Metabolic preconditioning in CD4+ T cells restores inducible immune tolerance in lupus-prone mice

JCI Insight. 2021 Oct 8;6(19):e143245. doi: 10.1172/jci.insight.143245.

Abstract

Autoimmune disease has presented an insurmountable barrier to restoration of durable immune tolerance. Previous studies indicate that chronic therapy with metabolic inhibitors can reduce autoimmune inflammation, but it remains unknown whether acute metabolic modulation enables permanent immune tolerance to be established. In an animal model of lupus, we determined that targeting glucose metabolism with 2-deoxyglucose (2DG) and mitochondrial metabolism with metformin enables endogenous immune tolerance mechanisms to respond to tolerance induction. A 2-week course of 2DG and metformin, when combined with tolerance-inducing therapy anti-CD45RB, prevented renal deposition of autoantibodies for 6 months after initial treatment and restored tolerance induction to allografts in lupus-prone mice. The restoration of durable immune tolerance was linked to changes in T cell surface glycosylation patterns, illustrating a role for glycoregulation in immune tolerance. These findings indicate that metabolic therapy may be applied as a powerful preconditioning to reinvigorate tolerance mechanisms in autoimmune and transplant settings that resist current immune therapies.

Keywords: Autoimmune diseases; Autoimmunity; Lupus; Tolerance; Transplantation.

Publication types

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

MeSH terms

  • Animals
  • Antibodies / pharmacology
  • Antimetabolites / pharmacology*
  • CD4-Positive T-Lymphocytes / immunology*
  • Deoxyglucose / pharmacology*
  • Disease Models, Animal
  • Glycolysis / drug effects
  • Glycosylation / drug effects
  • Hypoglycemic Agents / pharmacology*
  • Immune Tolerance / drug effects*
  • Immune Tolerance / immunology
  • Kidney / drug effects*
  • Kidney / immunology
  • Leukocyte Common Antigens / antagonists & inhibitors
  • Leukocyte Common Antigens / immunology*
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / metabolism*
  • Metformin / pharmacology*
  • Mice
  • Oxidative Phosphorylation / drug effects
  • Transplantation Tolerance / drug effects
  • Transplantation Tolerance / immunology
  • Transplantation, Homologous

Substances

  • Antibodies
  • Antimetabolites
  • Hypoglycemic Agents
  • Metformin
  • Deoxyglucose
  • Leukocyte Common Antigens