Department of Biology, Miami University, Oxford, OH 45056, USA.
Center for Visual Sciences, Miami University, Oxford, OH 45056, USA.
Development. 2024 Aug 1;151(15). doi: 10.1242/dev.202462. Epub 2024 Aug 9.
During tissue regeneration, proliferation, dedifferentiation and reprogramming are necessary to restore lost structures. However, it is not fully understood how metabolism intersects with these processes. Chicken embryos can regenerate their retina through retinal pigment epithelium (RPE) reprogramming when treated with fibroblast factor 2 (FGF2). Using transcriptome profiling, we uncovered extensive regulation of gene sets pertaining to proliferation, neurogenesis and glycolysis throughout RPE-to-neural retina reprogramming. By manipulating cell media composition, we determined that glucose, glutamine or pyruvate are individually sufficient to support RPE reprogramming, identifying glycolysis as a requisite. Conversely, the activation of pyruvate dehydrogenase by inhibition of pyruvate dehydrogenase kinases, induces epithelial-to-mesenchymal transition, while simultaneously blocking the activation of neural retina fate. We also identified that epithelial-to-mesenchymal transition fate is partially driven by an oxidative environment. Our findings provide evidence that metabolism controls RPE cell fate decisions and provide insights into the metabolic state of RPE cells, which are prone to fate changes in regeneration and pathologies, such as proliferative vitreoretinopathy.
在组织再生过程中,增殖、去分化和重编程对于恢复丢失的结构是必要的。然而,代谢如何与这些过程相互作用还不完全清楚。鸡胚胎在接受成纤维细胞生长因子 2 (FGF2) 处理时,可以通过视网膜色素上皮 (RPE) 重编程来再生其视网膜。通过转录组谱分析,我们发现了广泛的基因集调节,这些基因集与增殖、神经发生和糖酵解有关,贯穿于 RPE 到神经视网膜重编程过程中。通过操纵细胞培养基组成,我们确定葡萄糖、谷氨酰胺或丙酮酸单独就足以支持 RPE 重编程,确定糖酵解是必需的。相反,通过抑制丙酮酸脱氢酶激酶来激活丙酮酸脱氢酶,诱导上皮细胞向间充质转化,同时阻止神经视网膜命运的激活。我们还发现上皮细胞向间充质转化命运部分由氧化环境驱动。我们的研究结果提供了证据表明代谢控制 RPE 细胞命运决定,并深入了解了 RPE 细胞的代谢状态,这些细胞在再生和病理学中,如增生性玻璃体视网膜病变,容易发生命运变化。