Department of Pediatrics, Columbia University Medical Center, New York, New York 10032, USA.
J Biol Chem. 2011 Jul 8;286(27):23842-51. doi: 10.1074/jbc.M111.227645. Epub 2011 Apr 13.
Niemann-Pick type C (NP-C) disease is a fatal lysosomal lipid storage disorder for which no effective therapy exists. A genome-wide, conditional synthetic lethality screen was performed using the yeast model of NP-C disease during anaerobiosis, an auxotrophic condition that requires yeast to utilize exogenous sterol. We identified 12 pathways and 13 genes as modifiers of the absence of the yeast NPC1 ortholog (NCR1) and quantified the impact of loss of these genes on sterol metabolism in ncr1Δ strains grown under viable aerobic conditions. Deletion of components of the yeast NuA4 histone acetyltransferase complex in ncr1Δ strains conferred anaerobic inviability and accumulation of multiple sterol intermediates. Thus, we hypothesize an imbalance in histone acetylation in human NP-C disease. Accordingly, we show that the majority of the 11 histone deacetylase (HDAC) genes are transcriptionally up-regulated in three genetically distinct fibroblast lines derived from patients with NP-C disease. A clinically approved HDAC inhibitor (suberoylanilide hydroxamic acid) reverses the dysregulation of the majority of the HDAC genes. Consequently, three key cellular diagnostic criteria of NP-C disease are dramatically ameliorated as follows: lysosomal accumulation of both cholesterol and sphingolipids and defective esterification of LDL-derived cholesterol. These data suggest HDAC inhibition as a candidate therapy for NP-C disease. We conclude that pathways that exacerbate lethality in a model organism can be reversed in human cells as a novel therapeutic strategy. This "exacerbate-reverse" approach can potentially be utilized in any model organism for any disease.
尼曼-匹克 C 型(NP-C)疾病是一种致命的溶酶体脂质贮积病,目前尚无有效的治疗方法。在酵母 NP-C 疾病模型中进行了全基因组条件性合成致死筛选,该模型在无氧条件下(酵母需要利用外源性固醇的营养缺陷条件)进行。我们确定了 12 条途径和 13 个基因作为酵母 NPC1 同源物(NCR1)缺失的修饰因子,并在有氧条件下生长的 ncr1Δ 菌株中定量了这些基因缺失对固醇代谢的影响。在 ncr1Δ 菌株中删除酵母 NuA4 组蛋白乙酰转移酶复合物的成分会导致无氧条件下的致死性和多种固醇中间产物的积累。因此,我们假设在人类 NP-C 疾病中存在组蛋白乙酰化失衡。相应地,我们表明,在源自 NP-C 疾病患者的三个遗传上不同的成纤维细胞系中,大多数 11 个组蛋白去乙酰化酶(HDAC)基因的转录水平上调。一种临床批准的 HDAC 抑制剂(丁氧羰基苯丙氨酸羟肟酸)可逆转大多数 HDAC 基因的失调。因此,NP-C 疾病的三个关键细胞诊断标准得到了显著改善:溶酶体中胆固醇和鞘脂的积累以及 LDL 衍生胆固醇的酯化缺陷。这些数据表明 HDAC 抑制是 NP-C 疾病的候选治疗方法。我们得出结论,在模型生物中加剧致死性的途径可以在人类细胞中逆转,作为一种新的治疗策略。这种“加剧-逆转”方法可潜在地用于任何疾病的任何模型生物。