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Hexokinase 1 forms rings that constrict mitochondria during energy stress

Pilic, J.; Gottschalk, B.; Bourgeois, B.; Koshenov, Z.; Oflaz, F. E.; Erdogan, Y. C.; Shoshan-Barmatz, V.; Madl, T.; Graier, W. F.; Malli, R.

2023-03-21 cell biology
10.1101/2023.03.20.533440 bioRxiv
Show abstract

Metabolic enzymes can adapt during energy stress, but the precise mechanisms and consequences of these adaptations remain understudied. Here, we discovered that hexokinase 1 (HK1), a key glycolytic enzyme, clusters into ring-like structures around mitochondria during energy stress. These HK1-rings constrict mitochondria at contact sites with the endoplasmic reticulum (ER) and prevent mitochondrial fission by displacing the dynamin-related protein 1 (Drp1) from mitochondrial constriction sites. Mechanistically, we identified that the lack of ATP and glucose-6-phosphate (G6P) promotes the clustering of HK1. Moreover, we found several mutations that are critical for the formation of HK1-rings. Utilizing these mutations, we could show that HK1-rings keep mitochondria connected and rewire cellular metabolism during energy stress. Our findings highlight that HK1 is a robust energy stress sensor that regulates the shape, connectivity and metabolic activity of mitochondria. Thus, the formation of HK1-rings may affect mitochondrial function in energy stress-related pathologies.

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