Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany.
Department of Genetics, University of Alabama at Birmingham, Birmingham, AL, 36394, USA.
Hum Genet. 2020 Apr;139(4):483-498. doi: 10.1007/s00439-019-02105-6. Epub 2020 Feb 13.
Biallelic variants in TOR1AIP1, encoding the integral nuclear membrane protein LAP1 (lamina-associated polypeptide 1) with two functional isoforms LAP1B and LAP1C, have initially been linked to muscular dystrophies with variable cardiac and neurological impairment. Furthermore, a recurrent homozygous nonsense alteration, resulting in loss of both LAP1 isoforms, was identified in seven likely related individuals affected by multisystem anomalies with progeroid-like appearance and lethality within the 1st decade of life. Here, we have identified compound heterozygosity in TOR1AIP1 affecting both LAP1 isoforms in two unrelated individuals affected by congenital bilateral hearing loss, ventricular septal defect, bilateral cataracts, mild to moderate developmental delay, microcephaly, mandibular hypoplasia, short stature, progressive muscular atrophy, joint contractures and severe chronic heart failure, with much longer survival. Cellular characterization of primary fibroblasts of one affected individual revealed absence of both LAP1B and LAP1C, constitutively low lamin A/C levels, aberrant nuclear morphology including nuclear cytoplasmic channels, and premature senescence, comparable to findings in other progeroid forms of nuclear envelopathies. We additionally observed an abnormal activation of the extracellular signal-regulated kinase 1/2 (ERK 1/2). Ectopic expression of wild-type TOR1AIP1 mitigated these cellular phenotypes, providing further evidence for the causal role of identified genetic variants. Altogether, we thus further expand the TOR1AIP1-associated phenotype by identifying individuals with biallelic loss-of-function variants who survived beyond the 1st decade of life and reveal novel molecular consequences underlying the TOR1AIP1-associated disorders.
双等位基因变异在 TOR1AIP1 中,编码具有两种功能性同工型 LAP1(核膜相关多肽 1)的完整核膜蛋白 LAP1,最初与具有可变心脏和神经损伤的肌肉营养不良有关。此外,在七个可能相关的个体中发现了一种反复出现的纯合无义改变,导致两种 LAP1 同工型丢失,这些个体受多系统异常影响,表现出类早老样外观和生命在生命的第一个十年内丧失。在这里,我们在两个无关个体中鉴定了 TOR1AIP1 的复合杂合性,影响了两种 LAP1 同工型,这两个个体受先天性双侧听力损失、室间隔缺损、双侧白内障、轻度至中度发育迟缓、小头畸形、下颌发育不良、身材矮小、进行性肌肉萎缩、关节挛缩和严重慢性心力衰竭的影响,存活时间更长。受影响个体的原代成纤维细胞的细胞特征显示两种 LAP1B 和 LAP1C 均缺失,层粘连蛋白 A/C 水平持续较低,核形态异常包括核细胞质通道,以及过早衰老,与其他核包膜疾病的早老形式的发现相当。我们还观察到细胞外信号调节激酶 1/2(ERK 1/2)的异常激活。野生型 TOR1AIP1 的异位表达减轻了这些细胞表型,为鉴定的遗传变异的因果作用提供了进一步的证据。总之,我们通过鉴定在生命的第一个十年后存活的具有双等位基因功能丧失变异的个体,进一步扩展了 TOR1AIP1 相关表型,并揭示了 TOR1AIP1 相关疾病的新分子后果。