Department of Pediatrics, Xiangya Hospital, Central South University, Xiangya Road 87, Changsha, 410005, Hunan, China.
Hunan Intellectual and Developmental Disabilities Research Center, Changsha, 410005, China.
Mol Neurobiol. 2022 Aug;59(8):5056-5069. doi: 10.1007/s12035-022-02900-9. Epub 2022 Jun 6.
Dominant TUBB4A variants result in different phenotypes, including hypomyelination with atrophy of the basal ganglia and cerebellum (H-ABC), dystonia type 4 (DYT4), and isolated hypomyelination. Here, we report four new patients with a novel TUBB4A variant (p.K324T) and three new patients with previously reported variants (p.Q292K, p.V255I, p.E410K). The individual carrying the novel p.K324T variant exhibits epilepsy of infancy with migrating focal seizures (EIMFS), while the other three have isolated hypomyelination phenotype. We also present a study of the cellular effects of TUBB4A variants responsible for H-ABC (p.D249N), DYT4 (p.R2G), a severe combined phenotype with combination of hypomyelination and EIMFS (p.K324T), and isolated hypomyelination (p.Q292K and p.E410K) on microtubule stability and dynamics, neurite outgrowth, dendritic spine development, and kinesin binding. Cellular-based assays reveal that all variants except p.R2G increase microtubule stability, decrease microtubule polymerization rates, reduce axonal outgrowth, and alter the density and shape of dendritic spines. We also find that the p.K324T and p.E410K variants perturb the binding of TUBB4A to KIF1A, a neuron-specific kinesin required for transport of synaptic vesicle precursors. Taken together, our data suggest that impaired microtubule stability and dynamics, defected axonal growth, and dendritic spine development form the common molecular basis of TUBB4A-related leukodystrophy. Impairment of TUBB4A binding to KIF1A is more likely to be involved in the isolated hypomyelination phenotype, which suggests that alterations in kinesin binding may cause different phenotypes. In conclusion, our study extends the spectrum of TUBB4A mutations and related phenotypes and provides insight into why different TUBB4A variants cause distinct clinical phenotypes.
主要 TUBB4A 变异导致不同的表型,包括基底节和小脑萎缩伴轻度脑白质营养不良(H-ABC)、肌张力障碍 4 型(DYT4)和孤立性轻度脑白质营养不良。在这里,我们报告了四个新的 TUBB4A 变异(p.K324T)的新患者和三个以前报道的变异(p.Q292K、p.V255I、p.E410K)的新患者。携带新型 p.K324T 变异的个体表现为婴儿癫痫伴移行性局灶性发作(EIMFS),而其他三个具有孤立性轻度脑白质营养不良表型。我们还介绍了一项研究,研究了导致 H-ABC(p.D249N)、DYT4(p.R2G)、轻度脑白质营养不良和 EIMFS 合并(p.K324T)以及孤立性轻度脑白质营养不良(p.Q292K 和 p.E410K)的 TUBB4A 变异对微管稳定性和动态、神经突生长、树突棘发育和驱动蛋白结合的影响。基于细胞的检测表明,除 p.R2G 外,所有变异都增加了微管稳定性,降低了微管聚合速率,减少了轴突生长,并改变了树突棘的密度和形状。我们还发现 p.K324T 和 p.E410K 变体扰乱了 TUBB4A 与 KIF1A 的结合,KIF1A 是一种神经元特异性驱动蛋白,对于突触小泡前体的运输是必需的。总之,我们的数据表明,微管稳定性和动态受损、轴突生长缺陷和树突棘发育形成了 TUBB4A 相关白质营养不良的共同分子基础。TUBB4A 与 KIF1A 的结合受损更可能与孤立性轻度脑白质营养不良表型有关,这表明驱动蛋白结合的改变可能导致不同的表型。总之,我们的研究扩展了 TUBB4A 突变和相关表型的范围,并深入了解了为什么不同的 TUBB4A 变异导致不同的临床表型。