5-aminolevulinic acid combined with sodium ferrous citrate ameliorated lupus nephritis in a mouse chronic graft-versus-host disease model

Int Immunopharmacol. 2021 Jul:96:107626. doi: 10.1016/j.intimp.2021.107626. Epub 2021 Apr 13.

Abstract

Systemic lupus erythematosus (SLE) is a systemic autoimmune disease characterized by the abnormal activation of immune cells and hypersecretion of autoantibodies and causes irreversible chronic damage, such as lupus nephritis. Chronic graft-versus-host-disease (cGvHD) in mice induced by the injection of parental mouse lymphocytes into F1 hybrids leads to a disease similar to SLE. 5-aminolevulinic acid (5-ALA) is a key progenitor of heme, and its combination with sodium ferrous citrate (SFC) can up-regulate the heme oxygenase (HO-1) expression, resulting in an anti-inflammatory effect. While HO-1 had been reported to be involved in T cell activation and can limit immune-based tissue damage through Treg suppression, which promotes effector response. Thus, we hypothesized that treatment with 5-ALA/SFC could ameliorate lupus nephritis in a mouse cGvHD model. Our results showed that 5-ALA/SFC-treatment significantly decreased the anti-double-stranded DNA (ds-DNA) autoantibodies, blood urea nitrogen (BUN) and creatinine (Cre) levels, reduced kidney inflammatory dendritic cells (DCs) and B cell activation, and increased the regulatory T cells (Tregs) at nine weeks. Furthermore, 5-ALA/SFC suppressed mRNA expression of TNF-α, IL-1β, IFN-γ and markers on DCs. In addition, we also found that 5-ALA/SFC treatment increased the HO-1 expression on donor-derived DCs and Tregs concurrently, increased the number of Tregs, and reduced the population of activated DCs, B cells and CD8+ T cells at three weeks (early stage of the disease). We thus identified a novel role of 5-ALA/SFC for therapeutically improving the symptoms of lupus nephritis in a mouse cGvHD model and expanded the current understanding of how this immunoregulatory agent can be used to generate beneficial immune responses and treat autoimmune disease.

Keywords: 5-aminolevulinic acid; CD8(+) T cell; Chronic graft-versus-host-disease; Sodium ferrous citrate; Systemic lupus erythematosus.

MeSH terms

  • Aminolevulinic Acid
  • Animals
  • B-Lymphocytes / drug effects
  • Blood Urea Nitrogen
  • Body Weight / drug effects
  • CD8-Positive T-Lymphocytes / drug effects
  • Citric Acid / pharmacology*
  • Citric Acid / therapeutic use
  • Creatine / blood
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Drug Therapy, Combination
  • Female
  • Ferrous Compounds / pharmacology*
  • Ferrous Compounds / therapeutic use
  • Fibrosis / metabolism
  • Fibrosis / prevention & control
  • Graft vs Host Disease / complications
  • Graft vs Host Disease / drug therapy*
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism
  • Levulinic Acids / pharmacology*
  • Levulinic Acids / therapeutic use
  • Lupus Nephritis / etiology
  • Lupus Nephritis / pathology
  • Lupus Nephritis / prevention & control*
  • Lymphocyte Activation / drug effects
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Spleen / drug effects
  • Spleen / immunology
  • T-Lymphocytes, Regulatory / drug effects

Substances

  • Cytokines
  • Ferrous Compounds
  • Levulinic Acids
  • Membrane Proteins
  • Citric Acid
  • ferrous citrate
  • Heme Oxygenase-1
  • Hmox1 protein, mouse
  • Creatine