Absence of chemokine (C-x-C motif) ligand 10 diminishes perfusion recovery after local arterial occlusion in mice

Arterioscler Thromb Vasc Biol. 2014 Mar;34(3):594-602. doi: 10.1161/ATVBAHA.113.303050. Epub 2014 Jan 9.

Abstract

Objective: In arteriogenesis, pre-existing anastomoses undergo enlargement to restore blood flow in ischemic tissues. Chemokine (C-X-C motif) ligand 10 (CXCL10) is secreted after Toll-like receptor activation. Toll-like receptors are involved in arteriogenesis; however, the role of CXCL10 is still unclear. In this study, we investigated the role for CXCL10 in a murine hindlimb ischemia model.

Approach and results: Unilateral femoral artery ligation was performed in wild-type (WT) and CXCL10(-/-) knockout (KO) mice and perfusion recovery was measured using laser-Doppler perfusion analysis. Perfusion recovery was significantly lower in KO mice compared with WT at days 4 and 7 after surgery (KO versus WT: 28±5% versus 81±13% at day 4; P=0.003 and 57±12% versus 107±8% at day 7; P=0.003). Vessel measurements of α-smooth muscle actin-positive vessels revealed increasing numbers in time after surgery, which was significantly higher in WT when compared with that in KO. Furthermore, α-smooth muscle actin-positive vessels were significantly larger in WT when compared with those in KO at day 7 (wall thickness, P<0.001; lumen area, P=0.003). Local inflammation was assessed in hindlimb muscles, but this did not differ between WT and KO. Chimerization experiments analyzing perfusion recovery and histology revealed an equal contribution for bone marrow-derived and circulating CXCL10. Migration assays showed a stimulating role for both intrinsic and extrinsic CXCL10 in vascular smooth muscle cell migration.

Conclusions: CXCL10 plays a causal role in arteriogenesis. Bone marrow-derived CXCL10 and tissue-derived CXCL10 play a critical role in accelerating perfusion recovery after arterial occlusion in mice probably by promoting vascular smooth muscle cell recruitment and maturation of pre-existing anastomoses.

Keywords: cell movement; chemokine CXCL10; inflammation; interferon-γ-inducible protein of 10 kDa; myocytes, smooth muscle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta / cytology
  • Bone Marrow / metabolism
  • Cells, Cultured
  • Chemokine CXCL10 / antagonists & inhibitors
  • Chemokine CXCL10 / blood
  • Chemokine CXCL10 / deficiency*
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / pharmacology
  • Chemokine CXCL10 / physiology
  • Collateral Circulation / physiology*
  • Female
  • Femoral Artery
  • Hindlimb / blood supply
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Inflammation
  • Ischemia / physiopathology
  • Laser-Doppler Flowmetry
  • Ligation
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Skeletal / blood supply
  • Muscle, Skeletal / metabolism
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / metabolism
  • Neovascularization, Physiologic / physiology*
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • Radiation Chimera
  • Recombinant Proteins / pharmacology
  • Reperfusion Injury / physiopathology*

Substances

  • CXCL10 protein, human
  • Chemokine CXCL10
  • Cxcl10 protein, mouse
  • RNA, Small Interfering
  • Recombinant Proteins