Oral Biofilms from Symbiotic to Pathogenic Interactions and Associated Disease –Connection of Periodontitis and Rheumatic Arthritis by Peptidylarginine Deiminase

Kriebel, Katja; Hieke, Cathleen; Müller-Hilke, Brigitte; Nakata, Masanobu; Kreikemeyer, Bernd

doi:10.3389/fmicb.2018.00053

Cited by 118Oral microbiology and periodontitis researchBacterial biofilms and quorum sensingOral Health Pathology and Treatment

Oral Biofilms from Symbiotic to Pathogenic Interactions and Associated Disease –Connection of Periodontitis and Rheumatic Arthritis by Peptidylarginine Deiminase

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Kriebel, Katja, Hieke, Cathleen, Müller-Hilke, Brigitte, Nakata, Masanobu, Kreikemeyer, Bernd·2018·Frontiers in Microbiology

DOI 10.3389/fmicb.2018.00053PMC PMC5797574

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Abstract

A wide range of bacterial species are harbored in the oral cavity, with the resulting complex network of interactions between the microbiome and host contributing to physiological as well as pathological conditions at both local and systemic levels. Bacterial communities inhabit the oral cavity as primary niches in a symbiotic manner and form dental biofilm in a stepwise process. However, excessive formation of biofilm in combination with a corresponding deregulated immune response leads to intra-oral diseases, such as dental caries, gingivitis, and periodontitis. Moreover, oral commensal bacteria, which are classified as so-called “pathobionts” according to a now widely accepted terminology, were recently shown to be present in extra-oral lesions with distinct bacterial species found to be involved in the onset of various pathophysiological conditions, including cancer, atherosclerosis, chronic infective endocarditis, and rheumatoid arthritis. The present review focuses on oral pathobionts as commensal and healthy members of oral biofilms that can turn into initiators of disease. We will shed light on the processes involved in dental biofilm formation and also provide an overview of the interactions of P. gingivalis, as one of the most prominent oral pathobionts, with host cells, including epithelial cells, phagocytes, and dental stem cells present in dental tissues. Notably, a previously unknown interaction of P. gingivalis bacteria with human stem cells that has impact on human immune response is discussed. In addition to this very specific interaction, the present review summarizes current knowledge regarding the immunomodulatory effect of P. gingivalis and other oral pathobionts, members of the oral microbiome, that pave the way for systemic and chronic diseases, thereby showing a link between periodontitis and rheumatoid arthritis.

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Dental plaque matrices create unique microenvironments that harbor acidic and anaerobic microenvironments, and thus select for organisms distinct from those growing directly on the tooth surface.
“These complex dental plaque matrices create unique microenvironments that harbor acidic and anaerobic microenvironments, and thus select for organisms distinct from those growing directly on the tooth surface.21”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [21]
Early inflammatory processes, such as gingivitis, can be mitigated through oral hygiene and removal of the bacterial biofilm.
“Early inflammatory processes, such as gingivitis, can be mitigated through oral hygiene and removal of the bacterial biofilm.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [21]
Inflammatory and immune-mediated processes, directly instigated by the microbes in the local plaque environment, mediate the development of gingivitis and periodontal disease.
“Inflammatory and immune‐mediated processes, directly instigated by the microbes in the local plaque environment, mediate the development of gingivitis and periodontal disease.21”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [21]
Stable plaque, which can also acquire opportunistic pathogens, can cause long-term inflammation that leads to periodontal disease.
“Stable plaque, which can also acquire opportunistic pathogens, can cause long‐term inflammation that leads to periodontal disease.21”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [21]

