Protective role of hematopoietic prostaglandin D synthase in transient focal cerebral ischemia in mice

Neuroscience. 2009 Sep 29;163(1):296-307. doi: 10.1016/j.neuroscience.2009.06.027. Epub 2009 Jun 13.

Abstract

Cerebral ischemia/reperfusion injury is characterized by the development of inflammatory response, in which vascular macrophages and endogenous microglia are involved. Recent studies showed marked induction of hematopoietic prostaglandin D synthase (HPGDS) after ischemic/reperfusion injury and its localization in microglia, but the molecular mechanism(s) of HPGDS actions in cerebral ischemia is not clear. To clarify the role of HPGDS in cerebral ischemia, C57BL/6 mice and bone marrow chimera mice with cerebral ischemia/reperfusion injury were treated with (4-benzhydryloxy-(1) {3-(1H-tetrazol-5-yl)-propyl}piperidine (HQL-79), a specific inhibitor of HPGDS. The bone marrow chimera mice exhibit expression of enhanced green fluorescent protein (EGFP) in bone marrow/blood-derived monocytes/macrophages. Mice were subjected to ischemia/reperfusion and either treated with HQL-79 (n=44) or vehicle (n=44). Brain sections prepared at 72 h and 7 days after reperfusion were analyzed for neuronal nuclei (NeuN), HPGDS, ionized calcium-binding adapter molecule 1 (Iba1), inducible NO synthase (iNOS), nitrotyrosine, nuclear factor kappa B (NF-kB) and cyclooxygenase-2 (COX-2). The mortality rate (80%) and infarct size were larger in HQL-79- than vehicle-treated mice (58.7+/-8.5 versus 45.2+/-4.9 mm(3); mean+/-SEM, P<0.0001) at 7 days after reperfusion. HQL-79 reduced NeuN expression in the transition area and Iba1 expression (P<0.0001) in the ischemic peri- and penumbra area, but increased COX-2 (P<0.05) and NF-kB expression (P<0.05) in ischemic penumbra and increased formation of nitrotyrosine (P<0.0001) and iNOS (P<0.0001) in the ischemic core area at 72 h and 7 days after reperfusion. In EGFP chimera mice, HQL-79 increased the migration of Iba1/EGFP-positive bone marrow-derived monocytes/macrophages, and simultaneously upregulated iNOS expression in the ischemic core area (P<0.0001), but increased intrinsic microglia/macrophages in ischemic peri-area and penumbra (P<0.0001) at 72 h and 7 days after reperfusion, suggesting involvement of monocytes/macrophages in HQL-79-induced expansion of ischemic injury. Our results demonstrated that the neuroprotective effects of HPGDS in our model are mediated by suppression of activation and infiltration of inflammatory cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Anti-Inflammatory Agents / therapeutic use
  • Biomarkers / metabolism
  • Bone Marrow Transplantation / methods
  • Brain / drug effects*
  • Brain / enzymology
  • Brain / physiopathology
  • Chemotaxis, Leukocyte / drug effects
  • Chemotaxis, Leukocyte / physiology
  • Disease Models, Animal
  • Encephalitis / drug therapy*
  • Encephalitis / physiopathology
  • Encephalitis / prevention & control
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use
  • Green Fluorescent Proteins / genetics
  • Hypoxia-Ischemia, Brain / drug therapy*
  • Hypoxia-Ischemia, Brain / physiopathology
  • Hypoxia-Ischemia, Brain / prevention & control
  • Intramolecular Oxidoreductases / antagonists & inhibitors
  • Intramolecular Oxidoreductases / metabolism*
  • Ischemic Attack, Transient / drug therapy*
  • Ischemic Attack, Transient / physiopathology
  • Ischemic Attack, Transient / prevention & control
  • Isomerases / antagonists & inhibitors
  • Isomerases / metabolism*
  • Lipocalins / antagonists & inhibitors
  • Lipocalins / metabolism*
  • Macrophages / drug effects
  • Macrophages / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia / drug effects
  • Microglia / physiology
  • Nerve Tissue Proteins / metabolism
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use
  • Nitric Oxide Synthase Type II / metabolism
  • Piperidines / pharmacology
  • Piperidines / therapeutic use
  • Reperfusion Injury / drug therapy*
  • Reperfusion Injury / physiopathology
  • Reperfusion Injury / prevention & control
  • Transplantation Chimera

Substances

  • 4-benzhydryloxy-1-(3-(1H-tetrazol-5-yl-)-propyl)piperidine
  • Anti-Inflammatory Agents
  • Biomarkers
  • Enzyme Inhibitors
  • Lipocalins
  • Nerve Tissue Proteins
  • Neuroprotective Agents
  • Piperidines
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Nitric Oxide Synthase Type II
  • Isomerases
  • Intramolecular Oxidoreductases
  • HPGDS protein, mouse
  • prostaglandin R2 D-isomerase