IL-1β promotes corneal epithelial cell migration by increasing MMP-9 expression through NF-κB- and AP-1-dependent pathways

PLoS One. 2013;8(3):e57955. doi: 10.1371/journal.pone.0057955. Epub 2013 Mar 7.

Abstract

Interleukin-1β (IL-1β) plays a critical mediator in the pathogenesis of eye diseases. The implication of IL-1β in inflammatory responses has been shown to be mediated through up-regulation of inflammatory genes, including matrix metalloproteinase-9 (MMP-9). However, the detailed mechanisms of IL-1β-induced MMP-9 expression in Statens Seruminstitut Rabbit Corneal Cells (SIRCs) are largely unclear. Here, we demonstrated that in SIRCs, IL-1β induced MMP-9 promoter activity and mRNA expression associated with an increase in the secretion of pro-MMP-9. IL-1β-induced pro-MMP-9 expression and MMP-9 mRNA levels were attenuated by pretreatment with the inhibitor of MEK1/2 (U0126), JNK1/2 (SP600125), NF-κB (Bay11-7082), or AP-1 (Tanshinone IIA) and transfection with siRNA of p42 or JNK2. Moreover, IL-1β markedly stimulated p42/p44 MAPK and JNK1/2 phosphorylation in SIRCs. In addition, IL-1β also enhanced p42/p44 MAPK translocation from the cytosol into the nucleus. On the other hand, IL-1β induced c-Jun and c-Fos mRNA expression, c-Jun phosphorylation, and AP-1 promoter activity. NF-κB translocation, IκBα degradation, and NF-κB promoter activity were also enhanced by IL-1β. Pretreatment with U0126 or SP600125 inhibited IL-1β-induced AP-1 and NF-κB promoter activity, but not NF-κB translocation from the cytosol into the nucleus. Finally, we established that IL-1β could stimulate SIRCs migration via p42/p44 MAPK-, JNK1/2-, AP-1-, and NF-κB-dependent MMP-9 induction. These results suggested that NF-κB and AP-1 activated by JNK1/2 and p42/p44 MAPK cascade are involved in IL-1β-induced MMP-9 expression in SIRCs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Movement / drug effects
  • Cell Movement / genetics
  • Epithelial Cells / metabolism*
  • Epithelium, Corneal / metabolism*
  • Gene Expression Regulation / drug effects
  • Interleukin-1beta / pharmacology*
  • Matrix Metalloproteinase 9 / genetics*
  • Matrix Metalloproteinase 9 / metabolism
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mitogen-Activated Protein Kinase 8 / metabolism
  • Mitogen-Activated Protein Kinase 9 / metabolism
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Promoter Regions, Genetic
  • Rabbits
  • Signal Transduction*
  • Transcription Factor AP-1 / genetics
  • Transcription Factor AP-1 / metabolism*
  • Transcriptional Activation / drug effects

Substances

  • Interleukin-1beta
  • NF-kappa B
  • Transcription Factor AP-1
  • Mitogen-Activated Protein Kinase 9
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinase 8
  • Matrix Metalloproteinase 9

Grants and funding

This work was supported by NSC101-2314-B-182A-112, NSC98-2321-B-182-004, NSC99-2321-B-182-003, NSC98-2320-B-182-004-MY3, and NSC98-2314-B-182-021-MY3, from National Science Council, Taiwan; EMRPD1B0311, and EMRPD1B0321 from Ministry of Education, Taiwan; and CMRPG391032, CMRPG381522, CMRPD170493, CMRPD180373, CMRPD1A0151, CMRPD1B0381, and CMRPG3B1091 from Chang Gung Medical Research Foundation, Taiwan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of manuscript.