Bone marrow-derived Kruppel-like factor 10 controls reendothelialization in response to arterial injury

Arterioscler Thromb Vasc Biol. 2013 Jul;33(7):1552-60. doi: 10.1161/ATVBAHA.112.300655. Epub 2013 May 16.

Abstract

Objective: The objective of this study was to investigate the role of Kruppel-like factor (KLF) 10, a zinc-finger transcription factor, in bone marrow (BM)-derived cell responses to arterial endothelial injury. Accumulating evidence indicates that BM-derived progenitors are recruited to sites of vascular injury and contribute to endothelial repair.

Approach and results: In response to carotid artery endothelial denudation, KLF10 mRNA expression was markedly increased in both BM and circulating lin(-) progenitor cells. To examine the specific role of KLF10 in arterial reendothelialization, we used 2 models of endothelial denudation (wire- and thermal-induced injury) of the carotid artery in wild-type (WT) and KLF10(-/-) mice. WT mice displayed higher areas of reendothelialization compared with KLF10(-/-) mice after endothelial injury using either method. BM transplant studies revealed that reconstitution of KLF10(-/-) mice with WT BM fully rescued the defect in reendothelialization and increased lin(-)CD34(+)kinase insert domain receptor(+) progenitors in the blood and injured carotid arteries. Conversely, reconstitution of WT mice with KLF10(-/-) BM recapitulated the defects in reendothelialization and peripheral cell progenitors. The media from cultured KLF10(-)/(-) BM progenitors was markedly inefficient in promoting endothelial cell growth and migration compared with the media from WT progenitors, indicative of defective paracrine trophic effects from KLF10(-)/(-) BM progenitors. Finally, BM-derived KLF10(-/-) lin(-) progenitors from reconstituted mice had reduced CXC-chemokine receptor 4 expression and impaired migratory responses.

Conclusions: Collectively, these observations demonstrate a protective role for BM-derived KLF10 in paracrine and homing responses important for arterial endothelial injury and highlight KLF10 as a possible therapeutic target to promote endothelial repair in vascular disease states.

Keywords: Kruppel-like factor 10; bone marrow; endothelial cells; vascular system injuries.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD34 / metabolism
  • Biomarkers / metabolism
  • Bone Marrow Cells / metabolism*
  • Bone Marrow Transplantation
  • Carotid Artery Injuries / genetics
  • Carotid Artery Injuries / metabolism*
  • Carotid Artery Injuries / pathology
  • Cell Proliferation*
  • Chemotaxis
  • Culture Media, Conditioned / metabolism
  • Disease Models, Animal
  • Early Growth Response Transcription Factors / deficiency
  • Early Growth Response Transcription Factors / genetics
  • Early Growth Response Transcription Factors / metabolism*
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Female
  • Gene Expression Regulation
  • Kruppel-Like Transcription Factors / deficiency
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Paracrine Communication*
  • RNA, Messenger / metabolism
  • Receptors, CCR4 / metabolism
  • Signal Transduction
  • Stem Cell Transplantation
  • Stem Cells / metabolism*
  • Time Factors
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism
  • Vascular System Injuries / genetics
  • Vascular System Injuries / metabolism*
  • Vascular System Injuries / pathology

Substances

  • Antigens, CD34
  • Biomarkers
  • CCR4 protein, human
  • Culture Media, Conditioned
  • Early Growth Response Transcription Factors
  • KLF10 protein, mouse
  • Kruppel-Like Transcription Factors
  • RNA, Messenger
  • Receptors, CCR4
  • Vascular Endothelial Growth Factor Receptor-2