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Chlamydia Pneumoniae Is Present in the Dental Plaque of Periodontitis

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Chlamydia Pneumoniae Is Present in the Dental Plaque of Periodontitis University of the Pacific Scholarly Commons Dugoni School of Dentistry Faculty Articles Arthur A. Dugoni School of Dentistry 3-11-2019 Chlamydia pneumoniae is present in the dental plaque of periodontitis patients and stimulates an inflammatory response in gingival epithelial cells Cássio Luiz Coutinho Almeida-da-Silva Tamer Alpagot Ye Zhu Sonho Sierra Lee Brian P Roberts See next page for additional authors Follow this and additional works at: https://scholarlycommons.pacific.edu/dugoni-facarticles Part of the Dentistry Commons Recommended Citation Almeida-da-Silva, C., Alpagot, T., Zhu, Y., Lee, S., Roberts, B., Hung, S., Tang, N., & Ojcius, D. (2019). Chlamydia pneumoniae is present in the dental plaque of periodontitis patients and stimulates an inflammatory response in gingival epithelial cells. Microbial Cell, 6(4), 197–208. DOI: 10.15698/mic2019.04.674 https://scholarlycommons.pacific.edu/dugoni-facarticles/459 This Article is brought to you for free and open access by the Arthur A. Dugoni School of Dentistry at Scholarly Commons. It has been accepted for inclusion in Dugoni School of Dentistry Faculty Articles by an authorized administrator of Scholarly Commons. For more information, please contact [email protected]. Authors Cássio Luiz Coutinho Almeida-da-Silva, Tamer Alpagot, Ye Zhu, Sonho Sierra Lee, Brian P Roberts, Shu- Chen Hung, Norina Tang, and David M Ojcius This article is available at Scholarly Commons: https://scholarlycommons.pacific.edu/dugoni-facarticles/459 Research Article www.microbialcell.com Chlamydia pneumoniae is present in the dental plaque of periodontitis patients and stimulates an inflammatory response in gingival epithelial cells Cássio Luiz Coutinho Almeida-da-Silva1, Tamer Alpagot2, Ye Zhu1, Sonho Sierra Lee3,4, Brian P. Roberts5, Shu-Chen Hung1, Norina Tang1,2 and David M. Ojcius1,* 1 Department of Biomedical Sciences, Arthur A. Dugoni School of Dentistry, University of the Pacific, San Francisco, CA 94103, USA. 2 Department of Periodontics, Arthur A. Dugoni School of Dentistry, University of the Pacific, San Francisco, CA 94103, USA. 3 College of Letters and Science, University of California, Berkeley, CA 94720, USA. 4 Program of Doctor of Dental Surgery, Arthur A. Dugoni School of Dentistry, University of the Pacific, San Francisco, CA 94103, USA. 5 College of Letters and Science, University of California, Los Angeles, CA 90095, USA. * Corresponding Author: David M. Ojcius, Department of Biomedical Sciences, University of the Pacific, Arthur A. Dugoni School of Dentistry, 155 Fifth Street, San Francisco, CA 94103, USA; E-mail: [email protected] ABSTRACT Chlamydia pneumoniae is an airborne, Gram-negative, obligate doi: 10.15698/mic2019.04.674 intracellular bacterium which causes human respiratory infections and has Received originally: 01.08.2018; been associated with atherosclerosis. Because individuals with periodontitis in revised form: 03.02.2019, Accepted 25.02.2019, are at greater risk for atherosclerosis as well as respiratory infections, we in- Published 11.03.2019. vestigated the role of C. pneumoniae in inflammation and periodontal dis- ease. We found that C. pneumoniae was more frequently found in subgingival dental plaque obtained from periodontally diseased sites of the mouth versus Keywords: Chlamydia, healthy sites. The known periodontal pathogens, Porphyromonas gingivalis inflammasome, periodontitis, and Aggregatibacter actinomycetemcomitans, were also found in the plaque. inflammation, caspase-1. In addition, C. pneumoniae could efficiently invade human gingival epithelial cells (GECs) in vitro, causing translocation of NF-κB to the nucleus along with Abbreviations: increased secretion of mature IL-1β cytokine. Supernatants collected from C. EB – elementary body, pneumoniae-infected GECs showed increased activation of caspase-1 protein, GEC – gingival epithelial cell, which was significantly reduced when nlrp3 gene expression was silenced MOI – multiplicities of infection, NLR – NOD-like receptor, using shRNA lentiviral vectors. Our results demonstrate that C. pneumoniae RB – reticulate body. was found in higher levels in periodontitis patients compared to control pa- tients. Additionally, C. pneumoniae could infect GECs, leading to inflammation caused by activation of NF-κB and the NLRP3 inflammasome. We propose that the presence of C. pneumoniae in subgingival dental plaque may contribute to periodontal disease and could be used as a potential risk indicator of perio- dontal disease. INTRODUCTION species of bacteria are present in the human oral microbi- Periodontitis is the most common oral inflammatory dis- ome, only about ten have been identified as