Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling

Circ Res. 2009 May 8;104(9):1095-102. doi: 10.1161/CIRCRESAHA.108.192138. Epub 2009 Apr 2.

Abstract

We evaluated the healing potential of human fetal aorta-derived CD133(+) progenitor cells and their conditioned medium (CD133(+) CCM) in a new model of ischemic diabetic ulcer. Streptozotocin-induced diabetic mice underwent bilateral limb ischemia and wounding. One wound was covered with collagen containing 2x10(4) CD133(+) or CD133(-) cells or vehicle. The contralateral wound, covered with only collagen, served as control. Fetal CD133(+) cells expressed high levels of wingless (Wnt) genes, which were downregulated following differentiation into CD133(-) cells along with upregulation of Wnt antagonists secreted frizzled-related protein (sFRP)-1, -3, and -4. CD133(+) cells accelerated wound closure as compared with CD133(-) or vehicle and promoted angiogenesis through stimulation of endothelial cell proliferation, migration, and survival by paracrine effects. CD133(+) cells secreted high levels of vascular endothelial growth factor (VEGF)-A and interleukin (IL)-8. Consistently, CD133(+) CCM accelerated wound closure and reparative angiogenesis, with this action abrogated by co-administering the Wnt antagonist sFRP-1 or neutralizing antibodies against VEGF-A or IL-8. In vitro, these effects were recapitulated following exposure of high-glucose-primed human umbilical vein endothelial cells to CD133(+) CCM, resulting in stimulation of migration, angiogenesis-like network formation and induction of Wnt expression. The promigratory and proangiogenic effect of CD133(+) CCM was blunted by sFRP-1, as well as antibodies against VEGF-A or IL-8. CD133(+) cells stimulate wound healing by paracrine mechanisms that activate Wnt signaling pathway in recipients. These preclinical findings open new perspectives for the cure of diabetic ulcers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AC133 Antigen
  • Animals
  • Antigens, CD / analysis
  • Aorta / embryology
  • Cell Differentiation
  • Cell Movement
  • Cell Proliferation
  • Cell Survival
  • Cells, Cultured
  • Culture Media, Conditioned / metabolism
  • Diabetes Mellitus, Experimental / complications*
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / physiopathology
  • Diabetes Mellitus, Experimental / surgery
  • Diabetic Foot / etiology
  • Diabetic Foot / metabolism
  • Diabetic Foot / physiopathology
  • Diabetic Foot / surgery*
  • Fetal Stem Cells / immunology
  • Fetal Stem Cells / metabolism
  • Fetal Stem Cells / transplantation*
  • Glycoproteins / analysis
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Interleukin-8 / metabolism
  • Ischemia / complications*
  • Ischemia / metabolism
  • Ischemia / physiopathology
  • Ischemia / surgery
  • Lower Extremity / blood supply*
  • Male
  • Membrane Proteins / metabolism
  • Mice
  • Neovascularization, Physiologic*
  • Paracrine Communication
  • Peptides / analysis
  • Signal Transduction
  • Stem Cell Transplantation*
  • Time Factors
  • Vascular Endothelial Growth Factor A / metabolism
  • Wnt Proteins / metabolism*
  • Wound Healing*

Substances

  • AC133 Antigen
  • Antigens, CD
  • Culture Media, Conditioned
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Interleukin-8
  • Membrane Proteins
  • PROM1 protein, human
  • Peptides
  • Prom1 protein, mouse
  • Sfrp1 protein, mouse
  • Vascular Endothelial Growth Factor A
  • Wnt Proteins
  • vascular endothelial growth factor A, mouse