Faculty of Agriculture and Life Sciences, Lincoln University, Lincoln, Canterbury, New Zealand.
Department of Radiology, University of Otago, Christchurch, Canterbury, New Zealand.
PLoS One. 2022 Apr 11;17(4):e0261544. doi: 10.1371/journal.pone.0261544. eCollection 2022.
The neuronal ceroid lipofuscinoses (NCLs; Batten disease) are fatal, mainly childhood, inherited neurodegenerative lysosomal storage diseases. Sheep affected with a CLN6 form display progressive regionally defined glial activation and subsequent neurodegeneration, indicating that neuroinflammation may be causative of pathogenesis. In this study, aggregation chimeras were generated from homozygous unaffected normal and CLN6 affected sheep embryos, resulting in seven chimeric animals with varied proportions of normal to affected cells. These sheep were classified as affected-like, recovering-like or normal-like, based on their cell-genotype ratios and their clinical and neuropathological profiles. Neuropathological examination of the affected-like animals revealed intense glial activation, prominent storage body accumulation and severe neurodegeneration within all cortical brain regions, along with vision loss and decreasing intracranial volumes and cortical thicknesses consistent with ovine CLN6 disease. In contrast, intercellular communication affecting pathology was evident at both the gross and histological level in the normal-like and recovering-like chimeras, resulting in a lack of glial activation and rare storage body accumulation in only a few cells. Initial intracranial volumes of the recovering-like chimeras were below normal but progressively recovered to about normal by two years of age. All had normal cortical thicknesses, and none went blind. Extended neurogenesis was evident in the brains of all the chimeras. This study indicates that although CLN6 is a membrane bound protein, the consequent defect is not cell intrinsic. The lack of glial activation and inflammatory responses in the normal-like and recovering-like chimeras indicate that newly generated cells are borne into a microenvironment conducive to maturation and survival.
神经元蜡样质脂褐质沉积症(NCLs;Batten 病)是一种致命的、主要发生在儿童时期的遗传性神经退行性溶酶体贮积症。受 CLN6 影响的绵羊会出现进行性区域性胶质细胞激活和随后的神经退行性变,表明神经炎症可能是发病机制的原因。在这项研究中,从同型未受影响的正常和 CLN6 受影响的绵羊胚胎中生成了聚集嵌合体,产生了七个具有不同正常细胞与受影响细胞比例的嵌合动物。这些绵羊根据其细胞基因型比例及其临床和神经病理学特征被归类为受影响样、恢复样或正常样。受影响样动物的神经病理学检查显示,所有皮质脑区均存在强烈的胶质细胞激活、明显的储存体积累和严重的神经退行性变,同时伴有视力丧失以及颅内体积和皮质厚度的减少,与绵羊 CLN6 疾病一致。相比之下,正常样和恢复样嵌合体在大体和组织学水平上都存在影响病理学的细胞间通讯,导致只有少数细胞中出现胶质细胞激活和罕见的储存体积累。恢复样嵌合体的初始颅内体积低于正常水平,但到两岁时逐渐恢复到正常水平。所有嵌合体的皮质厚度均正常,且无失明。所有嵌合体的大脑中均可见到延长的神经发生。这项研究表明,尽管 CLN6 是一种膜结合蛋白,但由此产生的缺陷不是细胞内在的。正常样和恢复样嵌合体中缺乏胶质细胞激活和炎症反应表明,新生成的细胞进入了有利于成熟和存活的微环境。