Restricted STAT5 activation dictates appropriate thymic B versus T cell lineage commitment

J Immunol. 2005 Jun 15;174(12):7753-63. doi: 10.4049/jimmunol.174.12.7753.

Abstract

The molecular mechanisms regulating lymphocyte lineage commitment remain poorly characterized. To explore the role of the IL7R in this process, we generated transgenic mice that express a constitutively active form of STAT5 (STAT5b-CA), a key downstream IL7R effector, throughout lymphocyte development. STAT5b-CA mice exhibit a 40-fold increase in pro-B cells in the thymus. As documented by BrdU labeling studies, this increase is not due to enhanced B cell proliferation. Thymic pro-B cells in STAT5b-CA mice show a modest increase in cell survival ( approximately 4-fold), which correlates with bcl-x(L) expression. However, bcl-x(L) transgenic mice do not show increases in thymic B cell numbers. Thus, STAT5-dependent bcl-x(L) up-regulation and enhanced B cell survival are not sufficient to drive the thymic B cell development observed in STAT5b-CA mice. Importantly, thymic pro-B cells in STAT5b-CA mice are derived from early T cell progenitors (ETPs), suggesting that STAT5 acts by altering ETP lineage commitment. Supporting this hypothesis, STAT5 binds to the pax5 promoter in ETPs from STAT5b-CA mice and induces pax5, a master regulator of B cell development. Conversely, STAT5b-CA mice exhibit a decrease in the DN1b subset of ETPs, demonstrating that STAT5 activation inhibits early T cell differentiation or lineage commitment. On the basis of these findings, we propose that the observed expression of the IL-7R on common lymphoid progenitors, but not ETPs, results in differential STAT5 signaling within these distinct progenitor populations and thus helps ensure appropriate development of B cells and T cells in the bone marrow and thymic environments, respectively.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocyte Subsets / cytology*
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism
  • Cell Lineage / genetics
  • Cell Lineage / immunology
  • Cell Proliferation
  • Cell Survival / genetics
  • Cell Survival / immunology
  • DNA-Binding Proteins / biosynthesis
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • DNA-Binding Proteins / physiology
  • Growth Inhibitors / genetics
  • Growth Inhibitors / metabolism
  • Growth Inhibitors / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Milk Proteins / genetics
  • Milk Proteins / metabolism*
  • PAX5 Transcription Factor
  • Promoter Regions, Genetic
  • Protein Binding / genetics
  • Protein Binding / immunology
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • STAT5 Transcription Factor
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Stem Cells / cytology
  • Stem Cells / immunology
  • Stem Cells / metabolism
  • T-Lymphocyte Subsets / cytology*
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • Thymus Gland / cytology*
  • Thymus Gland / immunology*
  • Thymus Gland / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Trans-Activators / physiology
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Up-Regulation / genetics
  • Up-Regulation / immunology
  • bcl-X Protein

Substances

  • Bcl2l1 protein, mouse
  • DNA-Binding Proteins
  • Growth Inhibitors
  • Milk Proteins
  • PAX5 Transcription Factor
  • Pax5 protein, mouse
  • Proto-Oncogene Proteins c-bcl-2
  • STAT5 Transcription Factor
  • Stat5b protein, mouse
  • Trans-Activators
  • Transcription Factors
  • bcl-X Protein