The adenine nucleotide translocase family underlies cardiac ischemia-reperfusion injury through the mitochondrial permeability pore independently of cyclophilin D

Sci Adv. 2024 Dec 13;10(50):eadp7444. doi: 10.1126/sciadv.adp7444. Epub 2024 Dec 11.

Abstract

The mitochondrial permeability transition pore (mPTP) is implicated in cardiac ischemia-reperfusion (I/R) injury. During I/R, elevated mitochondrial Ca2+ triggers mPTP opening, leading to necrotic cell death. Although nonessential regulators of this pore are characterized, the molecular identity of the pore-forming component remains elusive. Two of these genetically verified regulators are cyclophilin D (CypD) and the adenine nucleotide translocase (ANT) family. We investigated the ANT/CypD relationship in mPTP dynamics and I/R injury. Despite lacking all ANT isoforms, Ca2+-dependent mPTP opening persisted in cardiac mitochondria but was desensitized. This desensitization conferred resistance to I/R injury in ANT-deficient mice. CypD is hypothesized to trigger mPTP opening through isomerization of ANTs at proline-62. To test this, we generated mice that expressed a P62A mutated version of ANT1. These mice showed similar mPTP dynamics and I/R sensitivity as the wild type, indicating that P62 is dispensable for CypD regulation. Together, these data indicate that the ANT family contributes to mPTP opening independently of CypD.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cyclophilins / genetics
  • Cyclophilins / metabolism
  • Mice
  • Mice, Knockout
  • Mitochondria, Heart / metabolism
  • Mitochondrial ADP, ATP Translocases* / genetics
  • Mitochondrial ADP, ATP Translocases* / metabolism
  • Mitochondrial Membrane Transport Proteins / genetics
  • Mitochondrial Membrane Transport Proteins / metabolism
  • Mitochondrial Permeability Transition Pore* / metabolism
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardial Reperfusion Injury* / pathology
  • Peptidyl-Prolyl Isomerase F* / genetics
  • Peptidyl-Prolyl Isomerase F* / metabolism

Substances

  • Mitochondrial Permeability Transition Pore
  • Peptidyl-Prolyl Isomerase F
  • Mitochondrial ADP, ATP Translocases
  • Calcium
  • Mitochondrial Membrane Transport Proteins
  • PPIF protein, mouse
  • Cyclophilins