putative path- ease [1]. It involves inflammation and destruction of the ogens causing periodontal disease [2]. These putative attachment apparatus of the teeth (i.e., gingiva, periodon- pathogens are mainly Gram-negative anaerobic bacteria tal ligament, root cementum and alveolar bone). Periodon- and include Aggregatibacter actinomycetemcomitans, Por- titis begins with an infection of the gingival tissue by etio- phyromonas gingivalis, Porphyromonas intermedia, Bac- logic agents. Bacterial invasion of the gingiva elicits a host teroides forsythus, Campylobacter rectus, Eubacterium immune response which begins with inflammation of the nodatum, Porphyromonas micros, Staphylococcus interme- gingiva, progressing to destruction of deep periodontal dius and Treponema spp. [3]. Of these ten species, tissues and loss of alveolar bone. Even though over 600 OPEN ACCESS | www.microbialcell.com 197 Microbial Cell | APRIL 2019 | Vol. 6 No. 4 C.L.C. Almeida-da-Silva et al. (2019) Chlamydia pneumoniae in periodontitis patients A. actinomycetemcomitans, P. gingivalis and B. forsythus C. pneumoniae has not been traditionally considered a are most commonly associated with periodontitis [4-6]. member of the human oral microbiome and was not Chlamydiae are obligate, intracellular bacteria that thought to infect oral cells [2, 19, 20]. However, Rizzo et al. have a biphasic developmental cycle [7-9]. In the early reported infecting human gingival fibroblasts in vitro and stages, infectious forms called elementary bodies (EBs) eliciting secretion of the cytokines, interleukin-6 and inter- enter mucosal cells and reside in membrane-bound vacu- leukin-10 [21, 22]. In another study, C. pneumoniae was oles called inclusions. Within a few hours, the EBs differen- found in the gingival crevicular fluid of one periodontitis tiate into larger, metabolically active reticulate bodies patient with characteristics similar to a clinical strain [23]. (RBs) which are non-infectious. After several rounds of Moreover, a characterization of subgingival dental plaque replication, RBs differentiate back into EBs and are re- revealed that C. pneumoniae was present in one out of leased from the host cell, ready to infect neighboring cells. twelve clinical samples obtained from periodontitis pa- The cells infected by Chlamydia include epithelial cells, tients [24]. Unfortunately, in these studies, the clinical smooth muscle cells, fibroblasts, osteoblasts, mono- sample sizes were small and no comparisons to healthy cytes/macrophages and dendritic cells [10-13]. These sus- patient controls were made. In addition, no demonstration ceptible host cells recognize chlamydial antigens by several had been made that C. pneumoniae can invade the oral means: through cell surface receptors, endosomal recep- epithelium, one of the first and major barriers to oral dis- tors, and cytosolic innate immune sensors [10]. Activation ease. Currently, it is still not known whether C. pneumoni- of these receptors leads to the release of pro-inflammatory ae infects gingival epithelium and subsequently promotes a cytokines and chemokines which recruit inflammatory cells host-mediated immune response that leads to periodonti- to eliminate the infectious agent. Under immunopathologic tis. conditions, such as with chronic immune activation, these In this study, using 80 dental plaque samples, we ex- events can lead to tissue damage and scarring. amined whether C. pneumoniae can be found in subgingi- The two major chlamydial species that are pathogenic val dental plaque and whether its presence correlated with to humans are Chlamydia trachomatis and Chlamydia periodontal disease. In addition, we examined the ability of pneumoniae [14]. Infection with C. trachomatis can lead to C. pneumoniae to invade gingival epithelial cells and elicit a non-congenital blindness and genital tract infections and host inflammatory response. complications such as pelvic inflammatory disease, infertili- ty, ectopic pregnancy, urethritis and cervical cancer. RESULTS C. pneumoniae causes respiratory infections including C. pneumoniae is more frequent in subgingival plaque pneumonia, bronchitis, pharyngitis and sinusitis. Approxi- from patients with periodontal disease than in healthy mately 10% of community-acquired pneumonia cases are controls caused by C. pneumoniae infection [15]. C. pneumoniae has Eighty subgingival dental plaque samples were obtained also been linked to asthma, arthritis, atherosclerosis, from 20 subjects with and without periodontal disease. In stroke, multiple sclerosis and Alzheimer’s disease [12, 15- the healthy group, subgingival plaque samples were ob- 18]. Chlamydial infections are treatable with antibiotics, tained from four periodontally “healthy sites”. In patients but no vaccines are available for prevention. with periodontitis, subgingival plaque samples were ob- TABLE
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