STAT3 is a critical cell-intrinsic regulator of human unconventional T cell numbers and function

J Exp Med. 2015 Jun 1;212(6):855-64. doi: 10.1084/jem.20141992. Epub 2015 May 4.

Abstract

Unconventional T cells such as γδ T cells, natural killer T cells (NKT cells) and mucosal-associated invariant T cells (MAIT cells) are a major component of the immune system; however, the cytokine signaling pathways that control their development and function in humans are unknown. Primary immunodeficiencies caused by single gene mutations provide a unique opportunity to investigate the role of specific molecules in regulating human lymphocyte development and function. We found that individuals with loss-of-function mutations in STAT3 had reduced numbers of peripheral blood MAIT and NKT but not γδ T cells. Analysis of STAT3 mosaic individuals revealed that this effect was cell intrinsic. Surprisingly, the residual STAT3-deficient MAIT cells expressed normal levels of the transcription factor RORγt. Despite this, they displayed a deficiency in secretion of IL-17A and IL-17F, but were able to secrete normal levels of cytokines such as IFNγ and TNF. The deficiency in MAIT and NKT cells in STAT3-deficient patients was mirrored by loss-of-function mutations in IL12RB1 and IL21R, respectively. Thus, these results reveal for the first time the essential role of STAT3 signaling downstream of IL-23R and IL-21R in controlling human MAIT and NKT cell numbers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Separation
  • Cytokines / metabolism
  • Flow Cytometry
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-17 / metabolism
  • Interleukin-23 / metabolism
  • Interleukins / metabolism
  • Killer Cells, Natural / cytology
  • Leukocytes, Mononuclear / cytology
  • Lymphocytes / cytology
  • Mutation
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • Polymorphism, Single Nucleotide
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Receptors, Interleukin / metabolism
  • Receptors, Interleukin-12 / metabolism
  • Receptors, Interleukin-21 / metabolism
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction
  • T-Lymphocytes / cytology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Cytokines
  • IL12RB1 protein, human
  • IL23R protein, human
  • Interleukin-17
  • Interleukin-23
  • Interleukins
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • RORC protein, human
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, Interleukin
  • Receptors, Interleukin-12
  • Receptors, Interleukin-21
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • interleukin-21