Nox2 in regulatory T cells promotes angiotensin II-induced cardiovascular remodeling

J Clin Invest. 2018 Jul 2;128(7):3088-3101. doi: 10.1172/JCI97490. Epub 2018 Jun 11.

Abstract

The superoxide-generating enzyme Nox2 contributes to hypertension and cardiovascular remodeling triggered by activation of the renin-angiotensin system. Multiple Nox2-expressing cells are implicated in angiotensin II-induced (Ang II-induced) pathophysiology, but the importance of Nox2 in leukocyte subsets is poorly understood. Here, we investigated the role of Nox2 in T cells, particularly Tregs. Mice globally deficient in Nox2 displayed increased numbers of Tregs in the heart at baseline, whereas Ang II-induced effector T cell (Teff) infiltration was inhibited. To investigate the role of Treg Nox2, we generated a mouse line with CD4-targeted Nox2 deficiency (Nox2fl/flCD4Cre+). These animals showed inhibition of Ang II-induced hypertension and cardiac remodeling related to increased tissue-resident Tregs and reduction in infiltrating Teffs, including Th17 cells. The protection in Nox2fl/flCD4Cre+ mice was reversed by anti-CD25 antibody depletion of Tregs. Mechanistically, Nox2-/y Tregs showed higher in vitro suppression of Teff proliferation than WT Tregs, increased nuclear levels of FoxP3 and NF-κB, and enhanced transcription of CD25, CD39, and CD73. Adoptive transfer of Tregs confirmed that Nox2-deficient cells had greater inhibitory effects on Ang II-induced heart remodeling than WT cells. These results identify a previously unrecognized role of Nox2 in modulating suppression of Tregs, which acts to enhance hypertension and cardiac remodeling.

Keywords: Cardiology; Cardiovascular disease; Hypertension; Immunology; T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Angiotensin II / administration & dosage
  • Angiotensin II / metabolism*
  • Angiotensin II / toxicity
  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • Female
  • Forkhead Transcription Factors / metabolism
  • Hypertension / immunology
  • Hypertension / metabolism
  • Hypertension / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Cardiovascular
  • Myocardium / immunology
  • Myocardium / metabolism
  • Myocardium / pathology
  • NADPH Oxidase 2 / deficiency
  • NADPH Oxidase 2 / genetics
  • NADPH Oxidase 2 / metabolism*
  • NF-kappa B / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • T-Lymphocytes, Regulatory / pathology
  • Vascular Remodeling / drug effects
  • Vascular Remodeling / immunology
  • Vascular Remodeling / physiology*

Substances

  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • NF-kappa B
  • Angiotensin II
  • Cybb protein, mouse
  • NADPH Oxidase 2