Genomic Medicine Institute, Cleveland Clinic Lerner Research Institute, Cleveland, OH 44195, USA.
DDC Clinic for Special Needs Children, Middlefield, OH 44062, USA.
Hum Mol Genet. 2023 Oct 4;32(20):2981-2995. doi: 10.1093/hmg/ddad124.
Protein phosphatase 1 regulatory subunit 3F (PPP1R3F) is a member of the glycogen targeting subunits (GTSs), which belong to the large group of regulatory subunits of protein phosphatase 1 (PP1), a major eukaryotic serine/threonine protein phosphatase that regulates diverse cellular processes. Here, we describe the identification of hemizygous variants in PPP1R3F associated with a novel X-linked recessive neurodevelopmental disorder in 13 unrelated individuals. This disorder is characterized by developmental delay, mild intellectual disability, neurobehavioral issues such as autism spectrum disorder, seizures and other neurological findings including tone, gait and cerebellar abnormalities. PPP1R3F variants segregated with disease in affected hemizygous males that inherited the variants from their heterozygous carrier mothers. We show that PPP1R3F is predominantly expressed in brain astrocytes and localizes to the endoplasmic reticulum in cells. Glycogen content in PPP1R3F knockout astrocytoma cells appears to be more sensitive to fluxes in extracellular glucose levels than in wild-type cells, suggesting that PPP1R3F functions in maintaining steady brain glycogen levels under changing glucose conditions. We performed functional studies on nine of the identified variants and observed defects in PP1 binding, protein stability, subcellular localization and regulation of glycogen metabolism in most of them. Collectively, the genetic and molecular data indicate that deleterious variants in PPP1R3F are associated with a new X-linked disorder of glycogen metabolism, highlighting the critical role of GTSs in neurological development. This research expands our understanding of neurodevelopmental disorders and the role of PP1 in brain development and proper function.
蛋白磷酸酶 1 调节亚基 3F(PPP1R3F)是糖原靶向亚基(GTS)的成员,糖原靶向亚基属于蛋白磷酸酶 1(PP1)的大调节亚基家族,PP1 是一种主要的真核丝氨酸/苏氨酸蛋白磷酸酶,调节多种细胞过程。在这里,我们描述了与 13 个无关个体中一种新型 X 连锁隐性神经发育障碍相关的 PPP1R3F 半合子变异的鉴定。该疾病的特征是发育迟缓、轻度智力障碍、神经行为问题(如自闭症谱系障碍)、癫痫发作和其他神经学发现,包括肌张力、步态和小脑异常。PPP1R3F 变异与受影响的半合子男性中的疾病分离,这些男性从其杂合载体母亲那里遗传了变异。我们表明,PPP1R3F 主要在大脑星形胶质细胞中表达,并在细胞中定位于内质网。PPP1R3F 敲除星形胶质细胞瘤细胞中的糖原含量似乎比野生型细胞对细胞外葡萄糖水平的变化更敏感,这表明 PPP1R3F 在维持大脑糖原水平的稳定方面发挥作用在不断变化的葡萄糖条件下。我们对鉴定出的 9 种变体进行了功能研究,发现大多数变体在 PP1 结合、蛋白质稳定性、亚细胞定位和糖原代谢调节方面存在缺陷。总的来说,遗传和分子数据表明,PPP1R3F 中的有害变体与一种新的 X 连锁糖原代谢障碍有关,突出了 GTS 在神经发育中的关键作用。这项研究扩展了我们对神经发育障碍以及 PP1 在大脑发育和正常功能中的作用的理解。