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Streptococcus Gordonii Programs Epithelial Cells to Resist ZEB2 Induction by Porphyromonas Gingivalis

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Streptococcus Gordonii Programs Epithelial Cells to Resist ZEB2 Induction by Porphyromonas Gingivalis Streptococcus gordonii programs epithelial cells to resist ZEB2 induction by Porphyromonas gingivalis Jun Ohshimaa,1, Qian Wanga,1, Zackary R. Fitzsimondsa, Daniel P. Millera, Maryta N. Sztukowskaa,b, Young-Jung Junga,2, Mikako Hayashic, Marvin Whiteleyd,e, and Richard J. Lamonta,3 aDepartment of Oral Immunology and Infectious Diseases, University of Louisville School of Dentistry, Louisville, KY 40202; bUniversity of Information Technology and Management, 35-225 Rzeszow, Poland; cDepartment of Restorative Dentistry and Endodontology, Graduate School of Dentistry, Osaka University, 565-0871 Osaka, Japan; dSchool of Biological Sciences, Georgia Institute of Technology, Atlanta, GA 30332; and eEmory-Children’s Cystic Fibrosis Center, Atlanta, GA 30322 Edited by Lora V. Hooper, The University of Texas Southwestern, Dallas, TX, and approved March 15, 2019 (received for review January 3, 2019) The polymicrobial microbiome of the oral cavity is a direct precur- acquire a motile phenotype which can generate self-renewing sor of periodontal diseases, and changes in microhabitat or shifts tumor-initiating cells, and, in malignant tumors, it gives rise to in microbial composition may also be linked to oral squamous cell a population of migratory and invasive cancer cells (15). EMT is carcinoma. Dysbiotic oral epithelial responses provoked by indi- controlled by a group of transcription factors, including the zinc- vidual organisms, and which underlie these diseases, are widely finger E-box–binding homeobox proteins (ZEB1 and ZEB2), studied. However, organisms may influence community partner SNAI1/2, and TWIST1/2 (16, 17). We have found that P. gingi- species through manipulation of epithelial cell responses, an aspect valis can increase expression of ZEB1 in immortalized gingival of the host microbiome interaction that is poorly understood. We epithelial cells (11), and others have reported up-regulation of report here that Porphyromonas gingivalis, a keystone periodon- ZEB1 and SNAI1/2 following P. gingivalis challenge of primary tal pathogen, can up-regulate expression of ZEB2, a transcription cultures of gingival epithelial cells (12). In addition to EMT, factor which controls epithelial–mesenchymal transition and inflam- ZEB1/2, SNAI1/2, and TWIST1/2 also control inflammatory matory responses. ZEB2 regulation by P. gingivalis was mediated responses (18–20), which could provide a mechanistic conver- through pathways involving β-catenin and FOXO1. Among the com- gence between tumorigenic potential and periodontal diseases. munity partners of P. gingivalis, Streptococcus gordonii was capable Organisms that cocolonize the oral epithelium with P. gingivalis MICROBIOLOGY of antagonizing ZEB2 expression. Mechanistically, S. gordonii sup- include Fusobacterium nucleatum and oral streptococcal species of pressed FOXO1 by activating the TAK1-NLK negative regulatory the mitis group (21–23). These organisms can interact with each pathway, even in the presence of P. gingivalis. Collectively, these other in biofilms and can also modulate epithelial responses to results establish S. gordonii as homeostatic commensal, capable of partner species in mixed infections. For example, both P. gingivalis mitigating the activity of a more pathogenic organism through and streptococcal species can inhibit F. nucleatum-induced epithe- modulation of host signaling. lial IL-8 expression through blocking NF-κB nuclear translocation EMT | commensal | polymicrobial community | FOXO1 | periodontal Significance acterial colonizers of the skin and mucosal barriers tend to Many infections initiating at mucosal barriers involve poly- Borganize into polymicrobial communities. Disease can occur microbial communities of organisms within which there are when the homeostatic balance between these communities and often multiple mechanisms of polymicrobial synergy and an- the host is disrupted, resulting in dysbiosis. The interbacterial tagonism. However, we still understand little about another and bacteria–host interactions that dictate homeostasis or dysbiosis fundamental aspect of polymicrobial infection: that is, how the are, therefore, a subject of intense scrutiny. In the oral cavity, dys- interaction of one organism with host cells can modulate the biotic microbial communities in the gingival compartment can in- properties of another organism. We examined this topic using duce periodontal disease, which is the sixth most common infectious a model two-species microbial community and oral epithelial condition worldwide (1–5). Subgingival communities provoke a cells. The results show that Streptococcus gordonii