MMP-9-positive neutrophil infiltration is associated to blood-brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke

Stroke. 2008 Apr;39(4):1121-6. doi: 10.1161/STROKEAHA.107.500868. Epub 2008 Mar 6.

Abstract

Background and purpose: An abnormal expression of some matrix metalloproteinases (MMPs) is related with hemorrhagic transformation events after stroke. Our aim was to investigate MMP-2 and MMP-9 in the ischemic brain and its relation with blood-brain barrier breakdown after hemorrhagic transformation in human stroke.

Methods: We assessed 5 cases of fatal ischemic strokes with hemorrhagic complications; brain samples were obtained from infarct, hemorrhagic, and contralateral tissue. MMP-9 and MMP-2 content was analyzed by zymography and immunohistochemistry was performed to localize MMP-9 and to assess collagen IV integrity in the basal lamina. Laser capture microdissection was performed to isolate blood-brain barrier vessels to study these MMPs.

Results: Overall, MMP-9 levels were higher both in hemorrhagic and nonhemorrhagic infarcted tissue compared to contralateral areas (P<0.0001 and P<0.05). Moreover, levels of the cleaved MMP-9 85kDa-form were significantly elevated in the hemorrhagic compared to nonhemorrhagic and contralateral areas (P=0.033 and P<0.0001). No changes were found for MMP-2 content. Immunostaining revealed a strong MMP-9-positive neutrophil infiltration surrounding brain microvessels associated with severe basal lamina type IV collagen degradation and blood extravasation. Microdissection confirmed that content of MMP-9 was similarly high in microvessel endothelium from hemorrhagic and infarcted areas compared to contralateral hemisphere vessels (P<0.05), pointing to neutrophils surrounding dissected microvessels as the main source of MMP-9 in hemorrhagic areas.

Conclusions: Our results show a strong neutrophil infiltration in the infarcted and hemorrhagic areas with local high MMP-9 content closely related to basal lamina collagen IV degradation and blood-brain barrier breakdown. Microvessel and inflammatory MMP-9 response are associated with hemorrhagic complications after stroke.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basement Membrane / enzymology
  • Basement Membrane / immunology
  • Basement Membrane / pathology
  • Blood-Brain Barrier / enzymology*
  • Blood-Brain Barrier / immunology
  • Blood-Brain Barrier / pathology
  • Brain / enzymology
  • Brain / immunology
  • Brain / pathology
  • Brain Ischemia / immunology
  • Brain Ischemia / metabolism*
  • Brain Ischemia / pathology
  • Cerebral Hemorrhage / immunology
  • Cerebral Hemorrhage / metabolism*
  • Cerebral Hemorrhage / pathology
  • Collagen Type IV / metabolism*
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / immunology
  • Endothelium, Vascular / pathology
  • Female
  • Humans
  • Immunohistochemistry
  • Male
  • Matrix Metalloproteinase 2 / metabolism
  • Matrix Metalloproteinase 9 / metabolism*
  • Neutrophils / pathology
  • Stroke / immunology
  • Stroke / metabolism*
  • Stroke / pathology

Substances

  • Collagen Type IV
  • Matrix Metalloproteinase 2
  • Matrix Metalloproteinase 9