Impact of the neutrophil response to granulocyte colony-stimulating factor on the risk of hemorrhage when used in combination with tissue plasminogen activator during the acute phase of experimental stroke

J Neuroinflammation. 2014 May 27:11:96. doi: 10.1186/1742-2094-11-96.

Abstract

Background: Granulocyte colony-stimulating factor (G-CSF) is a pharmacologic agent inducing neutrophil mobilization and a new candidate for neuroprotection and neuroregeneration in stroke. Its effects when used in combination with tissue plasminogen activator (tPA) were explored during the acute phase of ischemic stroke.

Methods: We used a middle cerebral artery occlusion (MCAO) model of cerebral ischemia, associated with treatment with tPA, in male spontaneously hypertensive rats (SHR). Granulocyte colony-stimulating factor (G-CSF; 60 μg/kg) was injected just before tPA. Neutrophil response in peripheral blood and in the infarct area was quantified in parallel to the infarct volume. Protease matrix metallopeptidase 9 (MMP-9) release from circulating neutrophils was analyzed by immunochemistry and zymography. Vascular reactivity and hemorrhagic volume in the infarct area was also assessed.

Results: Twenty four hours after ischemia and tPA, G-CSF administration induced a significant increase of neutrophils in peripheral blood (P <0.05). At 72 hours post-ischemia, G-CSF was significantly associated with an increased risk of hemorrhage in the infarct area (2.5 times more likely; P <0.05) and significant cerebral endothelium-dependent dysfunction. Ex vivo, an increased MMP-9 release from neutrophils after tPA administration correlated to the increased hemorrhagic risk (P <0.05). In parallel, G-CSF administration was associated with a decreased neutrophil infiltration in the infarct area (-50%; P <0.05), with a concomitant significant neuroprotective effect (infarct volume: -40%; P <0.05).

Conclusions: We demonstrate that G-CSF potentiates the risk of hemorrhage in experimental stroke when used in combination with tPA by inducing neutrophilia. This effect is concomitant to an increased MMP-9 release from peripheral neutrophils induced by the tPA treatment. These results highlight the potential hemorrhagic risk of associating G-CSF to thrombolysis during the acute phase of stroke.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Infarction / etiology
  • Disease Models, Animal
  • Drug Administration Schedule
  • Endothelium / drug effects
  • Fibrinolytic Agents / adverse effects*
  • Granulocyte Colony-Stimulating Factor / administration & dosage*
  • Hemorrhage / chemically induced*
  • Infarction, Middle Cerebral Artery / drug therapy*
  • Male
  • Matrix Metalloproteinase 9 / metabolism
  • Neutrophil Infiltration / drug effects
  • Neutrophils / drug effects*
  • Neutrophils / metabolism
  • Peroxidase / metabolism
  • Rats
  • Rats, Inbred SHR
  • Reperfusion Injury / drug therapy
  • Reperfusion Injury / etiology
  • Statistics, Nonparametric
  • Time Factors
  • Tissue Plasminogen Activator / adverse effects*

Substances

  • Fibrinolytic Agents
  • Granulocyte Colony-Stimulating Factor
  • Peroxidase
  • Tissue Plasminogen Activator
  • Matrix Metalloproteinase 9