Laboratory of Cell Signaling and Metabolic Disorders, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland.
Division of Interdisciplinary Research, Institute of Nuclear Physics, Polish Academy of Sciences, 31-342 Krakow, Poland.
Int J Mol Sci. 2020 Sep 18;21(18):6844. doi: 10.3390/ijms21186844.
Metabolic stress, such as lipotoxicity, affects the DNA methylation profile in pancreatic β-cells and thus contributes to β-cell failure and the progression of type 2 diabetes (T2D). Stearoyl-CoA desaturase 1 (SCD1) is a rate-limiting enzyme that is involved in monounsaturated fatty acid synthesis, which protects pancreatic β-cells against lipotoxicity. The present study found that SCD1 is also required for the establishment and maintenance of DNA methylation patterns in β-cells. We showed that SCD1 inhibition/deficiency caused DNA hypomethylation and changed the methyl group distribution within chromosomes in β-cells. Lower levels of DNA methylation in SCD1-deficient β-cells were followed by lower levels of DNA methyltransferase 1 (DNMT1). We also found that the downregulation of SCD1 in pancreatic β-cells led to the activation of adenosine monophosphate-activated protein kinase (AMPK) and an increase in the activity of the NAD-dependent deacetylase sirtuin-1 (SIRT1). Furthermore, the physical association between DNMT1 and SIRT1 stimulated the deacetylation of DNMT1 under conditions of SCD1 inhibition/downregulation, suggesting a mechanism by which SCD1 exerts control over DNMT1. We also found that SCD1-deficient β-cells that were treated with compound c, an inhibitor of AMPK, were characterized by higher levels of both global DNA methylation and DNMT1 protein expression compared with untreated cells. Therefore, we found that activation of the AMPK/SIRT1 signaling pathway mediates the effect of SCD1 inhibition/deficiency on DNA methylation status in pancreatic β-cells. Altogether, these findings suggest that SCD1 is a gatekeeper that protects β-cells against the lipid-derived loss of DNA methylation and provide mechanistic insights into the mechanism by which SCD1 regulates DNA methylation patterns in β-cells and T2D-relevant tissues.
代谢应激,如脂毒性,会影响胰岛β细胞的 DNA 甲基化谱,从而导致β细胞衰竭和 2 型糖尿病(T2D)的进展。硬脂酰辅酶 A 去饱和酶 1(SCD1)是一种限速酶,参与单不饱和脂肪酸的合成,可保护胰岛β细胞免受脂毒性的影响。本研究发现 SCD1 对于β细胞中 DNA 甲基化模式的建立和维持也是必需的。我们表明,SCD1 抑制/缺失会导致β细胞中的 DNA 低甲基化,并改变染色体内的甲基化分布。SCD1 缺陷型β细胞中较低的 DNA 甲基化水平伴随着较低的 DNA 甲基转移酶 1(DNMT1)水平。我们还发现,胰腺β细胞中 SCD1 的下调导致腺苷单磷酸激活蛋白激酶(AMPK)的激活和 NAD 依赖性去乙酰化酶 SIRT1 的活性增加。此外,在 SCD1 抑制/下调的条件下,DNMT1 和 SIRT1 之间的物理相互作用刺激了 DNMT1 的去乙酰化,这表明了 SCD1 对 DNMT1 进行控制的一种机制。我们还发现,用 AMPK 的抑制剂 compound c 处理 SCD1 缺陷型β细胞后,与未处理的细胞相比,这些细胞的整体 DNA 甲基化水平和 DNMT1 蛋白表达水平都更高。因此,我们发现 AMPK/SIRT1 信号通路的激活介导了 SCD1 抑制/缺失对胰岛β细胞 DNA 甲基化状态的影响。总之,这些发现表明 SCD1 是一种保护β细胞免受脂源性 DNA 甲基化丢失的门卫,并为 SCD1 调节β细胞和与 T2D 相关组织中的 DNA 甲基化模式的机制提供了机制上的见解。