Nfatc2 and Tob1 have non-overlapping function in T cell negative regulation and tumorigenesis

PLoS One. 2014 Jun 19;9(6):e100629. doi: 10.1371/journal.pone.0100629. eCollection 2014.

Abstract

Nfatc2 and Tob1 are intrinsic negative regulators of T cell activation. Nfatc2-deficient and Tob1-deficient T cells show reduced thresholds of activation; however, whether these factors have independent or overlapping roles in negative regulation of T cell responses has not been previously examined. Here, we show that Nfatc2 knockout (KO) but not Tob1 KO mice have age-associated accumulation of persistently activated T cells in vivo and expansion of the CD44+ memory cell compartment and age-associated lymphocytic infiltrates in visceral organs, without significant changes in numbers of CD4+CD25+Foxp3+ regulatory T cells (Treg). In vitro, CD4+CD25- "conventional" T cells (Tconvs) from both KO strains showed greater proliferation than wild type (WT) Tconvs. However, while Tregs from Nfatc2 KO mice retained normal suppressive function, Tregs from Tob1 KOs had enhanced suppressive activity. Nfatc2 KO Tconvs expanded somewhat more rapidly than WT Tconvs under conditions of homeostatic proliferation, but their accelerated growth capacity was negated, at least acutely, in a lymphoreplete environment. Finally, Nfatc2 KO mice developed a previously uncharacterized increase in B-cell malignancies, which was not accelerated by the absence of Tob1. The data thus support the prevailing hypothesis that Nfatc2 and Tob1 are non-redundant regulators of lymphocyte homeostasis.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / metabolism*
  • B-Lymphocytes / pathology
  • CD4 Antigens / genetics
  • CD4 Antigens / metabolism
  • Carcinogenesis / genetics*
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Cell Transformation, Neoplastic
  • Female
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Gene Deletion
  • Gene Expression Regulation, Neoplastic*
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Intracellular Signaling Peptides and Proteins
  • Lymphoma / genetics*
  • Lymphoma / metabolism
  • Lymphoma / pathology
  • Male
  • Mice
  • Mice, Knockout
  • NFATC Transcription Factors / deficiency
  • NFATC Transcription Factors / genetics*
  • Signal Transduction
  • T-Lymphocytes, Regulatory / metabolism*
  • T-Lymphocytes, Regulatory / pathology

Substances

  • CD4 Antigens
  • Carrier Proteins
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Interleukin-2 Receptor alpha Subunit
  • Intracellular Signaling Peptides and Proteins
  • NFATC Transcription Factors
  • Nfatc2 protein, mouse
  • Tob1 protein, mouse