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Anaerobic Co-Culture of Mesenchymal Stem Cells and Anaerobic Pathogens - A New In Vitro Model System
Kriebel, K., Biedermann, A., Kreikemeyer, B., & Lang, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078226 · Cited by 26 · see citing works
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Gingival fibroblast responsiveness is differentially affected by P orphyromonas gingivalis: implications for the pathogenesis of periodontitis
Scheres, N., & Wim Crielaard, A. (2012) · Molecular Oral Microbiology · doi:10.1111/omi.12016 · Cited by 26 · see citing works
Stimulatory response of neutrophils from periodontitis patients with periodontal pathogens
Restaíno, C., Chaparro, A. P., Valenzuela, M., Kettlun, A. M., Vernal, R., Silva, A. D. N., Puente, J., Jaque, M., León, R., & Gamonal, J. A. (2007) · Oral Diseases · doi:10.1111/j.1601-0825.2006.01323.x · Cited by 26 · see citing works
Role ofPorphyromonas gingivalisHmuY in Immunopathogenesis of Chronic Periodontitis
de Carvalho-Filho, P. C., Gomes‐Filho, I. S., Meyer, R., Olczak, T., Xavier, M. T., & Trindade, S. C. (2016) · Mediators of Inflammation · doi:10.1155/2016/7465852 · Cited by 26 · see citing works
Modulation of stromal cell-derived factor 1 alpha (SDF-1α) and its receptor CXCR4 in Porphyromonas gingivalis-induced periodontal inflammation
Sun, J., Nemoto, E., Hong, G., & Sasaki, K. (2016) · BMC Oral Health · doi:10.1186/s12903-016-0250-8 · Cited by 26 · see citing works
Human dental stem cells suppress PMN activity after infection with the periodontopathogens Prevotella intermedia and Tannerella forsythia
Hieke, C., Kriebel, K., Engelmann, R., Müller‐Hilke, B., Lang, H., & Kreikemeyer, B. (2016) · Scientific Reports · doi:10.1038/srep39096 · Cited by 24 · see citing works
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Interactions of Anaerobic Bacteria with Dental Stem Cells: An In Vitro Study
Biedermann, A., Kriebel, K., Kreikemeyer, B., & Lang, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110616 · Cited by 23 · see citing works
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Isolation and characterization of Actinomyces viscosus mutants defective in binding salivary proline-rich proteins
Nesbitt, W. E., Beem, J. E., Leung, K. ‐., & CLARK, W. B. (1992) · Infection and Immunity · doi:10.1128/iai.60.3.1095-1100.1992 · Cited by 19 · see citing works
Recent Advances in Host Defense Mechanisms/ Therapies against Oral Infectious Diseases and Consequences for Systemic Disease
Gaffen, S. L., Herzberg, M. C., Taubman, M. A., & Dyke, T. E. V. (2014) · Advances in Dental Research · doi:10.1177/0022034514525778 · Cited by 19 · see citing works
Effect of Porphyromonas gingivalis on Citrullination of Proteins by Macrophages In Vitro
Marchant, C. L., Smith, M., Proudman, S., Haynes, D. R., & Bartold, P. M. (2012) · Journal of Periodontology · doi:10.1902/jop.2012.120103 · Cited by 17 · see citing works
The role of the RgpA–Kgp proteinase–adhesin complexes in the adherence of Porphyromonas gingivalis to fibroblasts
Pathirana, R. D., O’brien-simpson, N. M., Visvanathan, K., Hamilton, J. A., & Reynolds, E. C. (2008) · Microbiology · doi:10.1099/mic.0.2008/019943-0 · Cited by 17 · see citing works
Infection of primary human gingival fibroblasts by Porphyromonas gingivalis and Prevotella intermedia
Dogan, S., Gunzer, F., Guenay, H., Hillmann, G., & Geurtsen, W. (2000) · Clinical Oral Investigations · doi:10.1007/s007840050111 · Cited by 15 · see citing works
Expression profile of macrophage migration‐inhibitory factor in human gingiva and reconstituted human gingival epithelia stimulated by Porphyromonas gingivalis lipopolysaccharide
Li, X., Lan, H. Y., Huang, X., Zhang, C., & Jin, L. (2013) · Journal of Periodontal Research · doi:10.1111/jre.12035 · Cited by 13 · see citing works
Sterol Regulatory Element-Binding Protein-1c Regulates Inflammasome Activation in Gingival Fibroblasts Infected with High-Glucose-Treated Porphyromonas gingivalis
Kuo, H., Chang, L., Chen, T., Lee, K., Lee, K.-F., Chen, C., & Yu, H. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00195 · Cited by 10 · see citing works

