Depleting inositol pyrophosphate 5-InsP7 protected the heart against ischaemia-reperfusion injury by elevating plasma adiponectin

Cardiovasc Res. 2024 Jul 2;120(8):954-970. doi: 10.1093/cvr/cvae017.

Abstract

Aims: Adiponectin is an adipocyte-derived circulating protein that exerts cardiovascular and metabolic protection. Due to the futile degradation of endogenous adiponectin and the challenges of exogenous administration, regulatory mechanisms of adiponectin biosynthesis are of significant pharmacological interest.

Methods and results: Here, we report that 5-diphosphoinositol 1,2,3,4,6-pentakisphosphate (5-InsP7) generated by inositol hexakisphosphate kinase 1 (IP6K1) governed circulating adiponectin levels via thiol-mediated protein quality control in the secretory pathway. IP6K1 bound to adiponectin and DsbA-L and generated 5-InsP7 to stabilize adiponectin/ERp44 and DsbA-L/Ero1-Lα interactions, driving adiponectin intracellular degradation. Depleting 5-InsP7 by either IP6K1 deletion or pharmacological inhibition blocked intracellular adiponectin degradation. Whole-body and adipocyte-specific deletion of IP6K1 boosted plasma adiponectin levels, especially its high molecular weight forms, and activated AMPK-mediated protection against myocardial ischaemia-reperfusion injury. Pharmacological inhibition of 5-InsP7 biosynthesis in wild-type but not adiponectin knockout mice attenuated myocardial ischaemia-reperfusion injury.

Conclusion: Our findings revealed that 5-InsP7 is a physiological regulator of adiponectin biosynthesis that is amenable to pharmacological intervention for cardioprotection.

Keywords: AMPK; DsbA-L; ERp44; Ero1-Lα; IP6K.

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism
  • Adipocytes / drug effects
  • Adipocytes / enzymology
  • Adipocytes / metabolism
  • Adiponectin* / blood
  • Adiponectin* / genetics
  • Adiponectin* / metabolism
  • Animals
  • Disease Models, Animal
  • Humans
  • Inositol Phosphates / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout*
  • Myocardial Reperfusion Injury* / blood
  • Myocardial Reperfusion Injury* / enzymology
  • Myocardial Reperfusion Injury* / genetics
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardial Reperfusion Injury* / pathology
  • Myocardial Reperfusion Injury* / prevention & control
  • Phosphotransferases (Phosphate Group Acceptor) / genetics
  • Phosphotransferases (Phosphate Group Acceptor) / metabolism
  • Proteolysis
  • Signal Transduction

Substances

  • Adiponectin
  • Adipoq protein, mouse
  • Phosphotransferases (Phosphate Group Acceptor)
  • Inositol Phosphates
  • AMP-Activated Protein Kinases
  • Ihpk1 protein, mouse