CXCR-4 desensitization is associated with tissue localization of hemopoietic progenitor cells

J Immunol. 2001 Apr 15;166(8):5027-33. doi: 10.4049/jimmunol.166.8.5027.

Abstract

The chemokine stroma-derived factor (SDF)-1, and its receptor, CXCR-4, have been shown to be essential for the translocation of hemopoietic stem cells from the fetal liver to the bone marrow (BM). We hypothesized that if CXCR-4 plays a crucial role in the localization of human hemopoiesis, stem cells from distinct tissue sources should demonstrate distinct CXCR-4 expression or signaling profiles. CD34(+) cells from BM were compared with blood: either mobilized peripheral blood or umbilical cord blood. Unexpectedly, significantly higher levels of CXCR-4 surface expression on CD34(+) cells from blood sources, mobilized peripheral blood, or cord blood were observed compared with BM (p = 0.0005 and p = 0.002, respectively). However, despite lower levels of CXCR-4, responsiveness of the cells to SDF-1 as measured by either calcium flux or transmigration was proportionally greatest in cells derived from BM. Further, internalization of CXCR-4 in response to ligand, associated with receptor desensitization, was significantly lower on BM-derived cells. Therefore, preserved chemokine receptor signaling was highly associated with marrow rather than blood localization. To test the functional effects of perturbing CXCR-4 signaling, adult mice were exposed to the methionine-SDF-1beta analog that induces prolonged down-regulation/desensitization of CXCR-4 and observed mobilization of Lin(-), Sca-1(+), Thy-1(low), and c-kit(+) hemopoietic progenitor cells to the peripheral blood with a >30-fold increase compared with PBS control (p = 0.0007 day 1 and p = 0.004 day 2). These data demonstrate that CXCR-4 expression and function can be dissociated in progenitor cells and that desensitization of CXCR-4 induces stem cell entry into the circulation.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Calcium / metabolism
  • Cell Membrane / immunology
  • Cell Membrane / metabolism
  • Cell Movement / immunology
  • Chemokine CXCL12
  • Chemokines, CXC / physiology
  • Chemotaxis, Leukocyte / immunology
  • Cytokines / administration & dosage
  • Granulocyte Colony-Stimulating Factor / physiology
  • Hematopoietic Stem Cell Mobilization
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / immunology*
  • Hematopoietic Stem Cells / metabolism*
  • Humans
  • Intracellular Fluid / metabolism
  • Ligands
  • Mice
  • Mice, Inbred Strains
  • Organ Specificity / immunology*
  • Receptors, CXCR4 / biosynthesis*
  • Receptors, CXCR4 / blood
  • Receptors, CXCR4 / metabolism
  • Receptors, CXCR4 / physiology*
  • Signal Transduction / immunology

Substances

  • CXCL12 protein, human
  • Chemokine CXCL12
  • Chemokines, CXC
  • Cxcl12 protein, mouse
  • Cytokines
  • Ligands
  • Receptors, CXCR4
  • Granulocyte Colony-Stimulating Factor
  • Calcium