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The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
The Structure of Dental Plaque Microbial Communities in the Transition from Health to Dental Caries and Periodontal Disease
Valm, A. M. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.016 · Cited by 425 · see citing works
The Oral Microbiota: Community Composition, Influencing Factors, Pathogenesis, and Interventions
Li, X., Liu, Y., Yang, X., Li, C., & Song, Z. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.895537 · Cited by 344 · see citing works
The Gut Microbiota: Emerging Evidence in Autoimmune Diseases
Zhang, X., Chen, B.-D., Zhao, L., & Li, H. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.04.001 · Cited by 257 · see citing works
Can an Infection Hypothesis Explain the Beta Amyloid Hypothesis of Alzheimer’s Disease?
Fülöp, T., Witkowski, J. M., Bourgade, K., Khalil, A., Zerif, E., Larbi, A., Hirokawa, K., Pawelec, G., Bocti, C., Lacombe, G., et al. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00224 · Cited by 201 · see citing works
Harmful chemicals emitted from electronic cigarettes and potential deleterious effects in the oral cavity
Ebersole, J. L., Samburova, V., Son, Y., Cappelli, D. P., Demopoulos, C. A., Capurro, A., Pinto, A., Chrzan, B., Kingsley, K., Howard, K. M., et al. (2020) · Tobacco Induced Diseases · doi:10.18332/tid/116988 · Cited by 132 · see citing works
Talk to your gut: the oral-gut microbiome axis and its immunomodulatory role in the etiology of rheumatoid arthritis
Espina, M. D. T., Gabarrini, G., Harmsen, H. J. M., Westra, J., Winkelhoff, A. J. V., & van Dijl, J. M. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy035 · Cited by 130 · see citing works
Effect of curcumin on growth, biofilm formation and virulence factor gene expression of Porphyromonas gingivalis
Kumbar, V. M., Peram, M. R., Kugaji, M. S., Shah, T., Patil, S., Muddapur, U. M., & Bhat, K. G. (2020) · Odontology · doi:10.1007/s10266-020-00514-y · Cited by 109 · see citing works
Smart dental materials for antimicrobial applications
Montoya, C., Roldan, L., Yu, M., Valliani, S., Ta, C., Yang, M., & Orrego, S. (2022) · Bioactive Materials · doi:10.1016/j.bioactmat.2022.12.002 · Cited by 108 · see citing works
The Human Respiratory Microbiome: Current Understandings and Future Directions
Zhao, L., Luo, J., Ali, M. K., Spiekerkoetter, E. F., & Nicolls, M. R. (2022) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2022-0208tr · Cited by 92 · see citing works
Increased citrullination and expression of peptidylarginine deiminases independently of P. gingivalis and A. actinomycetemcomitans in gingival tissue of patients with periodontitis
Engström, M., Eriksson, K., Lee, L., Hermansson, M., Johansson, A. S., Nicholas, A. P., Gerasimčik, N., Lundberg, K., Klareskog, L., Catrina, A. I., et al. (2018) · Journal of Translational Medicine · doi:10.1186/s12967-018-1588-2 · Cited by 86 · see citing works
Therapeutic effects of antibiotics loaded cellulose nanofiber and κ-carrageenan oligosaccharide composite hydrogels for periodontitis treatment
Johnson, A., Kong, F., Miao, S., Lin, H. V., Thomas, S., Huang, Y., & Kong, Z. (2020) · Scientific Reports · doi:10.1038/s41598-020-74845-9 · Cited by 86 · see citing works
Mineral-Doped Poly(L-lactide) Acid Scaffolds Enriched with Exosomes Improve Osteogenic Commitment of Human Adipose-Derived Mesenchymal Stem Cells
