Seeger Drew R, Schofield Brennon, Besch Derek, Golovko Svetlana A, Kotha Peddanna, Golovko Mikhail Y
Department of Biomedical Sciences, School of Medicine and Health Sciences, University of North Dakota, Grand Forks, North Dakota, USA.
J Neurochem. 2025 Jun;169(6):e70121. doi: 10.1111/jnc.70121.
It is well documented that adenosine and adenine nucleotides, such as ATP, ADP, and AMP, undergo significant alterations within seconds upon brain ischemia. For their accurate quantification, in situ deactivation of enzymes involved in their metabolism is required to prevent postmortem alterations. Thus, techniques such as high energy head-focused microwave irradiation (MW) or freeze-blowing are often used prior to metabolome analysis. However, alterations of another important purine nucleotide, adenylosuccinate (AdSucc), under brain ischemia have not been previously addressed. AdSucc is an intermediate in purine nucleotide de novo synthesis. Over 50 years ago, it was also proposed to have a role in brain energy metabolism through the purine nucleotide cycle (PNC) similar to that in muscle, with, to the best of our knowledge, no follow-up studies. In the present study, we applied MW and LC-MS analysis for mouse brain AdSucc quantification in situ at baseline and upon 30 s, 2 min, and 10 min of global ischemia. Our data indicate that in situ enzyme deactivation is required for brain AdSucc quantification. We report, for the first time, that brain AdSucc is dramatically increased 19-fold at 30 s ischemia and 77-fold at 2 min, from 0.007 ± 0.001 to 0.136 ± 0.026 and 0.555 ± 0.036 nmol/mg of brain wet weight (ww), respectively, without further increase at 10 min, positioning it as one of the major brain metabolites under ischemia (~0.56 mM). Quantification of PNC and tricarboxylic acid cycle (TCA) metabolites did not support the role of AdSucc induction in the activation of these pathways under ischemia. Importantly, a significant AdSucc increase up to ~0.56 mM did not affect its precursor aspartate (Asp), which remained at ~1 mM (0.923 ± 0.036 nmol/mg ww) during ischemia, indicating that AdSucc is not produced by the condensation reaction between Asp and IMP in the PNC catalyzed by adenylosuccinate synthase (ADSS). Further studies are required to elucidate the mechanisms for AdSucc increase and its role under brain ischemia.
有充分的文献记载,腺苷和腺嘌呤核苷酸,如ATP、ADP和AMP,在脑缺血后数秒内会发生显著变化。为了对它们进行准确的定量分析,需要对参与其代谢的酶进行原位失活,以防止死后发生变化。因此,在代谢组分析之前,经常使用高能头部聚焦微波辐射(MW)或冷冻吹气等技术。然而,此前尚未研究过另一种重要的嘌呤核苷酸——腺苷酸琥珀酸(AdSucc)在脑缺血时的变化。AdSucc是嘌呤核苷酸从头合成的中间体。50多年前,也曾有人提出它通过类似于肌肉中的嘌呤核苷酸循环(PNC)在脑能量代谢中发挥作用,但据我们所知,没有后续研究。在本研究中,我们应用MW和LC-MS分析对小鼠脑在基线以及全脑缺血30秒、2分钟和10分钟时的AdSucc进行原位定量。我们的数据表明,对脑AdSucc进行定量分析需要原位酶失活。我们首次报告,在缺血30秒时脑AdSucc显著增加19倍,在2分钟时增加77倍,分别从0.007±0.001增加到0.136±0.026和0.555±0.036nmol/mg脑湿重(ww),在10分钟时没有进一步增加,使其成为缺血状态下主要的脑代谢物之一(约0.56mM)。对PNC和三羧酸循环(TCA)代谢物的定量分析不支持AdSucc诱导在缺血状态下激活这些途径中的作用。重要的是,AdSucc显著增加至约0.56mM并不影响其前体天冬氨酸(Asp),在缺血期间Asp保持在约1mM(0.923±0.036nmol/mg ww),这表明AdSucc不是由腺苷酸琥珀酸合酶(ADSS)催化的PNC中天冬氨酸和肌苷酸(IMP)之间的缩合反应产生的。需要进一步研究以阐明脑缺血时AdSucc增加的机制及其作用。