Effects of a CCR2 antagonist on macrophages and Toll-like receptor 9 expression in a mouse model of diabetic nephropathy

Am J Physiol Renal Physiol. 2021 Dec 1;321(6):F757-F770. doi: 10.1152/ajprenal.00191.2021. Epub 2021 Nov 1.

Abstract

The pathogenesis of diabetic nephropathy (DN) is related to macrophage (Mφ) recruitment to the kidneys, tumor necrosis factor-α (TNF-α) production, and oxidative stress. Toll-like receptor 9 (TLR9) activation is reportedly involved in systemic inflammation, and it exacerbates this condition in metabolic syndrome. Therefore, we hypothesized that TLR9 plays a role in the pathogenesis of DN. Two subsets of kidney Mφs in DN model (db/db) mice were analyzed using flow cytometry to evaluate their distribution and TLR9 expression and function. Mice were administered the CCR2 antagonist INCB3344 for 8 wk; changes in Mφ distribution and function and its therapeutic effects on DN pathology were examined. Bone marrow-derived CD11bhigh (BM-Mφ) and tissue-resident CD11blow Mφs (Res-Mφ) were identified in the mouse kidneys. As DN progressed, the BM-Mφ number, TLR9 expression, and TNF-α production increased significantly. In Res-Mφs, reactive oxygen species (ROS) production and phagocytic activity were enhanced. INCB3344 decreased albuminuria, serum creatinine level, BM-Mφ abundance, TLR9 expression, and TNF-α production by BM-Mφs and ROS production by Res-Mφs. Both increased activation of BM-Mφ via TLR9 and TNF-α production and increased ROS production by Res-Mφs were involved in DN progression. Thus, inactivating Mφs and their TLR9 expression by INCB3344 is a potential therapeutic strategy for DN.NEW & NOTEWORTHY We classified kidney macrophages (Mφs) into bone marrow-derived Mφs (BM-Mφs) expressing high CD11b and tissue-specific resident Mφ (Res-Mφs) expressing low CD11b. In diabetic nephropathy (DN) model mice, Toll-like receptor 9 (TLR9) expression and TNF-α production via TLR9 activation in BM-Mφs and ROS production in Res-Mφs were enhanced. Furthermore, CCR2 antagonist suppressed the kidney infiltration of BM-Mφs and their function and the ROS production by Res-Mφs, with concomitant TLR9 suppression. Our study presents a new therapeutic strategy for DN.

Keywords: C-C chemokine receptor type 2; Toll-like receptor 9; diabetic nephropathy; macrophage; tumor necrosis factor-α.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diabetic Nephropathies / drug therapy*
  • Diabetic Nephropathies / genetics
  • Diabetic Nephropathies / immunology
  • Diabetic Nephropathies / metabolism
  • Disease Models, Animal
  • Kidney / drug effects*
  • Kidney / immunology
  • Kidney / metabolism
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phagocytosis / drug effects
  • Phenotype
  • Pyrrolidines / pharmacology*
  • Reactive Oxygen Species / metabolism
  • Receptors, CCR2 / antagonists & inhibitors*
  • Receptors, CCR2 / metabolism
  • Receptors, Leptin / genetics
  • Signal Transduction
  • Toll-Like Receptor 9 / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Ccr2 protein, mouse
  • INCB3344
  • Pyrrolidines
  • Reactive Oxygen Species
  • Receptors, CCR2
  • Receptors, Leptin
  • Tlr9 protein, mouse
  • Tnf protein, mouse
  • Toll-Like Receptor 9
  • Tumor Necrosis Factor-alpha
  • leptin receptor, mouse

Associated data

  • figshare/10.6084/m9. figshare.16607996