Two-stage evolution of mammalian adipose tissue thermogenesis

• 成果类型: Article
• 署名作者: Keipert, Susanne; Gaudry, Michael J.; Kutschke, Maria; Keuper, Michaela; Dela Rosa, Margeoux A. S.; Cheng, Yiming; Monroy Kuhn, Jose M.; Laterveer, Rutger; Cotrim, Camila A.; Giere, Peter; Perocchi, Fabiana; Feederle, Regina; Crichton, Paul G.; Lutter, Dominik; Jastroch, Martin
• 署名单位: Stockholm University; University of East Anglia; Technical University of Munich; University of Munich; Helmholtz Association; Helmholtz-Center Munich - German Research Center for Environmental Health; German Center for Diabetes Research (DZD); Helmholtz Association; Helmholtz-Center Munich - German Research Center for Environmental Health; Leibniz Institut fur Evolutions und Biodiversitatsforschung; Helmholtz Association; Helmholtz-Center Munich - German Research Center for Environmental Health
• 刊物名称: SCIENCE
• ISSN/ISSBN: 0036-11204
• DOI: 10.1126/science.adg1947
• 发表日期: 2024-06-07
• 页码: 1111-1117
• 关键词: uncoupling protein-1; identification; nucleotides; slc25; ucp1; fat

摘要

Brown adipose tissue (BAT) is a heater organ that expresses thermogenic uncoupling protein 1 (UCP1) to maintain high body temperatures during cold stress. BAT thermogenesis is considered an overarching mammalian trait, but its evolutionary origin is unknown. We show that adipose tissue of marsupials, which diverged from eutherian mammals similar to 150 million years ago, expresses a nonthermogenic UCP1 variant governed by a partial transcriptomic BAT signature similar to that found in eutherian beige adipose tissue. We found that the reconstructed UCP1 sequence of the common eutherian ancestor displayed typical thermogenic activity, whereas therian ancestor UCP1 is nonthermogenic. Thus, mammalian adipose tissue thermogenesis may have evolved in two distinct stages, with a prethermogenic stage in the common therian ancestor linking UCP1 expression to adipose tissue and thermal stress. We propose that in a second stage, UCP1 acquired its thermogenic function specifically in eutherians, such that the onset of mammalian BAT thermogenesis occurred only after the divergence from marsupials.