Gandolfi, M. G., Gardin, C., Zamparini, F., Ferroni, L., Esposti, M. D., Parchi, G., Ercan, B., Manzoli, L., Fava, F., Fabbri, P., et al. (2020) · Nanomaterials · doi:10.3390/nano10030432 · Cited by 84 · see citing works
Gut microbiome and autoimmune disorders
Shaheen, W., Quraishi, M. N., & Iqbal, T. H. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac057 · Cited by 85 · see citing works
Oral Biofilm: Development Mechanism, Multidrug Resistance, and Their Effective Management with Novel Techniques
Rath, S., Bal, S. C. B., & Dubey, D. (2021) · Rambam Maimonides Medical Journal · doi:10.5041/rmmj.10428 · Cited by 78 · see citing works
Gardnerella and vaginal health: the truth is out there
Rosca, A. S., Castro, J., Sousa, L. G. V., & Cerca, N. (2019) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuz027 · Cited by 78 · see citing works
The systemic oral health connection: Biofilms
Kurtzman, G. M., Horowitz, R. A., Johnson, R., Prestiano, R. A., & Klein, B. I. (2022) · Medicine · doi:10.1097/md.0000000000030517 · Cited by 70 · see citing works
The Oral Microbiome Bank of China
Xian, P., Zhou, X., Xu, X., Yuqing, L., Li, Y., Li, J., Su, X., Huang, S., Xu, J., & Liao, G. (2018) · International Journal of Oral Science · doi:10.1038/s41368-018-0018-x · Cited by 65 · see citing works
Anti-bacterial efficacy via drug-delivery system from layer-by-layer coating for percutaneous dental implant components
de Ávila, É. D., Castro, A. G. B., Tagit, O., Krom, B. P., Löwik, D. W. P. M., van Well, A. A., Bannenberg, L. J., Vergani, C. E., & van den Beucken, J. J. J. P. (2019) · Applied Surface Science · doi:10.1016/j.apsusc.2019.05.154 · Cited by 65 · see citing works
A review of co-culture models to study the oral microenvironment and disease
Mountcastle, S. E., Cox, S. C., Sammons, R. L., Jabbari, S., Shelton, R. M., & Kuehne, S. A. (2020) · Journal of Oral Microbiology · doi:10.1080/20002297.2020.1773122 · Cited by 62 · see citing works
Modulation of pathogenic oral biofilms towards health with nisin probiotic
Radaic, A., Ye, C., Parks, B., Gao, L., Kuraji, R., Malone, E., Kamarajan, P., Zhan, L., & Kapila, Y. L. (2020) · Journal of Oral Microbiology · doi:10.1080/20002297.2020.1809302 · Cited by 59 · see citing works
Candida albicans Shields the Periodontal Killer Porphyromonas gingivalis from Recognition by the Host Immune System and Supports the Bacterial Infection of Gingival Tissue
Bartnicka, D., Gonzalez‐Gonzalez, M., Sykut, J., Kozieł, J., Ciastoń, I., Adamowicz, K., Braś, G., Zawrotniak, M., Karkowska‐Kuleta, J., Satała, D., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21061984 · Cited by 59 · see citing works
Gut Microbiota and Autoimmune Diseases: Mechanisms, Treatment, Challenges, and Future Recommendations
Heravi, F. S. (2024) · Current Clinical Microbiology Reports · doi:10.1007/s40588-023-00213-6 · Cited by 65 · see citing works
Highly porous polycaprolactone scaffolds doped with calcium silicate and dicalcium phosphate dihydrate designed for bone regeneration
Gandolfi, M. G., Zamparini, F., Esposti, M. D., Chiellini, E., Fava, F., Fabbri, P., Taddei, P., & Prati, C. (2019) · Materials Science and Engineering C · doi:10.1016/j.msec.2019.04.040 · Cited by 58 · see citing works
Oral Biofilm and Its Impact on Oral Health, Psychological and Social Interaction
Meseret, A. G. (2021) · International Journal of Oral and Dental Health · doi:10.23937/2469-5734/1510127 · Cited by 56 · see citing works
Rational Designs of Biomaterials for Combating Oral Biofilm Infections
Yin, Z., Liu, Y., Anniwaer, A., You, Y., Guo, J., Tang, Y., Fu, L., Yi, L., & Huang, C. (2023) · Advanced Materials · doi:10.1002/adma.202305633 · Cited by 55 · see citing works
