氨酸硫醇对于感知和转导氧化信号至关重要,通常是通过诱导二硫键来改变其活性或相互作用。如今,识别此类氧化还原活性蛋白大多是通过硫醇氧化还原蛋白质组学来实现的,并且此类数据集越来越多。随后,我们面临着确定目标蛋白氧化还原状态的变化如何改变其活性或相互作用,以及这如何影响生理过程或疾病进展(包括体内情况)的挑战。此类研究需要测量蛋白质氧化还原状态如何随着与健康或疾病相关的干预而变化,而依靠资源密集型的蛋白质组学来实现这一点并不总是可行的。在一些蛋白质中,氧化成二硫键状态会导致非还原性凝胶迁移,但大多情况并非如此,因此需要其他有效的方法来标记氧化还原状态的变化。在这里,我们评估了固定化的固相苯砷氧化物(PAO-琼脂糖)作为一种工具的实用性,用于标记来自与氧化应激相关的体内干预的心脏样本中候选蛋白的硫醇氧化还原状态。PAO-琼脂糖能结合具有近端还原硫醇对的蛋白质,但当它们形成二硫键时则不能结合,它还被用于通过蛋白质组学鉴定在暴露于过氧化氢或二酰胺的离体灌注小鼠心脏中被氧化的蛋白质。这与使用心脏特异性FLAG-硫氧还蛋白-1C35S-HA转基因“陷阱突变体 ”小鼠模型的补充研究一起,使得能够通过蛋白质组学鉴定易受氧化剂诱导形成二硫键的心脏蛋白。因此,两种体外方法鉴定出了假定的心脏硫醇氧化还原传感器蛋白,然后通过体内后续研究评估它们在小鼠中由脂多糖诱导的内毒素血症或由链脲佐菌素诱导的I型糖尿病期间对氧化的敏感性。通过PAO-琼脂糖结合选择进行进一步分析的五种蛋白质中,有两种,即凋亡蛋白酶激活因子1相互作用蛋白(APIP)和γ-谷氨酰环转移酶(GGCT),在来自脂多糖或链脲佐菌素处理小鼠的心脏中显示出明显较低的亲和力捕获,这与它们邻近硫醇的氧化一致。我们得出结论,PAO-琼脂糖是一种在氧化应激的离体和体内模型中识别对氧化剂敏感的蛋白质硫醇的有效且可及的工具。随着越来越多的硫醇氧化还原蛋白被鉴定出来,PAO-琼脂糖结合是一种有效的方法,用于确定它们在与健康和疾病相关的干预过程中是否改变其氧化状态。