Russier Marion, Fiore Alessandra, Bici Ana, Groß Annette, Tanzer Maria, Yeroslaviz Assa, Mann Matthias, Murray Peter J
Immunoregulation Research Group, Max Planck Institute of Biochemistry, Martinsried, Germany.
Department of Proteomics and Signal Transduction, Max Planck Institute of Biochemistry, Martinsried, Germany.
Life Sci Alliance. 2025 Sep 5;8(11). doi: 10.26508/lsa.202503324. Print 2025 Nov.
Amino acid (AA) detection is fundamental for cellular function, balancing translation demands, biochemical pathways, and signaling networks. Although the GCN2 and mTORC1 pathways are known to regulate AA sensing, the global cellular response to AA deprivation remains poorly understood, particularly in non-transformed cells, which may exhibit distinct adaptive strategies compared with cancer cells. Here, we employed murine pluripotent embryonic stem (ES) cells as a model system to dissect responses to AA stress. Using multi-omics analyses over an extended time course, we examined the effects of arginine (Arg) and leucine (Leu) deprivation. We uncovered a broad array of proteomic, phosphoproteomic, transcriptomic, and metabolomic adaptations, including an increase in lysosome production, all occurring without lethality. We found that Arg or Leu starvation induces reversible cell cycle exit, promoting a quiescent state that enhances resistance to cytotoxic stressors. In contrast, cysteine (Cys) and threonine (Thr) deprivation led to cell death via distinct pathways: ferroptosis for Cys starvation, whereas Thr deprivation triggered a previously uncharacterized form of cell death, which could be entirely suppressed by methionine (Met) co-starvation, and mTOR or translational inhibition. These findings suggest that ES cells implement specialized survival strategies in response to different AA limitations, highlighting their ability to reprogram cellular biochemistry under nutrient stress.
氨基酸(AA)检测对于细胞功能、平衡翻译需求、生化途径和信号网络至关重要。尽管已知GCN2和mTORC1途径可调节氨基酸感知,但细胞对氨基酸剥夺的整体反应仍知之甚少,尤其是在未转化细胞中,与癌细胞相比,这些细胞可能表现出不同的适应性策略。在这里,我们采用小鼠多能胚胎干细胞作为模型系统来剖析对氨基酸应激的反应。通过在延长的时间过程中进行多组学分析,我们研究了精氨酸(Arg)和亮氨酸(Leu)剥夺的影响。我们发现了广泛的蛋白质组学、磷酸蛋白质组学、转录组学和代谢组学适应性变化,包括溶酶体产生增加,所有这些变化都不会导致细胞死亡。我们发现精氨酸或亮氨酸饥饿会诱导可逆的细胞周期退出,促进静止状态,增强对细胞毒性应激源的抵抗力。相比之下,半胱氨酸(Cys)和苏氨酸(Thr)剥夺通过不同途径导致细胞死亡:半胱氨酸饥饿导致铁死亡,而苏氨酸剥夺引发一种以前未被描述的细胞死亡形式,甲硫氨酸(Met)共饥饿、mTOR或翻译抑制可完全抑制这种细胞死亡。这些发现表明,胚胎干细胞针对不同的氨基酸限制实施专门的生存策略,突出了它们在营养应激下重新编程细胞生物化学的能力。