Regulation of gingival keratinocyte monocyte chemoattractant protein-1-induced protein (MCPIP)-1 and mucosa-associated lymphoid tissue lymphoma translocation protein (MALT)-1 expressions by periodontal bacteria, lipopolysaccharide, and interleukin-1β

J Periodontol. 2023 Jan;94(1):130-140. doi: 10.1002/JPER.22-0093. Epub 2022 Aug 4.

Abstract

Background: The aim of this study was to evaluate oral bacteria- and interleukin (IL)-1β-induced protein and mRNA expression profiles of monocyte chemoattractant protein-1-induced protein (MCPIP)-1 and mucosa-associated lymphoid tissue lymphoma translocation protein (MALT)-1 in human gingival keratinocyte monolayers and organotypic oral mucosal models.

Methods: Human gingival keratinocyte (HMK) monolayers were incubated with Porphyromonas gingivalis, Fusobacterium nucleatum, P. gingivalis lipopolysaccharide (LPS) and IL-1β. The protein levels of MCPIP-1 and MALT-1 were examined by immunoblots and mRNA levels by qPCR. MCPIP-1 and MALT-1 protein expression levels were also analyzed immunohistochemically using an organotypic oral mucosal model. One-way analysis of variance followed by Tukey correction was used in statistical analyses.

Results: In keratinocyte monolayers, MCPIP-1 protein expression was suppressed by F. nucleatum and MALT-1 protein expression was suppressed by F. nucleatum, P. gingivalis LPS and IL-1β. P. gingivalis seemed to degrade MCPIP-1 and MALT-1 at all tested time points and degradation was inhibited when P. gingivalis was heat-killed. MCPIP-1 mRNA levels were increased by P. gingivalis, F. nucleatum, and IL-1β, however, no changes were observed in MALT-1 mRNA levels.

Conclusion: Gingival keratinocyte MCPIP-1 and MALT-1 mRNA and protein expression responses are regulated by infection and inflammatory mediators. These findings suggest that periodontitis-associated bacteria-induced modifications in MCPIP-1 and MALT-1 responses can be a part of periodontal disease pathogenesis.

Keywords: infections; inflammation; periodontal diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chemokine CCL2 / metabolism
  • Fusobacterium nucleatum / physiology
  • Gingiva / metabolism
  • Humans
  • Interleukin-1beta / metabolism
  • Keratinocytes / metabolism
  • Lipopolysaccharides* / metabolism
  • Lipopolysaccharides* / pharmacology
  • Lymphoma, B-Cell, Marginal Zone* / metabolism
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / metabolism
  • Porphyromonas gingivalis / metabolism
  • RNA, Messenger / metabolism

Substances

  • Interleukin-1beta
  • Lipopolysaccharides
  • Chemokine CCL2
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein
  • RNA, Messenger