Department of Pharmacology, Physiology and Neuroscience, University of South Carolina School of Medicine, Columbia, SC, USA.
Department of Computer Science and Engineering, University of South Carolina, Columbia, SC, USA.
Transl Psychiatry. 2023 Mar 31;13(1):106. doi: 10.1038/s41398-023-02399-1.
Dysregulated sleep is commonly reported in individuals with neuropsychiatric disorders, including schizophrenia (SCZ) and bipolar disorder (BPD). Physiology and pathogenesis of these disorders points to aberrant metabolism, during neurodevelopment and adulthood, of tryptophan via the kynurenine pathway (KP). Kynurenic acid (KYNA), a neuroactive KP metabolite derived from its precursor kynurenine by kynurenine aminotransferase II (KAT II), is increased in the brains of individuals with SCZ and BPD. We hypothesize that elevated KYNA, an inhibitor of glutamatergic and cholinergic neurotransmission, contributes to sleep dysfunction. Employing the embryonic kynurenine (EKyn) paradigm to elevate fetal brain KYNA, we presently examined pharmacological inhibition of KAT II to reduce KYNA in adulthood to improve sleep quality. Pregnant Wistar rats were fed either kynurenine (100 mg/day)(EKyn) or control (ECon) diet from embryonic day (ED) 15 to ED 22. Adult male (N = 24) and female (N = 23) offspring were implanted with devices to record electroencephalogram (EEG) and electromyogram (EMG) telemetrically for sleep-wake data acquisition. Each subject was treated with either vehicle or PF-04859989 (30 mg/kg, s.c.), an irreversible KAT II inhibitor, at zeitgeber time (ZT) 0 or ZT 12. KAT II inhibitor improved sleep architecture maintaining entrainment of the light-dark cycle; ZT 0 treatment with PF-04859989 induced transient improvements in rapid eye movement (REM) and non-REM (NREM) sleep during the immediate light phase, while the impact of ZT 12 treatment was delayed until the subsequent light phase. PF-04859989 administration at ZT 0 enhanced NREM delta spectral power and reduced activity and body temperature. In conclusion, reducing de novo KYNA production alleviated sleep disturbances and increased sleep quality in EKyn, while also improving sleep outcomes in ECon offspring. Our findings place attention on KAT II inhibition as a novel mechanistic approach to treating disrupted sleep behavior with potential translational implications for patients with neurodevelopmental and neuropsychiatric disorders.
睡眠失调在患有神经精神疾病的个体中很常见,包括精神分裂症 (SCZ) 和双相情感障碍 (BPD)。这些疾病的生理学和发病机制表明,在神经发育和成年期,色氨酸通过犬尿氨酸途径 (KP) 代谢异常。犬尿酸 (KYNA) 是一种神经活性 KP 代谢物,由犬尿氨酸氨基转移酶 II (KAT II) 从其前体犬尿氨酸衍生而来,在 SCZ 和 BPD 患者的大脑中增加。我们假设,升高的 KYNA 作为谷氨酸能和胆碱能神经递质传递的抑制剂,导致睡眠功能障碍。我们利用胚胎犬尿氨酸 (EKyn) 范式升高胎儿大脑 KYNA,目前研究了 KAT II 的药理学抑制作用,以降低成年后的 KYNA 来改善睡眠质量。怀孕的 Wistar 大鼠从胚胎期 15 天 (ED) 到 ED 22 天,每天喂食犬尿氨酸 (100mg/天) (EKyn) 或对照 (ECon) 饮食。成年雄性 (N=24) 和雌性 (N=23) 后代被植入设备,以记录脑电图 (EEG) 和肌电图 (EMG),进行睡眠-觉醒数据采集。每个实验对象都在 zeitgeber 时间 (ZT) 0 或 ZT 12 时接受载体或 PF-04859989(30mg/kg,sc)治疗,PF-04859989 是一种不可逆的 KAT II 抑制剂。KAT II 抑制剂改善了睡眠结构,维持了光-暗周期的同步;ZT 0 时用 PF-04859989 治疗可在光相的即刻诱导 REM 和非 REM (NREM) 睡眠的短暂改善,而 ZT 12 时治疗的影响则延迟到随后的光相。ZT 0 时给予 PF-04859989 可增强 NREM 德尔塔频谱功率,并减少活动和体温。总之,减少新生成的 KYNA 可缓解 EKyn 中的睡眠障碍并提高睡眠质量,同时改善 ECon 后代的睡眠结果。我们的研究结果表明,KAT II 抑制作为一种治疗神经发育和神经精神疾病患者睡眠障碍的新机制方法,具有潜在的转化意义。