Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1

Nat Med. 2004 Aug;10(8):858-64. doi: 10.1038/nm1075. Epub 2004 Jul 4.

Abstract

The trafficking of circulating stem and progenitor cells to areas of tissue damage is poorly understood. The chemokine stromal cell-derived factor-1 (SDF-1 or CXCL12) mediates homing of stem cells to bone marrow by binding to CXCR4 on circulating cells. SDF-1 and CXCR4 are expressed in complementary patterns during embryonic organogenesis and guide primordial stem cells to sites of rapid vascular expansion. However, the regulation of SDF-1 and its physiological role in peripheral tissue repair remain incompletely understood. Here we show that SDF-1 gene expression is regulated by the transcription factor hypoxia-inducible factor-1 (HIF-1) in endothelial cells, resulting in selective in vivo expression of SDF-1 in ischemic tissue in direct proportion to reduced oxygen tension. HIF-1-induced SDF-1 expression increases the adhesion, migration and homing of circulating CXCR4-positive progenitor cells to ischemic tissue. Blockade of SDF-1 in ischemic tissue or CXCR4 on circulating cells prevents progenitor cell recruitment to sites of injury. Discrete regions of hypoxia in the bone marrow compartment also show increased SDF-1 expression and progenitor cell tropism. These data show that the recruitment of CXCR4-positive progenitor cells to regenerating tissues is mediated by hypoxic gradients via HIF-1-induced expression of SDF-1.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Analysis of Variance
  • Animals
  • Bone Marrow / metabolism
  • Cell Adhesion / physiology
  • Cell Hypoxia / physiology
  • Cell Movement / physiology*
  • Chemokine CXCL12
  • Chemokines, CXC / metabolism*
  • Chemokines, CXC / physiology
  • DNA-Binding Proteins / metabolism*
  • Disease Models, Animal
  • Endothelial Cells / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Gene Expression Regulation*
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • In Situ Hybridization
  • Ischemia / metabolism*
  • Mice
  • Mice, Nude
  • Nuclear Proteins / metabolism*
  • Precipitin Tests
  • Receptors, CXCR4 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stem Cells / physiology*
  • Transcription Factors*

Substances

  • Chemokine CXCL12
  • Chemokines, CXC
  • Cxcl12 protein, mouse
  • DNA-Binding Proteins
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Nuclear Proteins
  • Receptors, CXCR4
  • Transcription Factors