can redirect poorly controlled immune response which fails to eliminate the signal transduction pathways within epithelial cells that would microbial challenge and eventually leads to tissue destruction (2). otherwise be induced by the keystone pathogen Porphyr- Polymicrobial synergistic interactions among community inhabitants omonas gingivalis and which converge on a proinflammatory, raise the community pathogenic potential, or nososymbiocity; and mesenchymal-like transcriptional program. These observations species such as Porphyromonas gingivalis that can effect the transi- represent a mechanism by which commensals can maintain tion of a commensal community to a pathogenic entity, even at low homeostasis in the presence of more pathogenic organisms. abundance, are known as keystone pathogens (6). Increasing epi- Author contributions: M.H., M.W., and R.J.L. designed research; J.O., Q.W., Z.R.F., D.P.M., demiological and mechanistic evidence also implicates the oral M.N.S., and Y.-J.J. performed research; J.O., Q.W., Z.R.F., D.P.M., and R.J.L. analyzed data; microbiota in cancers such as oral squamous cell carcinoma (OSCC) and J.O., Q.W., Z.R.F., D.P.M., M.N.S., Y.-J.J., M.H., M.W., and R.J.L. wrote the paper. (7, 8). Periodontal organisms can contribute to a tumorigenic en- The authors declare no conflict of interest. vironment by subverting epithelial cell pathways to reduce apoptosis This article is a PNAS Direct Submission. and increase cell cycle progression, and also by disruption of local Published under the PNAS license. – inflammatory responses (7 10). Data deposition: Microscopy files are available in the BioStudies database (www.ebi.ac. Characterization of the epithelial cell responses to the oral uk/biostudies) under accession no. S-BSST247. – microbiota is imperative for understanding the host microbe 1J.O. and Q.W. contributed equally to this work. interface that dictates the dysbiotic potential underlying peri- 2Present address: Department of Oral Microbiology and Immunology, School of Dentistry, odontal diseases and potentially OSCC. In addition to its role as Seoul National University, Seoul 08826, Republic of Korea. a keystone periodontal pathogen, P. gingivalis has also been 3To whom correspondence should be addressed. Email: [email protected]. shown to increase the mesenchymal properties of epithelial cells This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. (11–14). The epithelial–mesenchymal transition (EMT) is an 1073/pnas.1900101116/-/DCSupplemental. orchestrated process by which epithelial cells change shape and www.pnas.org/cgi/doi/10.1073/pnas.1900101116 PNAS Latest Articles | 1of10 Downloaded by guest on September 25, 2021 (24, 25). Moreover, Streptococcus gordonii can reprogram epithelial of under twofold only observed for TWIST1 at 24 and 48 h at an cell global transcriptional patterns such that the subsequent re- MOI of 100 (Fig. 1B). To corroborate the quantitative reverse sponse to P. gingivalis is diminished (26), and S. gordonii can prevent transcription-PCR (qRT-PCR) data and begin to test functional P. gingivalis-induced gingival epithelial cell (GEC) proliferation (26). relevance, the expression and location of ZEB2 protein were ex- The mechanistic details of the influence of S. gordonii on epithelial amined. P. gingivalis challenge increased both the amount of cell transcriptional responses has yet to be addressed. ZEB2 protein expression and localization in the nucleus where it In this study, we focus on the ZEB2 transcription factor and is functionally active (Fig. 1C). show that expression of ZEB2 is induced specifically by P. gin- P. gingivalis is a host adapted organism with a nonclonal givalis through pathways involving β-catenin and FOXO1. While population structure, and isolates from different individuals can neither S. gordonii nor F. nucleatum regulated ZEB2, S. gordonii vary extensively (27–29). Hence, we next examined the ability of antagonized ZEB2 induction by P. gingivalis through blocking different strains of P. gingivalis to enhance ZEB2 mRNA levels. the dephosphorylation and activation of FOXO1. The results As shown in Fig. 1D, the commonly used laboratory strain W83, position S. gordonii as a homeostatic commensal which operates along with the low passage clinical isolate MP4-504, induced via host cell manipulation to mitigate the action of a pathogen. ZEB2 expression to a similar degree as did 33277. The property of ZEB2 induction by P. gingivalis thus spans both fimbriated/ Results nonencapsulated (33277) and nonfimbriated/capsulated (W83) Regulation of EMT-Inducing Transcription Factors by P. gingivalis lineages. Regulation of ZEB2 by W83 contrasts to ZEB1, which Alone and in Dual Species Conglomerates. P. gingivalis has been is not induced by W83 (11), indicating that differential pathways shown to induce a partial or transition EMT phenotype in gin-
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