HNF-1β alleviates podocyte injury in lupus nephritis by maintaining endoplasmic reticulum homeostasis

Lupus Sci Med. 2024 Nov 27;11(2):e001349. doi: 10.1136/lupus-2024-001349.

Abstract

Objective: The current study aims to elucidate the critical function of hepatocyte nuclear factor 1-beta (HNF1-β) in lupus nephritis (LN) by investigating its modulation of the Derlin-1/valosin-containing protein (VCP)/VCP-interacting membrane selenoprotein (VIMP) complex, endoplasmic reticulum (ER) stress and podocyte apoptosis.

Methods: In vitro and in vivo models of LN were established using glomerular podocytes treated with LN serum and MRL/lpr mice, respectively. The expression levels of HNF1-β were analysed in kidney tissues from patients with LN and MRL/lpr mice. To assess the effects of HNF1-β inhibition, an adeno-associated virus vector carrying HNF1-β short hairpin was administered to MRL/lpr mice. In vitro, glomerular podocytes were transfected with HNF1-β small interfering RNA (siRNA) or HNF1-β overexpression plasmids to explore their regulatory effects on the Derlin-1/VCP/VIMP complex and podocyte apoptosis. Dual-luciferase reporter assays and chromatin immunoprecipitation (ChIP) assays were performed to investigate the transcriptional activation of Derlin-1 and VCP promoters by HNF1-β.

Results: A significant decrease in HNF1-β levels was observed in kidney tissues from patients with LN while MRL/lpr mice exhibited an initial compensatory increase followed by a subsequent decrease in renal HNF1-β expression. Overexpression of HNF1-β transcriptionally upregulated Derlin-1 and VCP mitigating LN serum-induced ER stress and podocyte apoptosis. In contrast, HNF1-β inhibition exacerbated renal dysfunction and structural damage in MRL/lpr mice. Interestingly, HNF1-β inhibition transcriptionally repressed ERP44, leading to calcium ions (Ca²+) release-mediated disruption and inactivation of the Derlin-1/VCP/VIMP complex. This finding suggests that HNF1-β not only regulates the expression of key proteins in the Derlin-1/VCP/VIMP complex but also influences their assembly through Ca²+ release regulation.

Conclusion: This study provides novel insights into the regulatory mechanisms of HNF1-β in LN emphasising its impact on the Derlin-1/VCP/VIMP complex, ER stress and podocyte apoptosis. These findings have the potential to inform the development of new diagnostic tools and therapeutic strategies for LN.

Keywords: Autoimmune Diseases; Inflammation; Lupus Nephritis.

MeSH terms

  • Adult
  • Animals
  • Apoptosis*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Disease Models, Animal
  • Endoplasmic Reticulum Stress*
  • Endoplasmic Reticulum* / metabolism
  • Female
  • Hepatocyte Nuclear Factor 1-beta* / genetics
  • Hepatocyte Nuclear Factor 1-beta* / metabolism
  • Homeostasis*
  • Humans
  • Lupus Nephritis* / metabolism
  • Lupus Nephritis* / pathology
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred MRL lpr*
  • Podocytes* / metabolism
  • Podocytes* / pathology

Substances

  • Hepatocyte Nuclear Factor 1-beta
  • Membrane Proteins
  • Cell Cycle Proteins