Glucose Induces IL-1α-Dependent Inflammation and Extracellular Matrix Proteins Expression and Deposition in Renal Tubular Epithelial Cells in Diabetic Kidney Disease

Front Immunol. 2020 Jul 7:11:1270. doi: 10.3389/fimmu.2020.01270. eCollection 2020.

Abstract

Diabetes mellitus is linked with metabolic stress that induces cellular damage and can provoke renal inflammation and fibrotic responses that eventually lead to chronic kidney disease. Because the inflammasome, interleukin 1 (IL-1), IL-1α/IL-β, and IL-1R are central elements of kidney inflammation and pharmacological IL-1R antagonist (IL-1Ra) was shown to prevent or even reverse diabetic nephropathy (DN) in animal models, we explored the intrinsic expression of IL-1 molecules in kidney tissue of DN patients as regulators of renal inflammation. We used biopsies taken from DN patients and controls and show a high level of IL-1α expression in renal tubular epithelial cells, whereas both IL-1 agonistic molecules (i.e., IL-1α and IL-1β) were devoid of the glomeruli. Human proximal tubular kidney HK-2 cells exposed to high glucose (HG) gradually increase the expression of IL-1α but not IL-1β and induce the expression and deposition of extracellular matrix (ECM) proteins. We further demonstrate that in vitro ectopic addition of recombinant IL-1α in low glucose concentration leads to a similar effect as in HG, while supplementing excess amounts of IL-1Ra in HG significantly attenuates the ECM protein overexpression and deposition. Accordingly, inhibition of IL-1α cleaving protease calpain, but not caspapse-1, also strongly reduces ECM protein production by HK-2 cells. Collectively, we demonstrate that IL-1α and not IL-1β, released from renal tubular cells is the key inflammatory molecule responsible for the renal inflammation in DN. Our result suggests that the clinical use of IL-1Ra in DN should be promoted over the individual neutralization of IL-1α or IL-1β in order to achieve better blocking of IL-1R signaling.

Keywords: alarmins; diabetic nephropathy (DN); extracellular matrix; inflammation; interleukin 1; kidney; stressorin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Biomarkers
  • Cell Line, Tumor
  • Diabetic Nephropathies / etiology
  • Diabetic Nephropathies / metabolism*
  • Diabetic Nephropathies / pathology
  • Epithelial Cells / metabolism*
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism*
  • Female
  • Fluorescent Antibody Technique
  • Gene Expression Regulation
  • Glucose / metabolism*
  • Humans
  • Immunohistochemistry
  • Interleukin-1alpha / genetics
  • Interleukin-1alpha / metabolism*
  • Kidney Tubules / metabolism*
  • Kidney Tubules / pathology
  • Male
  • Middle Aged

Substances

  • Biomarkers
  • Extracellular Matrix Proteins
  • IL1A protein, human
  • Interleukin-1alpha
  • Glucose