Specific Notch receptor-ligand interactions control human TCR-αβ/γδ development by inducing differential Notch signal strength

J Exp Med. 2013 Apr 8;210(4):683-97. doi: 10.1084/jem.20121798. Epub 2013 Mar 25.

Abstract

In humans, high Notch activation promotes γδ T cell development, whereas lower levels promote αβ-lineage differentiation. How these different Notch signals are generated has remained unclear. We show that differential Notch receptor-ligand interactions mediate this process. Whereas Delta-like 4 supports both TCR-αβ and -γδ development, Jagged1 induces mainly αβ-lineage differentiation. In contrast, Jagged2-mediated Notch activation primarily results in γδ T cell development and represses αβ-lineage differentiation by inhibiting TCR-β formation. Consistently, TCR-αβ T cell development is rescued through transduction of a TCR-β transgene. Jagged2 induces the strongest Notch signal through interactions with both Notch1 and Notch3, whereas Delta-like 4 primarily binds Notch1. In agreement, Notch3 is a stronger Notch activator and only supports γδ T cell development, whereas Notch1 is a weaker activator supporting both TCR-αβ and -γδ development. Fetal thymus organ cultures in JAG2-deficient thymic lobes or with Notch3-blocking antibodies confirm the importance of Jagged2/Notch3 signaling in human TCR-γδ differentiation. Our findings reveal that differential Notch receptor-ligand interactions mediate human TCR-αβ and -γδ T cell differentiation and provide a mechanistic insight into the high Notch dependency of human γδ T cell development.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / immunology
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Female
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / immunology
  • Jagged-1 Protein
  • Jagged-2 Protein
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Mice
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / immunology*
  • Receptor, Notch3
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Receptors, Antigen, T-Cell, alpha-beta / immunology*
  • Receptors, Antigen, T-Cell, gamma-delta / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / immunology*
  • Receptors, Notch / genetics
  • Receptors, Notch / immunology*
  • Serrate-Jagged Proteins
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • T-Lymphocytes / immunology*
  • Thymus Gland / cytology
  • Thymus Gland / immunology*

Substances

  • Calcium-Binding Proteins
  • Intercellular Signaling Peptides and Proteins
  • JAG1 protein, human
  • JAG2 protein, human
  • Jag1 protein, mouse
  • Jag2 protein, mouse
  • Jagged-1 Protein
  • Jagged-2 Protein
  • Membrane Proteins
  • NOTCH1 protein, human
  • NOTCH3 protein, human
  • Notch1 protein, mouse
  • Notch3 protein, mouse
  • Receptor, Notch1
  • Receptor, Notch3
  • Receptors, Antigen, T-Cell, alpha-beta
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, Notch
  • Serrate-Jagged Proteins