Microglia regulate blood clearance in subarachnoid hemorrhage by heme oxygenase-1

J Clin Invest. 2015 Jul 1;125(7):2609-25. doi: 10.1172/JCI78443. Epub 2015 May 26.

Abstract

Subarachnoid hemorrhage (SAH) carries a 50% mortality rate. The extravasated erythrocytes that surround the brain contain heme, which, when released from damaged red blood cells, functions as a potent danger molecule that induces sterile tissue injury and organ dysfunction. Free heme is metabolized by heme oxygenase (HO), resulting in the generation of carbon monoxide (CO), a bioactive gas with potent immunomodulatory capabilities. Here, using a murine model of SAH, we demonstrated that expression of the inducible HO isoform (HO-1, encoded by Hmox1) in microglia is necessary to attenuate neuronal cell death, vasospasm, impaired cognitive function, and clearance of cerebral blood burden. Initiation of CO inhalation after SAH rescued the absence of microglial HO-1 and reduced injury by enhancing erythrophagocytosis. Evaluation of correlative human data revealed that patients with SAH have markedly higher HO-1 activity in cerebrospinal fluid (CSF) compared with that in patients with unruptured cerebral aneurysms. Furthermore, cisternal hematoma volume correlated with HO-1 activity and cytokine expression in the CSF of these patients. Collectively, we found that microglial HO-1 and the generation of CO are essential for effective elimination of blood and heme after SAH that otherwise leads to neuronal injury and cognitive dysfunction. Administration of CO may have potential as a therapeutic modality in patients with ruptured cerebral aneurysms.

Publication types

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

MeSH terms

  • Acute-Phase Reaction / cerebrospinal fluid
  • Animals
  • Apoptosis
  • Carbon Monoxide / administration & dosage
  • Carbon Monoxide / metabolism
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Erythrocytes / pathology
  • Female
  • Heme Oxygenase-1 / antagonists & inhibitors
  • Heme Oxygenase-1 / cerebrospinal fluid
  • Heme Oxygenase-1 / deficiency
  • Heme Oxygenase-1 / physiology*
  • Humans
  • Intracranial Aneurysm / cerebrospinal fluid
  • Intracranial Aneurysm / enzymology
  • Male
  • Maze Learning / physiology
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / deficiency
  • Membrane Proteins / physiology*
  • Metalloporphyrins / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / enzymology*
  • Microglia / pathology
  • Phagocytosis / physiology
  • Protoporphyrins / pharmacology
  • Subarachnoid Hemorrhage / blood*
  • Subarachnoid Hemorrhage / enzymology*
  • Subarachnoid Hemorrhage / pathology

Substances

  • Enzyme Inhibitors
  • Membrane Proteins
  • Metalloporphyrins
  • Protoporphyrins
  • Carbon Monoxide
  • tin protoporphyrin IX
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Hmox1 protein, mouse