Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, People's Republic of China.
Endocrinology Department, Yancheng First People's Hospital, Affiliated Hospital of Medical School, Nanjing University, Yancheng, 224000, People's Republic of China.
Sci Rep. 2024 Aug 27;14(1):19876. doi: 10.1038/s41598-024-71099-7.
Frataxin (FXN) is required for iron-sulfur cluster biogenesis, and its loss causes the early-onset neurodegenerative disease Friedreich ataxia (FRDA). Loss of FXN is a susceptibility factor in the development of diabetes, a common metabolic complication after myocardial hypertrophy in patients with FRDA. The underlying mechanism of FXN deficient-induced hyperglycemia in FRDA is, however, poorly understood. In this study, we confirmed that the FXN deficiency mouse model YG8R develops insulin resistance in elder individuals by disturbing lipid metabolic homeostasis in adipose tissues. Evaluation of lipolysis, lipogenesis, and fatty acid β-oxidation showed that lipolysis is most severely affected in white adipose tissues. Consistently, FXN deficiency significantly decreased expression of lipolytic genes encoding adipose triglyceride lipase (Atgl) and hormone-sensitive lipase (Hsl) resulting in adipocyte enlargement and inflammation. Lipolysis induction by fasting or cold exposure remarkably upregulated FXN expression, though FXN deficiency lessened the competency of lipolysis compared with the control or wild type mice. Moreover, we found that the impairment of lipolysis was present at a young age, a few months earlier than hyperglycemia and insulin resistance. Forskolin, an activator of lipolysis, or pioglitazone, an agonist of PPARγ, improved insulin sensitivity in FXN-deficient adipocytes or mice. We uncovered the interplay between FXN expression and lipolysis and found that impairment of lipolysis, particularly the white adipocytes, is an early event, likely, as a primary cause for insulin resistance in FRDA patients at later age.
铁硫簇生物发生所需的 frataxin(FXN),其缺失会导致早发性神经退行性疾病弗里德里希共济失调症(FRDA)。FXN 的缺失是 FRDA 患者心肌肥厚后发生糖尿病这一常见代谢并发症的易感因素。然而,FRDA 中 FXN 缺乏引起高血糖的潜在机制仍不清楚。在这项研究中,我们通过扰乱脂肪组织中脂质代谢稳态,证实了 FXN 缺陷型 YG8R 小鼠模型在老年个体中存在胰岛素抵抗。对脂肪分解、脂肪生成和脂肪酸 β-氧化的评估表明,白色脂肪组织中的脂肪分解受到的影响最为严重。一致地,FXN 缺乏显著降低了脂肪甘油三酯脂肪酶(Atgl)和激素敏感脂肪酶(Hsl)等脂肪分解基因的表达,导致脂肪细胞增大和炎症。禁食或冷暴露诱导的脂肪分解显著上调了 FXN 的表达,尽管 FXN 缺乏使脂肪分解的能力比对照或野生型小鼠减弱。此外,我们发现脂肪分解的损伤出现在年轻时期,比高血糖和胰岛素抵抗早几个月。脂肪分解的激活剂 forskolin 或 PPARγ 的激动剂吡格列酮改善了 FXN 缺陷型脂肪细胞或小鼠的胰岛素敏感性。我们揭示了 FXN 表达与脂肪分解之间的相互作用,并发现脂肪分解的损伤,尤其是白色脂肪细胞,是 FRDA 患者后期胰岛素抵抗的早期事件,可能是主要原因。