A novel potential target of IL-35-regulated JAK/STAT signaling pathway in lupus nephritis

Clin Transl Med. 2021 Feb;11(2):e309. doi: 10.1002/ctm2.309.

Abstract

Background: In this study, we have investigated the potential regulatory mechanisms of IL-35 to relieve lupus nephritis (LN) through regulating Janus kinase (JAK)/signal transducers and activators of transcription (STAT) signaling pathway in mesangial cells.

Results: Among 105 significant differentially expressed proteins (DEPs) between juvenile systemic lupus erythematosus (JSLE) patients with LN and healthy controls, LAIR1, PDGFRβ, VTN, EPHB4, and EPHA4 were downregulated in JSLE-LN. They consist of an interactive network with PTPN11 and FN1, which involved in IL-35-related JAK/STAT signaling pathway. Besides, urinary LAIR1 was significantly correlated with JSLE-LN clinical parameters such as SLEDAI-2K, %CD19+ B, and %CD3+ T cells. Through bioinformatics analysis of co-immunoprecipitation with mass spectrometry results, including GO, KEGG, and STRING, five genes interacted with Lair1 were upregulated by IL-35, but only Myh10 was downregulated. Therefore, we presumed an interactive network among these DEPs, JAK/STAT, and IL-35. Moreover, the downregulated phosphorylated (p)-STAT3, p-p38 MAPK, and p-ERK, and the upregulated p-JAK2/p-STAT1/4 in IL-35 overexpressed mesangial cells, and RNA-sequencing results validated the potential regulatory mechanisms of IL-35 in alleviating JSLE-LN disease. Moreover, the relieved histopathological features of nephritis including urine protein and leukocyte scores, a decreased %CD90+ αSMA+ mesangial cells and pro-inflammatory cytokines, the inactivated JAK/STAT signals and the significant upregulated Tregs in spleen, thymus and peripheral blood were validated in Tregs and IL-35 overexpression plasmid-treated lupus mice.

Conclusions: Our study provided a reference proteomic map of urinary biomarkers for JSLE-LN and elucidated evidence that IL-35 may regulate the interactive network of LAIR1-PTPN11-JAK-STAT-FN1 to affect JAK/STAT and MAPK signaling pathways to alleviate inflammation in JSLE-LN. This finding may provide a further prospective mechanism for JSLE-LN clinical treatment.

Keywords: IL-35; JAK/STAT signaling pathway; JSLE-LN; LAIR1; mesangial calls.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / urine
  • Child
  • Child, Preschool
  • Disease Models, Animal
  • Female
  • Humans
  • Interleukins / genetics*
  • Interleukins / urine*
  • Janus Kinases / genetics
  • Janus Kinases / urine*
  • Lupus Nephritis / genetics*
  • Lupus Nephritis / urine*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • STAT Transcription Factors / genetics
  • STAT Transcription Factors / urine*
  • Signal Transduction / genetics*

Substances

  • Biomarkers
  • Interleukins
  • STAT Transcription Factors
  • interleukin-35, human
  • Janus Kinases