TGF-beta 1 regulates lymphocyte homeostasis by preventing activation and subsequent apoptosis of peripheral lymphocytes

J Immunol. 2003 May 1;170(9):4612-22. doi: 10.4049/jimmunol.170.9.4612.

Abstract

TGF-beta1 plays an important role in the maintenance of immune homeostasis and self-tolerance. To determine the mechanism by which TGF-beta1 prevents autoimmunity we have analyzed T cell activation in splenic lymphocytes from TGF-beta1-deficient mice. Here we demonstrate that unlike wild-type splenic lymphocytes, those from Tgfb1(-/-) mice are hyporesponsive to receptor-mediated mitogenic stimulation, as evidenced by diminished proliferation and reduced IL-2 production. However, they have elevated levels of IFN-gamma and eventually undergo apoptosis. Receptor-independent stimulation of Tgfb1(-/-) T cells by PMA plus ionomycin induces IL-2 production and mitogenic response, and it rescues them from anergy. Tgfb1(-/-) T cells display decreased CD3 expression; increased expression of the activation markers LFA-1, CD69, and CD122; and increased cell size, all of which indicate prior activation. Consistently, mutant CD4(+) T cells have elevated intracellular Ca(2+) levels. However, upon subsequent stimulation in vitro, increases in Ca(2+) levels are less than those in wild-type cells. This is also consistent with the anergic phenotype. Together, these results demonstrate that the ex vivo proliferative hyporesponsiveness of Tgfb1(-/-) splenic lymphocytes is due to prior in vivo activation of T cells resulting from deregulated intracellular Ca(2+) levels.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis / immunology*
  • CD28 Antigens / immunology
  • Calcium / metabolism
  • Cells, Cultured
  • Clonal Anergy / genetics
  • Concanavalin A / pharmacology
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Down-Regulation / immunology*
  • Drug Combinations
  • Immune Sera / pharmacology
  • Interferon-gamma / biosynthesis
  • Interleukin-2 / antagonists & inhibitors
  • Interleukin-2 / biosynthesis
  • Intracellular Fluid / immunology
  • Intracellular Fluid / metabolism
  • Ionomycin / pharmacology
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology*
  • Lymphocyte Subsets / cytology*
  • Lymphocyte Subsets / drug effects
  • Lymphocyte Subsets / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Knockout
  • Mitosis / genetics
  • Mitosis / immunology
  • Spleen / cytology
  • Spleen / immunology
  • Spleen / metabolism
  • T-Lymphocyte Subsets / cytology
  • T-Lymphocyte Subsets / drug effects
  • T-Lymphocyte Subsets / immunology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Transforming Growth Factor beta / deficiency
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / physiology*
  • Transforming Growth Factor beta1
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • CD28 Antigens
  • Drug Combinations
  • Immune Sera
  • Interleukin-2
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Concanavalin A
  • Ionomycin
  • Interferon-gamma
  • Tetradecanoylphorbol Acetate
  • Calcium