MiR-126 Contributes to Human Umbilical Cord Blood Cell-Induced Neurorestorative Effects After Stroke in Type-2 Diabetic Mice

Stem Cells. 2016 Jan;34(1):102-13. doi: 10.1002/stem.2193.

Abstract

Diabetes mellitus (DM) is a high risk factor for stroke and leads to more severe vascular and white-matter injury than stroke in non-DM. We tested the neurorestorative effects of delayed human umbilical cord blood cell (HUCBC) treatment of stroke in type-2 diabetes (T2DM). db/db-T2DM and db/+-non-DM mice were subjected to distal middle cerebral artery occlusion (dMCAo) and were treated 3 days after dMCAo with: (a) non-DM + Phosphate buffered saline (PBS); (b) T2DM + PBS; (c) T2DM + naïve-HUCBC; (d) T2DM + miR-126(-/-) HUCBC. Functional evaluation, vascular and white-matter changes, neuroinflammation, and miR-126 effects were measured in vivo and in vitro. T2DM mice exhibited significantly decreased serum and brain tissue miR-126 expression compared with non-DM mice. T2DM + HUCBC mice exhibited increased miR-126 expression, increased tight junction protein expression, axon/myelin, vascular density, and M2-macrophage polarization. However, decreased blood-brain barrier leakage, brain hemorrhage, and miR-126 targeted gene vascular cell adhesion molecule-1 and monocyte chemotactic protein 1 expression in the ischemic brain as well as improved functional outcome were present in HUCBC-treated T2DM mice compared with control T2DM mice. MiR-126(-/-) HUCBC-treatment abolished the benefits of naïve-HUCBC-treatment in T2DM stroke mice. In vitro, knock-in of miR-126 in primary cultured brain endothelial cells (BECs) or treatment of BECs with naïve-HUCBCs significantly increased capillary-like tube formation, and increased axonal outgrowth in primary cultured cortical neurons; whereas treatment of BECs or cortical neurons with miR-126(-/-) HUCBC attenuated HUCBC-treatment-induced capillary tube formation and axonal outgrowth. Our data suggest delayed HUCBC-treatment of stroke increases vascular/white-matter remodeling and anti-inflammatory effects; MiR-126 may contribute to HUCBC-induced neurorestorative effects in T2DM mice.

Keywords: Human umbilical cord blood cell; Stroke; Type-2 diabetes; White matter; microRNA126.

Publication types

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

MeSH terms

  • Animals
  • Axons / metabolism
  • Brain Ischemia / blood
  • Brain Ischemia / complications
  • Brain Ischemia / pathology
  • Cells, Cultured
  • Cerebral Cortex / pathology
  • Chemokine CCL2 / metabolism
  • Coculture Techniques
  • Diabetes Mellitus, Experimental / complications
  • Diabetes Mellitus, Experimental / genetics*
  • Diabetes Mellitus, Experimental / physiopathology
  • Endothelial Cells / metabolism
  • Fetal Blood / metabolism*
  • Gene Knockdown Techniques
  • Male
  • Mice
  • MicroRNAs / blood
  • MicroRNAs / metabolism*
  • Models, Biological
  • Neovascularization, Physiologic
  • Rats, Wistar
  • Recovery of Function
  • Stroke / complications
  • Stroke / genetics*
  • Stroke / physiopathology
  • Tight Junction Proteins / metabolism
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • MIRN126 microRNA, human
  • MIRN126 microRNA, mouse
  • MicroRNAs
  • Tight Junction Proteins
  • Vascular Cell Adhesion Molecule-1