Critical role for leukocyte hypoxia inducible factor-1alpha expression in post-myocardial infarction left ventricular remodeling

Circ Res. 2010 Feb 19;106(3):601-10. doi: 10.1161/CIRCRESAHA.109.208967. Epub 2009 Dec 24.

Abstract

Rationale: Hypoxia inducible factor (HIF)-1alpha is a transcription factor stabilized by hypoxia. It regulates cytokines involved in the inflammatory response after ischemia and affects white blood cell (WBCs) function. The effect of HIF-1alpha on WBC function and inflammation following myocardial infarction (MI) is unknown.

Objective: We assessed peritoneal and myocardial inflammation in the setting of low WBC HIF-1alpha expression through bone marrow transplantation of hematopoietic stem cells transfected with scramble or HIF-1alpha small interfering (si)RNA.

Methods and results: Rosa hematopoietic stem cells (lin(-), cKit(+)) were transfected with a green fluorescent protein (GFP) reporter lentivirus encoding a siRNA to HIF-1alpha or scramble. Irradiated 6- to 8-week-old C57/BL6J mice received 50 000 GFP(+) HIF-1alpha or scramble siRNA-transfected hematopoietic stem cells. Peritonitis or myocardial infarction via left anterior descending coronary artery ligation was induced 6 weeks after bone marrow transplantation. In the peritonitis model, HIF-1alpha siRNA group exhibited a significant decrease in neutrophil and monocyte entry to the peritoneum compared to scramble mice. Similarly neutrophil infiltration into the infarct zone was decreased in the HIF-1alpha siRNA group. No difference of myocardial infarct size was observed between groups. Interestingly, the ejection fraction were similar in both groups at baseline and 3 days post-MI but increased significantly in the HIF-1alpha siRNA group compared to control beginning 7 days after MI. Gene array studies demonstrated that downregulation of WBC HIF-1alpha was associated with decreased WBC CCR1, -2, and -4 expression. Chemotaxis assay results confirmed that decreased monocyte migration induced by downregulation of HIF-1alpha was partially reversed by overexpression of CCR2.

Conclusions: Downregulation of leukocyte HIF-1alpha expression resulted in decreased recruitment of WBC to the sites of inflammation and improvement in cardiac function following MI. Downregulation of HIF-1alpha suppressed WBC cytokine receptors CCR1, -2, and -4, which are necessary for WBC mobilization and recruitment to inflammatory cytokines following MI. The effects of downregulation of leukocyte HIF-1alpha on WBC migration are attributable, at least in part, to the decreased CCR2 expression. These results demonstrate that WBC infiltration into the newly injured myocardium plays a significant role in left ventricular remodeling, but not infarct size.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Transplantation
  • Carboxypeptidases A / biosynthesis
  • Carboxypeptidases A / genetics
  • Chemokine CCL2 / biosynthesis
  • Chemokine CCL2 / genetics
  • Chemotaxis, Leukocyte / physiology
  • Down-Regulation
  • Gene Expression Profiling
  • Gene Knockdown Techniques
  • Hypoxia-Inducible Factor 1, alpha Subunit / antagonists & inhibitors
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology*
  • Leukocytes / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myocardial Infarction / pathology
  • Myocardial Infarction / physiopathology*
  • Neutrophils / physiology
  • Oligonucleotide Array Sequence Analysis
  • Peritonitis / physiopathology
  • RNA, Small Interfering / genetics
  • Radiation Chimera
  • Random Allocation
  • Receptors, CCR1 / biosynthesis
  • Receptors, CCR1 / genetics
  • Receptors, CCR1 / physiology
  • Receptors, CCR2 / biosynthesis
  • Receptors, CCR2 / genetics
  • Receptors, CCR2 / physiology
  • Receptors, CCR4 / biosynthesis
  • Receptors, CCR4 / genetics
  • Receptors, CCR4 / physiology
  • Ventricular Remodeling / genetics
  • Ventricular Remodeling / physiology*

Substances

  • Ccl2 protein, mouse
  • Ccr1 protein, mouse
  • Ccr2 protein, mouse
  • Ccr4 protein, mouse
  • Chemokine CCL2
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • RNA, Small Interfering
  • Receptors, CCR1
  • Receptors, CCR2
  • Receptors, CCR4
  • Carboxypeptidases A
  • Cpa3 protein, mouse