Loss or silencing of the PHD1 prolyl hydroxylase protects livers of mice against ischemia/reperfusion injury

Gastroenterology. 2010 Mar;138(3):1143-54.e1-2. doi: 10.1053/j.gastro.2009.09.057. Epub 2009 Oct 8.

Abstract

Background & aims: Liver ischemia/reperfusion (I/R) injury is a frequent cause of organ dysfunction. Loss of the oxygen sensor prolyl hydroxylase domain enzyme 1 (PHD1) causes tolerance of skeletal muscle to hypoxia. We assessed whether loss or short-term silencing of PHD1 could likewise induce hypoxia tolerance in hepatocytes and protect them against hepatic I/R damage.

Methods: Hepatic ischemia was induced in mice by clamping of the portal vessels of the left lateral liver lobe; 90 minutes later livers were reperfused for 8 hours for I/R experiments. Hepatocyte damage following ischemia or I/R was investigated in PHD1-deficient (PHD1(-/-)) and wild-type mice or following short hairpin RNA-mediated short-term inhibition of PHD1 in vivo.

Results: PHD1(-/-) livers were largely protected against acute ischemia or I/R injury. Among mice subjected to hepatic I/R followed by surgical resection of all nonischemic liver lobes, more than half of wild-type mice succumbed, whereas all PHD1(-/-) mice survived. Also, short-term inhibition of PHD1 through RNA interference-mediated silencing provided protection against I/R. Knockdown of PHD1 also induced hypoxia tolerance of hepatocytes in vitro. Mechanistically, loss of PHD1 decreased production of oxidative stress, which likely relates to a decrease in oxygen consumption as a result of a reprogramming of hepatocellular metabolism.

Conclusions: Loss of PHD1 provided tolerance of hepatocytes to acute hypoxia and protected them against I/R-damage. Short-term inhibition of PHD1 is a novel therapeutic approach to reducing or preventing I/R-induced liver injury.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Hypoxia
  • Cells, Cultured
  • Disease Models, Animal
  • Gene Knockdown Techniques*
  • Hepatocytes / enzymology*
  • Hepatocytes / pathology
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Liver / enzymology*
  • Liver / pathology
  • Liver Diseases / enzymology
  • Liver Diseases / genetics
  • Liver Diseases / pathology
  • Liver Diseases / prevention & control*
  • Male
  • Mice
  • Mice, Knockout
  • Oxidative Stress
  • Oxygen Consumption
  • Procollagen-Proline Dioxygenase / deficiency*
  • Procollagen-Proline Dioxygenase / genetics
  • Procollagen-Proline Dioxygenase / metabolism
  • RNA Interference*
  • Reperfusion Injury / enzymology
  • Reperfusion Injury / genetics
  • Reperfusion Injury / pathology
  • Reperfusion Injury / prevention & control*
  • Time Factors

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • endothelial PAS domain-containing protein 1
  • PHD1 protein, mouse
  • Procollagen-Proline Dioxygenase