CUX1 and IκBζ (NFKBIZ) mediate the synergistic inflammatory response to TNF and IL-17A in stromal fibroblasts

Proc Natl Acad Sci U S A. 2020 Mar 10;117(10):5532-5541. doi: 10.1073/pnas.1912702117. Epub 2020 Feb 20.

Abstract

The role of stromal fibroblasts in chronic inflammation is unfolding. In rheumatoid arthritis, leukocyte-derived cytokines TNF and IL-17A work together, activating fibroblasts to become a dominant source of the hallmark cytokine IL-6. However, IL-17A alone has minimal effect on fibroblasts. To identify key mediators of the synergistic response to TNF and IL-17A in human synovial fibroblasts, we performed time series, dose-response, and gene-silencing transcriptomics experiments. Here we show that in combination with TNF, IL-17A selectively induces a specific set of genes mediated by factors including cut-like homeobox 1 (CUX1) and IκBζ (NFKBIZ). In the promoters of CXCL1, CXCL2, and CXCL3, we found a putative CUX1-NF-κB binding motif not found elsewhere in the genome. CUX1 and NF-κB p65 mediate transcription of these genes independent of LIFR, STAT3, STAT4, and ELF3. Transcription of NFKBIZ, encoding the atypical IκB factor IκBζ, is IL-17A dose-dependent, and IκBζ only mediates the transcriptional response to TNF and IL-17A, but not to TNF alone. In fibroblasts, IL-17A response depends on CUX1 and IκBζ to engage the NF-κB complex to produce chemoattractants for neutrophil and monocyte recruitment.

Keywords: RNA-seq; inflammation; regulation; time series; transcription.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Arthritis, Rheumatoid / genetics
  • Arthritis, Rheumatoid / metabolism*
  • Cells, Cultured
  • Chemokine CXCL1 / genetics
  • Chemokine CXCL2 / genetics
  • Chemokines, CXC / genetics
  • Chemotactic Factors / genetics
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism*
  • Interleukin-17 / pharmacology
  • Interleukin-17 / physiology*
  • Interleukin-6 / genetics
  • Matrix Metalloproteinase 3 / metabolism
  • Monocytes / drug effects
  • Monocytes / physiology
  • RNA, Small Interfering / genetics
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Stromal Cells / drug effects
  • Stromal Cells / metabolism
  • Synovial Fluid
  • Transcription Factor RelA / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcriptome / physiology*
  • Transcriptome / radiation effects
  • Tumor Necrosis Factor-alpha / pharmacology
  • Tumor Necrosis Factor-alpha / physiology*

Substances

  • Adaptor Proteins, Signal Transducing
  • CUX1 protein, human
  • CXCL1 protein, human
  • CXCL2 protein, human
  • CXCL3 protein, human
  • Chemokine CXCL1
  • Chemokine CXCL2
  • Chemokines, CXC
  • Chemotactic Factors
  • Homeodomain Proteins
  • IL6 protein, human
  • Interleukin-17
  • Interleukin-6
  • NFKBIZ protein, human
  • RELA protein, human
  • RNA, Small Interfering
  • Repressor Proteins
  • Transcription Factor RelA
  • Transcription Factors
  • Tumor Necrosis Factor-alpha
  • Matrix Metalloproteinase 3