Notch1 and IL-7 receptor interplay maintains proliferation of human thymic progenitors while suppressing non-T cell fates

J Immunol. 2006 Sep 15;177(6):3711-20. doi: 10.4049/jimmunol.177.6.3711.

Abstract

Notch signaling is critical for T cell development of multipotent hemopoietic progenitors. Yet, how Notch regulates T cell fate specification during early thymopoiesis remains unclear. In this study, we have identified an early subset of CD34high c-kit+ flt3+ IL-7Ralpha+ cells in the human postnatal thymus, which includes primitive progenitors with combined lymphomyeloid potential. To assess the impact of Notch signaling in early T cell development, we expressed constitutively active Notch1 in such thymic lymphomyeloid precursors (TLMPs), or triggered their endogenous Notch pathway in the OP9-Delta-like1 stroma coculture. Our results show that proliferation vs differentiation is a critical decision influenced by Notch at the TLMP stage. We found that Notch signaling plays a prominent role in inhibiting non-T cell differentiation (i.e., macrophages, dendritic cells, and NK cells) of TLMPs, while sustaining the proliferation of undifferentiated thymocytes with T cell potential in response to unique IL-7 signals. However, Notch activation is not sufficient for inducing T-lineage progression of proliferating progenitors. Rather, stroma-derived signals are concurrently required. Moreover, while ectopic IL-7R expression cannot replace Notch for the maintenance and expansion of undifferentiated thymocytes, Notch signals sustain IL-7R expression in proliferating thymocytes and induce IL-7R up-regulation in a T cell line. Thus, IL-7R and Notch pathways cooperate to synchronize cell proliferation and suppression of non-T lineage choices in primitive intrathymic progenitors, which will be allowed to progress along the T cell pathway only upon interaction with an inductive stromal microenvironment. These data provide insight into a mechanism of Notch-regulated amplification of the intrathymic pool of early human T cell progenitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cell Proliferation*
  • Cells, Cultured
  • Child, Preschool
  • Growth Inhibitors / physiology*
  • Humans
  • Infant
  • Infant, Newborn
  • Mice
  • Myeloid Progenitor Cells / cytology*
  • Myeloid Progenitor Cells / immunology
  • Myeloid Progenitor Cells / metabolism
  • Organ Culture Techniques
  • Proto-Oncogene Proteins c-kit / biosynthesis
  • Receptor, Notch1 / metabolism
  • Receptor, Notch1 / physiology*
  • Receptors, Interleukin-7 / metabolism
  • Receptors, Interleukin-7 / physiology*
  • Signal Transduction / immunology
  • T-Lymphocytes / cytology*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Thymus Gland / cytology*
  • Thymus Gland / immunology
  • Thymus Gland / metabolism
  • fms-Like Tyrosine Kinase 3 / biosynthesis

Substances

  • Growth Inhibitors
  • NOTCH1 protein, human
  • Receptor, Notch1
  • Receptors, Interleukin-7
  • FLT3 protein, human
  • Proto-Oncogene Proteins c-kit
  • fms-Like Tyrosine Kinase 3