Dysregulated heme oxygenase-1low M2-like macrophages augment lupus nephritis via Bach1 induced by type I interferons

Arthritis Res Ther. 2018 Apr 10;20(1):64. doi: 10.1186/s13075-018-1568-1.

Abstract

Background: Innate immunity including macrophages (Mϕ) in lupus nephritis (LN) has been gaining attention, but roles of Mϕ in LN remain uncertain.

Methods: Immunohistochemical staining was performed to determine CD68, CD163, heme oxygenase (HO)-1 (a stress-inducible heme-degrading enzyme with anti-inflammatory property), pSTAT1, and CMAF-expressing Mϕ in the glomeruli of patients with LN. Effects of type I interferons on the expression levels of CD163, HO-1, BTB and CNC homology 1 (Bach1; a transcriptional HO-1 repressor), interleukin (IL)-6, and IL-10 by human M2-like Mϕ, which were differentiated in vitro from peripheral monocytes with macrophage colony-stimulating factor, were assessed by RT-PCR and immunocytostaining. Clinical manifestations, anti-double-stranded DNA (anti-dsDNA), and local HO-1 expression were compared in Bach1-deficient and wild-type MRL/lpr mice.

Results: The number of glomerular M2-like Mϕ correlated with the amounts of proteinuria in patients with LN. Unlike monocyte-derived M2-like Mϕ, HO-1 expression was defective in the majority of glomerular M2-like Mϕ of patients with LN. Stimulation of human M2-like Mϕ with type I interferons led to reduced HO-1 expression and increased Bach1 and IL-6 expression. Bach1-deficient MRL/lpr mice exhibited increased HO-1 expression in kidneys, prolonged survival, reduced urine proteins, and serum blood urea nitrogen levels, but serum anti-dsDNA antibody levels were comparable. Increased expression of CD163 and HO-1 was found in peritoneal Mϕ from Bach1-deficient MRL/lpr mice.

Conclusions: Our data suggest that dysregulated M2-like Mϕ play a proinflammatory role in LN. Bach1 is a potential therapeutic target that could restore the anti-inflammatory property of M2 Mϕ.

Keywords: Bach1; Heme oxygenase 1; Lupus nephritis; Macrophage polarization; Type I interferons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Basic-Leucine Zipper Transcription Factors / deficiency*
  • Cells, Cultured
  • Female
  • Heme Oxygenase-1 / antagonists & inhibitors
  • Heme Oxygenase-1 / biosynthesis*
  • Humans
  • Interferon Type I / pharmacology*
  • Lupus Nephritis / metabolism*
  • Lupus Nephritis / pathology
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Male
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / biosynthesis*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Young Adult

Substances

  • Bach1 protein, mouse
  • Basic-Leucine Zipper Transcription Factors
  • Interferon Type I
  • Membrane Proteins
  • Heme Oxygenase-1
  • Hmox1 protein, mouse