ROS-induced ribosome impairment underlies ZAKα-mediated metabolic decline in obesity and aging

Goda Snieckute, Laura Ryder, Anna Constance Vind, Zhenzhen Wu, Frederic Schrøder Arendrup, Mark Stoneley, Sébastien Chamois, Ana Martinez-Val, Marion Leleu, René Dreos, Alexander Russell, David Michael Gay, Aitana Victoria Genzor, Beatrice So-Yun Choi, Astrid Linde Basse, Frederike Sass, Morten Dall, Lucile Chantal Marie Dollet, Melanie Blasius, Anne E WillisAnders H Lund, Jonas T Treebak, Jesper Velgaard Olsen, Steen Seier Poulsen, Mary Elizabeth Pownall, Benjamin Anderschou Holbech Jensen, Christoffer Clemmensen, Zach Gerhart-Hines, David Gatfield, Simon Bekker-Jensen

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Abstract

The ribotoxic stress response (RSR) is a signaling pathway in which the p38- and c-Jun N-terminal kinase (JNK)-activating mitogen-activated protein kinase kinase kinase (MAP3K) ZAKα senses stalling and/or collision of ribosomes. Here, we show that reactive oxygen species (ROS)-generating agents trigger ribosomal impairment and ZAKα activation. Conversely, zebrafish larvae deficient for ZAKα are protected from ROS-induced pathology. Livers of mice fed a ROS-generating diet exhibit ZAKα-activating changes in ribosomal elongation dynamics. Highlighting a role for the RSR in metabolic regulation, ZAK-knockout mice are protected from developing high-fat high-sugar (HFHS) diet-induced blood glucose intolerance and liver steatosis. Finally, ZAK ablation slows animals from developing the hallmarks of metabolic aging. Our work highlights ROS-induced ribosomal impairment as a physiological activation signal for ZAKα that underlies metabolic adaptation in obesity and aging.

Original languageEnglish
Article numbereadf3208
JournalScience (New York, N.Y.)
Volume382
Issue number6675
Number of pages14
ISSN0036-8075
DOIs
Publication statusPublished - 2023

Keywords

  • Mice
  • Animals
  • Reactive Oxygen Species/metabolism
  • Zebrafish
  • Ribosomes/metabolism
  • Aging
  • Obesity/genetics

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