Phosphoregulation of the ATP synthase beta subunit stimulates mitochondrial activity for G2/M progression

Adv Biol Regul. 2022 Aug:85:100905. doi: 10.1016/j.jbior.2022.100905. Epub 2022 Aug 19.

Abstract

Mitochondrial ATP synthase is a multifunctional enzyme complex involved in ATP production. We previously reported that the ATP synthase catalytic beta subunit (Atp2p in yeast) is regulated by the 2A-like protein phosphatase Sit4p, which targets Atp2p at T124/T317 impacting on ATP synthase levels and mitochondrial respiration. Here we report that Atp2-T124/T317 is also potentially regulated by Cdc5p, a polo-like mitotic kinase. Since both Cdc5p and Sit4p have established roles in cell cycle regulation, we investigated whether Atp2-T124/T317 phosphorylation was cell cycle-related. We present evidence that Atp2p levels and phosphorylation vary during cell cycle progression, with an increase at G2/M phase. Atp2-T124/T317 phosphorylation stimulates mitochondrial membrane potential, respiration and ATP levels at G2/M phase, indicating that dynamic Atp2p phosphorylation contributes to mitochondrial activity at this specific cell cycle phase. Preventing Atp2p phosphorylation delays G2/M to G1 transition, suggesting that enhanced bioenergetics at G2/M may help meet the energetic demands of cell cycle progression. However, mimicking constitutive T124/T317 phosphorylation or overexpressing Atp2p leads to mitochondrial DNA instability, indicating that reversible Atp2p phosphorylation is critical for homeostasis. These results indicate that transient phosphorylation of Atp2p, a protein at the core of the ATP production machinery, impacts on mitochondrial bioenergetics and supports cell cycle progression at G2/M.

Keywords: Atp2p phosphorylation; Bioenergetics; Cell cycle; Mitochondria; Yeast.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Humans
  • Mitochondria* / genetics
  • Mitochondria* / metabolism
  • Mitochondrial Proton-Translocating ATPases* / genetics
  • Mitochondrial Proton-Translocating ATPases* / metabolism
  • Phosphorylation
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Proton-Translocating ATPases / genetics
  • Proton-Translocating ATPases / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism

Substances

  • Cell Cycle Proteins
  • Saccharomyces cerevisiae Proteins
  • Adenosine Triphosphate
  • Protein Serine-Threonine Kinases
  • CDC5 protein, S cerevisiae
  • Mitochondrial Proton-Translocating ATPases
  • Proton-Translocating ATPases
  • ATP2 protein, S cerevisiae