Complex II assembly drives metabolic adaptation to OXPHOS dysfunction

Summary

During acute oxidative phosphorylation (OXPHOS) dysfunction, reversal of succinate dehydrogenase (complex II) maintains the redox state of the Coenzyme Q (Q)-pool by using fumarate as terminal electron acceptor in certain tissues and cell lines. We identified the action of SDHAF2 protein, a complex II assembly factor, as critical for metabolic adaptation during complex III dysfunction in HEK293T cells. SDHAF2 loss during complex III inhibition led to a net reductive TCA cycle from loss of succinate oxidation, loss of SDHA active site-derived reactive oxygen species (ROS) signaling, insufficient glycolytic adaptation, and a severe growth impairment. Glycolysis adapted cells, however, did not accumulate SDHAF2 upon Q-pool stress, exhibited a net reductive TCA cycle and mild growth phenotypes regardless of SDHAF2 presence. Thus, our study reveals how complex II assembly controls a balance between dynamics of TCA cycle directionality, protection from Q-pool stress, and an ability to use ROS-meditated signaling to overcome acute OXPHOS dysfunction in cells reliant on mitochondrial respiration.

Authors Kugapreethan R, Elahee Doomun SN, Sacharz J, Frazier AE, Sharma T, Low YC, Nie S, Leeming MG, Muellner-Wong L, Last K, Stait T, De Souza DP, Thorburn DR, McConville MJ, Stroud DA
Journal Science advances
Publication Date 2025 Aug 15;11(33):eadr6012
PubMed 40815660
PubMed Central PMC12356253
DOI 10.1126/sciadv.adr6012

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