Prolyl-hydroxylase inhibition induces SDF-1 associated with increased CXCR4+/CD11b+ subpopulations and cardiac repair

J Mol Med (Berl). 2017 Aug;95(8):825-837. doi: 10.1007/s00109-017-1543-3. Epub 2017 May 26.

Abstract

SDF-1/CXCR4 activation facilitates myocardial repair. Therefore, we aimed to activate the HIF-1α target genes SDF-1 and CXCR4 by dimethyloxalylglycine (DMOG)-induced prolyl-hydroxylase (PH) inhibition to augment CXCR4+ cell recruitment and myocardial repair. SDF-1 and CXCR4 expression was analyzed under normoxia and ischemia ± DMOG utilizing SDF-1-EGFP and CXCR4-EGFP reporter mice. In bone marrow and heart, CXCR4-EGFP was predominantly expressed in CD45+/CD11b+ leukocytes which significantly increased after myocardial ischemia. PH inhibition with 500 μM DMOG induced upregulation of SDF-1 mRNA in human microvascular endothelial cells (HMEC-1) and aortic vascular smooth muscle cells (HAVSMC). CXCR4 was highly elevated in HMEC-1 but almost no detectable in HAVSMC. In vivo, systemic administration of the PH inhibitor DMOG without pretreatment upregulated nuclear HIF-1α and SDF-1 in the ischemic mouse heart associated with increased recruitment of CD45+/CXCR4-EGFP+/CD11b+ cell subsets. Enhanced PH inhibition significantly upregulated reparative M2 like CXCR4-EGFP+ CD11b+/CD206+ cells compared to inflammatory M2-like CXCR4-EGFP+ CD11b+/CD86+ cells associated with reduced apoptotic cell death, increased neovascularization, reduced scar size, and an improved heart function after MI. In summary, our data suggest increased PH inhibition as a promising tool for a customized upregulation of SDF-1 and CXCR4 expression to attract CXCR4+/CD11b+ cells to the ischemic heart associated with increased cardiac repair.

Key messages: DMOG-induced prolyl-hydroxylase inhibition upregulates SDF-1 and CXCR4 in human endothelial cells. Systemic application of DMOG upregulates nuclear HIF-1α and SDF-1 in vivo. Enhanced prolyl-hydroxylase inhibition increases mainly CXCR4+/CD11b+ cells. DMOG increased reparative M2-like CD11b+/CD206+ cells compared to M1-like cells after MI. Enhanced prolyl-hydroxylase inhibition improved cardiac repair and heart function.

Keywords: CD11b; CXCR4; HIF-1α; Myocardial ischemia; Prolyl-hydroxylases inhibitors; SDF-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids, Dicarboxylic / pharmacology*
  • Animals
  • Apoptosis / drug effects
  • Bone Marrow / metabolism
  • CD11b Antigen / metabolism
  • Cell Line
  • Chemokine CXCL12 / genetics
  • Chemokine CXCL12 / metabolism*
  • Hemodynamics / drug effects
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Mice, Inbred C57BL
  • Myocardial Infarction / genetics
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / physiopathology
  • Myocardium / metabolism
  • Myocytes, Cardiac / metabolism
  • Neovascularization, Physiologic / drug effects
  • Prolyl-Hydroxylase Inhibitors / pharmacology*
  • RNA, Messenger / metabolism
  • Receptors, CXCR4 / genetics

Substances

  • Amino Acids, Dicarboxylic
  • CD11b Antigen
  • Chemokine CXCL12
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Prolyl-Hydroxylase Inhibitors
  • RNA, Messenger
  • Receptors, CXCR4
  • oxalylglycine