Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery

Proc Natl Acad Sci U S A. 2012 May 8;109(19):7505-10. doi: 10.1073/pnas.1121146109. Epub 2012 Apr 23.

Abstract

Crosstalk between the brain and systemic responses in blood is increasingly suspected of playing critical roles in stroke. However, how this communication takes place remains to be fully understood. Here, we show that reactive astrocytes can release a damage-associated molecular-pattern molecule called high-mobility-group-box-1 (HMGB1) that promotes endothelial progenitor cell (EPC)-mediated neurovascular remodeling during stroke recovery. Conditioned media from reactive astrocytes increase EPC proliferation in vitro. siRNA suppression of HMGB1 in astrocytes or blockade of the HMGB1 receptor for advanced glycation endproducts in EPCs prevents this effect. In a mouse model of focal cerebral ischemia, reactive astrocytes in the peri-infarct cortex up-regulate HMGB1 at 14 d poststroke, along with an accumulation of endogenous EPCs. In vivo siRNA suppression of HMGB1 blocks this EPC response, reduces peri-infact angiogenesis, and worsens neurological deficits. Taken together, these molecular and in vivo findings support a previously undescribed mechanism of crosstalk between reactive astrocytes and EPCs wherein HMGB1 promotes neurovascular remodeling and functional recovery after stroke and brain injury.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / cytology
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Blotting, Western
  • Brain Ischemia / genetics
  • Brain Ischemia / metabolism
  • Brain Ischemia / physiopathology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cerebral Infarction / genetics
  • Cerebral Infarction / metabolism
  • Cerebral Infarction / physiopathology
  • Culture Media, Conditioned / pharmacology
  • Disease Models, Animal
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • HMGB1 Protein / genetics
  • HMGB1 Protein / metabolism*
  • HMGB1 Protein / pharmacology
  • Humans
  • Immunohistochemistry
  • Interleukin-1beta / pharmacology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • RNA Interference
  • Rats
  • Rats, Sprague-Dawley
  • Recovery of Function
  • Stem Cells / cytology
  • Stem Cells / drug effects
  • Stem Cells / metabolism*
  • Stroke / genetics
  • Stroke / metabolism
  • Stroke / physiopathology
  • Time Factors

Substances

  • Culture Media, Conditioned
  • HMGB1 Protein
  • Interleukin-1beta