Department of Biology, Indiana University, Bloomington, IN 47405, USA.
Department of Biology, Indiana University-Purdue University Indianapolis, Indianapolis, IN 46202, USA.
Insect Biochem Mol Biol. 2020 Dec;127:103493. doi: 10.1016/j.ibmb.2020.103493. Epub 2020 Nov 3.
The oncometabolite L-2-hydroxyglutarate (L-2HG) is considered an abnormal product of central carbon metabolism that is capable of disrupting chromatin architecture, mitochondrial metabolism, and cellular differentiation. Under most circumstances, mammalian tissues readily dispose of this compound, as aberrant L-2HG accumulation induces neurometabolic disorders and promotes renal cell carcinomas. Intriguingly, Drosophila melanogaster larvae were recently found to accumulate high L-2HG levels under normal growth conditions, raising the possibility that L-2HG plays a unique role in insect metabolism. Here we explore this hypothesis by analyzing L-2HG levels in 18 insect species. While L-2HG was present at low-to-moderate levels in most of these species (<100 pmol/mg; comparable to mouse liver), dipteran larvae exhibited a tendency to accumulate high L-2HG concentrations (>100 pmol/mg), with the mosquito Aedes aegypti, the blow fly Phormia regina, and three representative Drosophila species harboring concentrations that exceed 1 nmol/mg - levels comparable to those measured in mutant mice that are unable to degrade L-2HG. Overall, our findings suggest that one of the largest groups of animals on earth commonly generate high concentrations of an oncometabolite during juvenile growth, hint at a role for L-2HG in the evolution of dipteran development, and raise the possibility that L-2HG metabolism could be targeted to restrict the growth of key disease vectors and agricultural pests.
代谢物 L-2-羟戊二酸(L-2HG)被认为是中央碳代谢的异常产物,能够破坏染色质结构、线粒体代谢和细胞分化。在大多数情况下,哺乳动物组织能够轻易处理这种化合物,因为异常的 L-2HG 积累会引起神经代谢紊乱,并促进肾细胞癌的发生。有趣的是,最近发现黑腹果蝇幼虫在正常生长条件下会积累高水平的 L-2HG,这表明 L-2HG 在昆虫代谢中可能发挥独特的作用。在这里,我们通过分析 18 种昆虫物种中的 L-2HG 水平来验证这一假说。虽然在大多数这些物种中(<100 pmol/mg;与小鼠肝脏相当),L-2HG 的水平较低,但双翅目幼虫表现出积累高浓度 L-2HG 的趋势(>100 pmol/mg),其中埃及伊蚊、丝光绿蝇和三种代表性的果蝇物种的 L-2HG 浓度超过 1 nmol/mg - 与那些无法降解 L-2HG 的突变小鼠中测量到的水平相当。总的来说,我们的研究结果表明,地球上最大的动物群体之一在幼年生长过程中通常会产生高浓度的致癌代谢物,这暗示了 L-2HG 在双翅目发育进化中的作用,并提出了 L-2HG 代谢可能被靶向以限制关键疾病载体和农业害虫生长的可能性。