Separation of Notch1 promoted lineage commitment and expansion/transformation in developing T cells

J Exp Med. 2001 Jul 2;194(1):99-106. doi: 10.1084/jem.194.1.99.

Abstract

Notch1 signaling is required for T cell development. We have previously demonstrated that expression of a dominant active Notch1 (ICN1) transgene in hematopoietic stem cells (HSCs) leads to thymic-independent development of CD4(+)CD8(+) double-positive (DP) T cells in the bone marrow (BM). To understand the function of Notch1 in early stages of T cell development, we assessed the ability of ICN1 to induce extrathymic T lineage commitment in BM progenitors from mice that varied in their capacity to form a functional pre-T cell receptor (TCR). Whereas mice repopulated with ICN1 transduced HSCs from either recombinase deficient (Rag-2(-/)-) or Src homology 2 domain--containing leukocyte protein of 76 kD (SLP-76)(-/)- mice failed to develop DP BM cells, recipients of ICN1-transduced Rag-2(-/)- progenitors contained two novel BM cell populations indicative of pre-DP T cell development. These novel BM populations are characterized by their expression of CD3 epsilon and pre-T alpha mRNA and the surface proteins CD44 and CD25. In contrast, complementation of Rag-2(-/)- mice with a TCR beta transgene restored ICN1-induced DP development in the BM within 3 wk after BM transfer (BMT). At later time points, this population selectively and consistently gave rise to T cell leukemia. These findings demonstrate that Notch signaling directs T lineage commitment from multipotent progenitor cells; however, both expansion and leukemic transformation of this population are dependent on T cell-specific signals associated with development of DP thymocytes.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow / physiology
  • Cell Lineage
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Hematopoietic Stem Cells / physiology
  • Hyaluronan Receptors / genetics
  • Hyaluronan Receptors / metabolism
  • Leukemia, T-Cell / genetics
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Transgenic
  • Receptor, Notch1
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Receptors, Antigen, T-Cell, alpha-beta / metabolism
  • Receptors, Cell Surface*
  • Receptors, Interleukin-2 / genetics
  • Receptors, Interleukin-2 / metabolism
  • Signal Transduction
  • T-Lymphocytes / physiology*
  • Thymus Gland / cytology
  • Transcription Factors*

Substances

  • DNA-Binding Proteins
  • Hyaluronan Receptors
  • Membrane Proteins
  • Notch1 protein, mouse
  • Rag2 protein, mouse
  • Receptor, Notch1
  • Receptors, Antigen, T-Cell, alpha-beta
  • Receptors, Cell Surface
  • Receptors, Interleukin-2
  • Transcription Factors
  • V(D)J recombination activating protein 2