Herrera José A, Ward Christopher S, Wehrens Xander H T, Neul Jeffrey L
Jan and Duncan Neurological Research Institute, Texas Children's Hospital, Houston, TX, USA.
Interdepartmental Program in Translational Biology and Molecular Medicine, Baylor College of Medicine, Houston, TX, USA.
Hum Mol Genet. 2016 Nov 15;25(22):4983-4995. doi: 10.1093/hmg/ddw326.
Sudden unexpected death occurs in one quarter of deaths in Rett Syndrome (RTT), a neurodevelopmental disorder caused by mutations in Methyl-CpG-binding protein 2 (MECP2). People with RTT show a variety of autonomic nervous system (ANS) abnormalities and mouse models show similar problems including QTc interval prolongation and hypothermia. To explore the role of cardiac problems in sudden death in RTT, we characterized cardiac rhythm in mice lacking Mecp2 function. Male and female mutant mice exhibited spontaneous cardiac rhythm abnormalities including bradycardic events, sinus pauses, atrioventricular block, premature ventricular contractions, non-sustained ventricular arrhythmias, and increased heart rate variability. Death was associated with spontaneous cardiac arrhythmias and complete conduction block. Atropine treatment reduced cardiac arrhythmias in mutant mice, implicating overactive parasympathetic tone. To explore the role of MeCP2 within the parasympathetic neurons, we selectively removed MeCP2 function from cholinergic neurons (MeCP2 ChAT KO), which recapitulated the cardiac rhythm abnormalities, hypothermia, and early death seen in RTT male mice. Conversely, restoring MeCP2 only in cholinergic neurons rescued these phenotypes. Thus, MeCP2 in cholinergic neurons is necessary and sufficient for autonomic cardiac control, thermoregulation, and survival, and targeting the overactive parasympathetic system may be a useful therapeutic strategy to prevent sudden unexpected death in RTT.
在雷特综合征(RTT)中,四分之一的死亡为意外猝死。RTT是一种神经发育障碍,由甲基CpG结合蛋白2(MECP2)突变引起。RTT患者表现出多种自主神经系统(ANS)异常,小鼠模型也显示出类似问题,包括QTc间期延长和体温过低。为了探究心脏问题在RTT猝死中的作用,我们对缺乏Mecp2功能的小鼠的心律进行了表征。雄性和雌性突变小鼠均表现出自发性心律异常,包括心动过缓事件、窦性停搏、房室传导阻滞、室性早搏、非持续性室性心律失常以及心率变异性增加。死亡与自发性心律失常和完全性传导阻滞有关。阿托品治疗可减少突变小鼠的心律失常,提示副交感神经张力亢进。为了探究MeCP2在副交感神经元中的作用,我们选择性地从胆碱能神经元中去除MeCP2功能(MeCP2 ChAT KO),这重现了RTT雄性小鼠中出现的心律异常、体温过低和早期死亡现象。相反,仅在胆碱能神经元中恢复MeCP2可挽救这些表型。因此,胆碱能神经元中的MeCP2对于自主心脏控制、体温调节和生存是必要且充分的,针对过度活跃副交感神经系统可能是预防RTT意外猝死的一种有用治疗策略。