Multi-species oral biofilm promotes reconstructed human gingiva epithelial barrier function

Lin Shang, Dongmei Deng, Jeroen Kees Buskermolen, Marleen Marga Janus, Bastiaan Philip Krom, Sanne Roffel, Taco Waaijman, Cor van Loveren, Wim Crielaard, Susan Gibbs

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Since the oral mucosa is continuously exposed to abundant microbes, one of its most important defense features is a highly proliferative, thick, stratified epithelium. The cellular mechanisms responsible for this are still unknown. The aim of this study was to determine whether multi-species oral biofilm contribute to the extensive stratification and primed antimicrobial defense in epithelium. Two in vitro models were used: 3D reconstructed human gingiva (RHG) and oral bacteria representative of multi-species commensal biofilm. The organotypic RHG consists of a reconstructed stratified gingiva epithelium on a gingiva fibroblast populated hydrogel (lamina propria). Biofilm was cultured from healthy human saliva, and consists of typical commensal genera Granulicatella and major oral microbiota genera Veillonella and Streptococcus. Biofilm was applied topically to RHG and host-microbiome interactions were studied over 7 days. Compared to unexposed RHG, biofilm exposed RHG showed increased epithelial thickness, more organized stratification and increased keratinocyte proliferation. Furthermore biofilm exposure increased production of RHG anti-microbial proteins Elafin, HBD2 and HBD3 but not HBD1, adrenomedullin or cathelicidin LL-37. Inflammatory and antimicrobial cytokine secretion (IL-6, CXCL8, CXCL1, CCL20) showed an immediate and sustained increase. In conclusion, exposure of RHG to commensal oral biofilm actively contributes to RHG epithelial barrier function.

Original languageEnglish
JournalScientific Reports
Volume8
Issue number1
DOIs
Publication statusPublished - 30 Oct 2018

Cite this

Shang, Lin ; Deng, Dongmei ; Buskermolen, Jeroen Kees ; Janus, Marleen Marga ; Krom, Bastiaan Philip ; Roffel, Sanne ; Waaijman, Taco ; van Loveren, Cor ; Crielaard, Wim ; Gibbs, Susan. / Multi-species oral biofilm promotes reconstructed human gingiva epithelial barrier function. In: Scientific Reports. 2018 ; Vol. 8, No. 1.
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title = "Multi-species oral biofilm promotes reconstructed human gingiva epithelial barrier function",
abstract = "Since the oral mucosa is continuously exposed to abundant microbes, one of its most important defense features is a highly proliferative, thick, stratified epithelium. The cellular mechanisms responsible for this are still unknown. The aim of this study was to determine whether multi-species oral biofilm contribute to the extensive stratification and primed antimicrobial defense in epithelium. Two in vitro models were used: 3D reconstructed human gingiva (RHG) and oral bacteria representative of multi-species commensal biofilm. The organotypic RHG consists of a reconstructed stratified gingiva epithelium on a gingiva fibroblast populated hydrogel (lamina propria). Biofilm was cultured from healthy human saliva, and consists of typical commensal genera Granulicatella and major oral microbiota genera Veillonella and Streptococcus. Biofilm was applied topically to RHG and host-microbiome interactions were studied over 7 days. Compared to unexposed RHG, biofilm exposed RHG showed increased epithelial thickness, more organized stratification and increased keratinocyte proliferation. Furthermore biofilm exposure increased production of RHG anti-microbial proteins Elafin, HBD2 and HBD3 but not HBD1, adrenomedullin or cathelicidin LL-37. Inflammatory and antimicrobial cytokine secretion (IL-6, CXCL8, CXCL1, CCL20) showed an immediate and sustained increase. In conclusion, exposure of RHG to commensal oral biofilm actively contributes to RHG epithelial barrier function.",
author = "Lin Shang and Dongmei Deng and Buskermolen, {Jeroen Kees} and Janus, {Marleen Marga} and Krom, {Bastiaan Philip} and Sanne Roffel and Taco Waaijman and {van Loveren}, Cor and Wim Crielaard and Susan Gibbs",
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Shang, L, Deng, D, Buskermolen, JK, Janus, MM, Krom, BP, Roffel, S, Waaijman, T, van Loveren, C, Crielaard, W & Gibbs, S 2018, 'Multi-species oral biofilm promotes reconstructed human gingiva epithelial barrier function' Scientific Reports, vol. 8, no. 1. https://doi.org/10.1038/s41598-018-34390-y

Multi-species oral biofilm promotes reconstructed human gingiva epithelial barrier function. / Shang, Lin; Deng, Dongmei; Buskermolen, Jeroen Kees; Janus, Marleen Marga; Krom, Bastiaan Philip; Roffel, Sanne; Waaijman, Taco; van Loveren, Cor; Crielaard, Wim; Gibbs, Susan.

In: Scientific Reports, Vol. 8, No. 1, 30.10.2018.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Deng, Dongmei

AU - Buskermolen, Jeroen Kees

AU - Janus, Marleen Marga

AU - Krom, Bastiaan Philip

AU - Roffel, Sanne

AU - Waaijman, Taco

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AU - Crielaard, Wim

AU - Gibbs, Susan

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N2 - Since the oral mucosa is continuously exposed to abundant microbes, one of its most important defense features is a highly proliferative, thick, stratified epithelium. The cellular mechanisms responsible for this are still unknown. The aim of this study was to determine whether multi-species oral biofilm contribute to the extensive stratification and primed antimicrobial defense in epithelium. Two in vitro models were used: 3D reconstructed human gingiva (RHG) and oral bacteria representative of multi-species commensal biofilm. The organotypic RHG consists of a reconstructed stratified gingiva epithelium on a gingiva fibroblast populated hydrogel (lamina propria). Biofilm was cultured from healthy human saliva, and consists of typical commensal genera Granulicatella and major oral microbiota genera Veillonella and Streptococcus. Biofilm was applied topically to RHG and host-microbiome interactions were studied over 7 days. Compared to unexposed RHG, biofilm exposed RHG showed increased epithelial thickness, more organized stratification and increased keratinocyte proliferation. Furthermore biofilm exposure increased production of RHG anti-microbial proteins Elafin, HBD2 and HBD3 but not HBD1, adrenomedullin or cathelicidin LL-37. Inflammatory and antimicrobial cytokine secretion (IL-6, CXCL8, CXCL1, CCL20) showed an immediate and sustained increase. In conclusion, exposure of RHG to commensal oral biofilm actively contributes to RHG epithelial barrier function.

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JO - Scientific Reports

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SN - 2045-2322

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