Department of Chemistry and Purdue University Center for Cancer Research, Purdue University, 560 Oval Drive West, Lafayette, IN, 47907, USA.
Mol Neurobiol. 2019 Feb;56(2):1366-1390. doi: 10.1007/s12035-018-1114-9. Epub 2018 Jun 8.
This study revealed multifaceted regulation of ALDH1A1 by Cdk5 in Alzheimer's disease (AD) pathogenesis. ALDH1A1 is a multifunctional enzyme with dehydrogenase, esterase, and anti-oxidant activities. ALDH1A1 is also a major regulator of retinoic acid (RA) signaling, which is critical for normal brain homeostasis. We identified ALDH1A1 as both physiological and pathological target of Cdk5. First, under neurotoxic conditions, Cdk5-induced oxidative stress upregulates ALDH1A1 transcription. Second, Cdk5 increases ALDH1A1 levels by preventing its ubiquitylation via direct phosphorylation. Third, ALDH1A1 phosphorylation increases its dehydrogenase activity by altering its tetrameric state to a highly active monomeric state. Fourth, persistent oxidative stress triggered by deregulated Cdk5 inactivates ALDH1A1. Thus, initially, the good Cdk5 attempts to mitigate ensuing oxidative stress by upregulating ALDH1A1 via phosphorylation and paradoxically by increasing oxidative stress. Later, sustained oxidative stress generated by Cdk5 inhibits ALDH1A1 activity, leading to neurotoxicity. ALDH1A1 upregulation is highly neuroprotective. In human AD tissues, ALDH1A1 levels increase with disease severity. However, ALDH1A1 activity was highest at mild and moderate stages, but declines significantly at severe stage. These findings confirm that during the initial stages, neurons attempt to upregulate and activate ALDH1A1 to protect from accruing oxidative stress-induced damage; however, persistently deleterious conditions inactivate ALDH1A1, further contributing to neurotoxicity. This study thus revealed two faces of Cdk5, good and bad in neuronal function and survival, with a single substrate, ALDH1A1. The bad Cdk5 prevails in the end, overriding the good Cdk5 act, suggesting that Cdk5 is an effective therapeutic target for AD.
这项研究揭示了 Cdk5 在阿尔茨海默病(AD)发病机制中对 ALDH1A1 的多方面调控。ALDH1A1 是一种具有脱氢酶、酯酶和抗氧化活性的多功能酶。ALDH1A1 也是视黄酸(RA)信号的主要调节剂,这对于大脑的正常内稳态至关重要。我们确定了 ALDH1A1 是 Cdk5 的生理和病理靶标。首先,在神经毒性条件下,Cdk5 诱导的氧化应激上调 ALDH1A1 转录。其次,Cdk5 通过直接磷酸化防止其泛素化来增加 ALDH1A1 水平。第三,ALDH1A1 的磷酸化通过改变其四聚体状态为高度活跃的单体状态来增加其脱氢酶活性。第四,Cdk5 失调引发的持续氧化应激使 ALDH1A1 失活。因此,最初,良好的 Cdk5 通过磷酸化和矛盾地通过增加氧化应激来上调 ALDH1A1 来尝试减轻随后的氧化应激。后来,Cdk5 产生的持续氧化应激抑制了 ALDH1A1 的活性,导致神经毒性。ALDH1A1 的上调具有高度神经保护作用。在人类 AD 组织中,ALDH1A1 水平随着疾病的严重程度而增加。然而,ALDH1A1 的活性在轻度和中度阶段最高,但在重度阶段显著下降。这些发现证实,在初始阶段,神经元试图上调和激活 ALDH1A1 以保护免受累积的氧化应激诱导的损伤;然而,持续的有害条件使 ALDH1A1 失活,进一步导致神经毒性。因此,这项研究揭示了 Cdk5 在神经元功能和存活方面的两种面孔,好的和坏的,有一个单一的底物,ALDH1A1。最终,坏的 Cdk5 占了上风,压倒了好的 Cdk5 作用,表明 Cdk5 是 AD 的一个有效的治疗靶点。