The PP2A regulatory subunit PPP2R2A controls NAD+ biosynthesis to regulate T cell subset differentiation in systemic autoimmunity

Cell Rep. 2024 Jul 23;43(7):114379. doi: 10.1016/j.celrep.2024.114379. Epub 2024 Jun 17.

Abstract

The protein phosphatase 2A (PP2A) regulatory subunit PPP2R2A is involved in the regulation of immune response. We report that lupus-prone mice with T cells deficient in PPP2R2A display less autoimmunity and nephritis. PPP2R2A deficiency promotes NAD+ biosynthesis through the nicotinamide riboside (NR)-directed salvage pathway in T cells. NR inhibits murine Th17 and promotes Treg cell differentiation, in vitro, by PΑRylating histone H1.2 and causing its reduced occupancy in the Foxp3 loci and increased occupancy in the Il17a loci, leading to increased Foxp3 and decreased Il17a transcription. NR treatment suppresses disease in MRL.lpr mice and restores NAD+-dependent poly [ADP-ribose] polymerase 1 (PARP1) activity in CD4 T cells from patients with systemic lupus erythematosus (SLE), while reducing interferon (IFN)-γ and interleukin (IL)-17 production. We conclude that PPP2R2A controls the level of NAD+ through the NR-directed salvage pathway and promotes systemic autoimmunity. Translationally, NR suppresses lupus nephritis in mice and limits the production of proinflammatory cytokines by SLE T cells.

Keywords: CP: Immunology; CP: Metabolism; NAD(+); NR; PARP1; PP2A; PPP2R2A; Th17; Treg; histone H1.2; systemic lupus erythematosus.

MeSH terms

  • Animals
  • Autoimmunity*
  • Cell Differentiation*
  • Female
  • Forkhead Transcription Factors / metabolism
  • Histones / metabolism
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-17 / metabolism
  • Lupus Erythematosus, Systemic* / immunology
  • Lupus Erythematosus, Systemic* / pathology
  • Lupus Nephritis / genetics
  • Lupus Nephritis / immunology
  • Lupus Nephritis / metabolism
  • Lupus Nephritis / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred MRL lpr
  • NAD* / biosynthesis
  • NAD* / metabolism
  • Niacinamide / analogs & derivatives
  • Poly (ADP-Ribose) Polymerase-1 / metabolism
  • Protein Phosphatase 2* / metabolism
  • Pyridinium Compounds
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • Th17 Cells / immunology
  • Th17 Cells / metabolism

Substances

  • Forkhead Transcription Factors
  • Histones
  • Interferon-gamma
  • Interleukin-17
  • NAD
  • Niacinamide
  • nicotinamide-beta-riboside
  • Poly (ADP-Ribose) Polymerase-1
  • Protein Phosphatase 2
  • Pyridinium Compounds
  • Ppp2r2a protein, mouse