Neuroprotection by hypoxic preconditioning involves oxidative stress-mediated expression of hypoxia-inducible factor and erythropoietin

Stroke. 2005 Jun;36(6):1264-9. doi: 10.1161/01.STR.0000166180.91042.02. Epub 2005 May 12.

Abstract

Background and purpose: Hypoxic preconditioning is an endogenous protection against subsequent lethal hypoxia, but the mechanism involved is not understood. Hypoxia is followed by reactive oxygen species (ROS) production and induces hypoxia-inducible factor (HIF) and its downstream factor erythropoietin (Epo), which is associated with neuroprotection. We hypothesized that these endogenous processes may contribute to hypoxic preconditioning.

Methods: We used a mouse neuronal culture model, with 2 hours of hypoxia as preconditioning followed by 15 hours of hypoxic insult, and examined the expression of HIF-1alpha, Epo, and their downstream proteins by Western blotting. Copper/zinc-superoxide dismutase (SOD1) transgenic (Tg) mice were used to detect the effect of ROS. Cell survival and apoptosis were detected by mitogen-activated protein 2 quantification, apoptotic-related DNA fragmentation, and caspase-3 fragmentation. Antisense Epo was used to block endogenously produced Epo.

Results: Hypoxic preconditioning was protective in wild-type (Wt) neurons but not in neurons obtained from SOD1 Tg mice. In Wt neurons, HIF-1alpha and Epo expression showed a greater increase after hypoxia compared with Tg neurons and reached a higher level with preconditioned hypoxia, followed by pJak2, pStat5, and nuclear factor kappaB (NF-kappaB) expression. Antisense Epo decreased these downstream proteins and the neuroprotection of hypoxic preconditioning.

Conclusions: Hypoxic preconditioning induces ROS, which may downregulate the threshold for production of HIF-1alpha and Epo expression during subsequent lethal hypoxia, thus exerting neuroprotection through the Jak2-Stat5 and NF-kappaB pathways.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis
  • Blotting, Western
  • Caspase 3
  • Caspases / metabolism
  • Cell Survival
  • Cells, Cultured
  • DNA Fragmentation
  • Erythropoietin / pharmacology*
  • Heterozygote
  • Hypoxia* / metabolism
  • Hypoxia-Inducible Factor 1 / metabolism
  • Ischemic Preconditioning*
  • Janus Kinase 2
  • Mice
  • Mice, Transgenic
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • NF-kappa B / metabolism
  • Neurons / metabolism
  • Neuroprotective Agents / pharmacology
  • Oligonucleotides, Antisense / pharmacology
  • Oxidative Stress*
  • Protein-Tyrosine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Reactive Oxygen Species
  • Recombinant Proteins
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT5 Transcription Factor / metabolism
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase / physiology

Substances

  • Hypoxia-Inducible Factor 1
  • NF-kappa B
  • Neuroprotective Agents
  • Oligonucleotides, Antisense
  • Proto-Oncogene Proteins
  • Reactive Oxygen Species
  • Recombinant Proteins
  • STAT5 Transcription Factor
  • Erythropoietin
  • Superoxide Dismutase
  • Protein-Tyrosine Kinases
  • Jak2 protein, mouse
  • Janus Kinase 2
  • Mitogen-Activated Protein Kinase 1
  • Casp3 protein, mouse
  • Caspase 3
  • Caspases