Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms
Polymicrobial interactions with oral mucosal surfaces determine the health status of the host. While a homeostatic balance provides protection from oral disease, a dysbiotic polymicrobial community promotes tissue destruction and chronic oral diseases. How polymicrobial communities transition from a...
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doaj-43995369947a4eabb4941e46655def1f2021-07-01T18:12:34ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-07-011110.3389/fcimb.2021.686479686479Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies BiofilmsUlrike Redanz0Sylvio Redanz1Sylvio Redanz2Puthalayai Treerat3Sivaraman Prakasam4Li-Jung Lin5Justin Merritt6Justin Merritt7Jens Kreth8Jens Kreth9Department of Restorative Dentistry, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Restorative Dentistry, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Translational Rheumatology and Immunology, Institute for Musculoskeletal Medicine, University of Münster, Münster, GermanyDepartment of Restorative Dentistry, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Periodontology, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Translational Rheumatology and Immunology, Institute for Musculoskeletal Medicine, University of Münster, Münster, GermanyDepartment of Restorative Dentistry, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Molecular Microbiology and Immunology, School of Medicine, Oregon Health & Science University, Portland, OR, United StatesDepartment of Restorative Dentistry, School of Dentistry, Oregon Health & Science University, Portland, OR, United StatesDepartment of Molecular Microbiology and Immunology, School of Medicine, Oregon Health & Science University, Portland, OR, United StatesPolymicrobial interactions with oral mucosal surfaces determine the health status of the host. While a homeostatic balance provides protection from oral disease, a dysbiotic polymicrobial community promotes tissue destruction and chronic oral diseases. How polymicrobial communities transition from a homeostatic to a dysbiotic state is an understudied process. Thus, we were interested to investigate this ecological transition by focusing on biofilm communities containing high abundance commensal species and low abundance pathobionts to characterize the host-microbiome interactions occurring during oral health. To this end, a multispecies biofilm model was examined using the commensal species Corynebacterium durum and Streptococcus sanguinis and the pathobiont Porphyromonas gingivalis. We compared how both single and multispecies biofilms interact with different oral mucosal and gingival cell types, including the well-studied oral keratinocyte cell lines OKF4/TERT-1and hTERT TIGKs as well as human primary periodontal ligament cells. While single species biofilms of C. durum, S. sanguinis, and P. gingivalis are all characterized by unique cytokine responses for each species, multispecies biofilms elicited a response resembling S. sanguinis single species biofilms. One notable exception is the influence of P. gingivalis upon TNF-α and Gro-α production in hTERT TIGKs cells, which was not affected by the presence of other species. This study is also the first to examine the host response to C. durum. Interestingly, C. durum yielded no notable inflammatory responses from any of the tested host cells, suggesting it functions as a true commensal species. Conversely, S. sanguinis was able to induce expression and secretion of the proinflammatory cytokines IL-6 and IL-8, demonstrating a much greater inflammatory potential, despite being health associated. Our study also demonstrates the variability of host cell responses between different cell lines, highlighting the importance of developing relevant in vitro models to study oral microbiome-host interactions.https://www.frontiersin.org/articles/10.3389/fcimb.2021.686479/fulloral biofilmimmune responseStreptococcusCorynebacteriumcytokine |
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DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ulrike Redanz Sylvio Redanz Sylvio Redanz Puthalayai Treerat Sivaraman Prakasam Li-Jung Lin Justin Merritt Justin Merritt Jens Kreth Jens Kreth |
spellingShingle |
Ulrike Redanz Sylvio Redanz Sylvio Redanz Puthalayai Treerat Sivaraman Prakasam Li-Jung Lin Justin Merritt Justin Merritt Jens Kreth Jens Kreth Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms Frontiers in Cellular and Infection Microbiology oral biofilm immune response Streptococcus Corynebacterium cytokine |
author_facet |
Ulrike Redanz Sylvio Redanz Sylvio Redanz Puthalayai Treerat Sivaraman Prakasam Li-Jung Lin Justin Merritt Justin Merritt Jens Kreth Jens Kreth |
author_sort |
Ulrike Redanz |
title |
Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms |
title_short |
Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms |
title_full |
Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms |
title_fullStr |
Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms |
title_full_unstemmed |
Differential Response of Oral Mucosal and Gingival Cells to Corynebacterium durum, Streptococcus sanguinis, and Porphyromonas gingivalis Multispecies Biofilms |
title_sort |
differential response of oral mucosal and gingival cells to corynebacterium durum, streptococcus sanguinis, and porphyromonas gingivalis multispecies biofilms |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cellular and Infection Microbiology |
issn |
2235-2988 |
publishDate |
2021-07-01 |
description |
Polymicrobial interactions with oral mucosal surfaces determine the health status of the host. While a homeostatic balance provides protection from oral disease, a dysbiotic polymicrobial community promotes tissue destruction and chronic oral diseases. How polymicrobial communities transition from a homeostatic to a dysbiotic state is an understudied process. Thus, we were interested to investigate this ecological transition by focusing on biofilm communities containing high abundance commensal species and low abundance pathobionts to characterize the host-microbiome interactions occurring during oral health. To this end, a multispecies biofilm model was examined using the commensal species Corynebacterium durum and Streptococcus sanguinis and the pathobiont Porphyromonas gingivalis. We compared how both single and multispecies biofilms interact with different oral mucosal and gingival cell types, including the well-studied oral keratinocyte cell lines OKF4/TERT-1and hTERT TIGKs as well as human primary periodontal ligament cells. While single species biofilms of C. durum, S. sanguinis, and P. gingivalis are all characterized by unique cytokine responses for each species, multispecies biofilms elicited a response resembling S. sanguinis single species biofilms. One notable exception is the influence of P. gingivalis upon TNF-α and Gro-α production in hTERT TIGKs cells, which was not affected by the presence of other species. This study is also the first to examine the host response to C. durum. Interestingly, C. durum yielded no notable inflammatory responses from any of the tested host cells, suggesting it functions as a true commensal species. Conversely, S. sanguinis was able to induce expression and secretion of the proinflammatory cytokines IL-6 and IL-8, demonstrating a much greater inflammatory potential, despite being health associated. Our study also demonstrates the variability of host cell responses between different cell lines, highlighting the importance of developing relevant in vitro models to study oral microbiome-host interactions. |
topic |
oral biofilm immune response Streptococcus Corynebacterium cytokine |
url |
https://www.frontiersin.org/articles/10.3389/fcimb.2021.686479/full |
work_keys_str_mv |
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