CXCR4 regulates interneuron migration in the developing neocortex

J Neurosci. 2003 Jun 15;23(12):5123-30. doi: 10.1523/JNEUROSCI.23-12-05123.2003.

Abstract

The chemotactic factors directing interneuron migration during cerebrocortical development are essentially unknown. Here we identify the CXC chemokine receptor 4 (CXCR4) in interneuron precursors migrating from the basal forebrain to the neocortex and demonstrate that stromal cell-derived factor-1 (SDF-1) is a potent chemoattractant for isolated striatal precursors. In addition, we show that CXCR4 is present in early generated Cajal-Retzius cells of the cortical marginal zone. In mice with a null mutation in CXCR4 or SDF-1, interneurons were severely underrepresented in the superficial layers and ectopically placed in the deep layers of the neocortex. In contrast, the submeningeal positioning of Cajal-Retzius cells was unaffected. Thus, our findings suggest that SDF-1, which is highly expressed in the embryonic leptomeninx, selectively regulates migration and layer-specific integration of CXCR4-expressing interneurons during neocortical development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion Molecules, Neuronal / biosynthesis
  • Cell Count
  • Cell Movement / drug effects
  • Cell Movement / physiology*
  • Chemokine CXCL12
  • Chemokines, CXC / deficiency
  • Chemokines, CXC / genetics
  • Chemokines, CXC / physiology
  • Choristoma / genetics
  • Choristoma / pathology
  • Extracellular Matrix Proteins / biosynthesis
  • Gene Expression Regulation, Developmental
  • Immunohistochemistry
  • In Situ Hybridization
  • Interneurons / cytology
  • Interneurons / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neocortex / abnormalities
  • Neocortex / cytology
  • Neocortex / metabolism*
  • Nerve Tissue Proteins
  • Nervous System Malformations / genetics
  • Nervous System Malformations / pathology
  • RNA, Messenger / biosynthesis
  • Rats
  • Rats, Wistar
  • Receptors, CXCR4 / deficiency
  • Receptors, CXCR4 / genetics
  • Receptors, CXCR4 / physiology*
  • Reelin Protein
  • Serine Endopeptidases
  • Signal Transduction / physiology
  • Stem Cells / cytology
  • Stem Cells / metabolism

Substances

  • Cell Adhesion Molecules, Neuronal
  • Chemokine CXCL12
  • Chemokines, CXC
  • Cxcl12 protein, mouse
  • Extracellular Matrix Proteins
  • Nerve Tissue Proteins
  • RNA, Messenger
  • Receptors, CXCR4
  • Reelin Protein
  • Serine Endopeptidases