Anti-Biofilm Effects of Synthetic Antimicrobial Peptides Against Drug-Resistant Pseudomonas aeruginosa and Staphylococcus aureus Planktonic Cells and Biofilm
Park, S., Lee, M. Y., Kim, J., Kim, H., Jung, M., Shin, M., Lee, W., Cheong, G., Lee, J. R., & Jang, M.-K. (2019) · Molecules · doi:10.3390/molecules24244560 · Cited by 52 · see citing works
Impact of diet on human gut microbiome and disease risk
Mansour, S. R., Moustafa, M., Saad, B. M., hamed, R. A., & Moustafa, A. (2021) · New Microbes and New Infections · doi:10.1016/j.nmni.2021.100845 · Cited by 55 · see citing works
Correlation of periodontal and microbiological evaluations, with serum levels of estradiol and progesterone, during different trimesters of gestation
Massoni, R. S. D. S., Aranha, A. M. F., Matos, F. Z., Guedes, O. A., Borges, Á. H., Miotto, M., & Porto, A. N. (2019) · Scientific Reports · doi:10.1038/s41598-019-48288-w · Cited by 52 · see citing works
Spatial scale in analysis of the dental plaque microbiome
Borisy, G. G., & Valm, A. M. (2021) · Periodontology 2000 · doi:10.1111/prd.12364 · Cited by 53 · see citing works
Oral dysbiosis and systemic diseases
Georges, F. M., Do, N. T., & Seleem, D. (2022) · Frontiers in Dental Medicine · doi:10.3389/fdmed.2022.995423 · Cited by 49 · see citing works
Calibrated interdental brushing for the prevention of periodontal pathogens infection in young adults - a randomized controlled clinical trial
Bourgeois, D., Bravo, M., Llodrá, J., Inquimbert, C., Viennot, S., Dussart, C., & Carrouel, F. (2019) · Scientific Reports · doi:10.1038/s41598-019-51938-8 · Cited by 47 · see citing works
Autologous platelet-rich fibrin stimulates canine periodontal regeneration
Kornsuthisopon, C., Pirarat, N., Osathanon, T., & Kalpravidh, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-58732-x · Cited by 43 · see citing works
In-Vitro Antibacterial and Anti-Inflammatory Effects of Surfactin-Loaded Nanoparticles for Periodontitis Treatment
Johnson, A., Kong, F., Miao, S., Thomas, S., Ansar, S., & Kong, Z. (2021) · Nanomaterials · doi:10.3390/nano11020356 · Cited by 42 · see citing works
How Good are Bacteriophages as an Alternative Therapy to Mitigate Biofilms of Nosocomial Infections
Singh, A., Padmesh, S., Dwivedi, M., & Kostova, I. P. (2022) · Infection and Drug Resistance · doi:10.2147/idr.s348700 · Cited by 41 · see citing works
Smart responsive materials for antibacterial therapy: Progress, opportunities, and challenges
Fu, J., Wang, C., Liu, X., Zhu, S., Zheng, Y., Li, Z., Cui, Z., Zhang, Y., Jiang, H., Cao, Y., et al. (2025) · Progress in Materials Science · doi:10.1016/j.pmatsci.2025.101532 · Cited by 42 · see citing works
Enterococcus faecalis Antagonizes Pseudomonas aeruginosa Growth in Mixed-Species Interactions
Tan, C. A. Z., Lam, L. N., Biuković, G., Soh, E. Y., Toh, X. W., Lemos, J. A. C., & Kline, K. A. (2022) · Journal of Bacteriology · doi:10.1128/jb.00615-21 · Cited by 45 · see citing works
Personalizing Nutrition Strategies: Bridging Research and Public Health
Clemente‐Suárez, V. J., Peris-Ramos, H. C., Redondo-Flórez, L., Beltrán-Velasco, A. I., Martín-Rodríguez, A., David-Fernandez, S., Sepulveda, R. A. Y., & Tornero-Aguilera, J. F. (2024) · Journal of Personalized Medicine · doi:10.3390/jpm14030305 · Cited by 35 · see citing works
Can metagenomics unravel the impact of oral bacteriome in human diseases?
Chattopadhyay, I., Lu, W., Manikam, R., Malarvili, M. B., Ambati, R. R., & Gundamaraju, R. (2022) · Biotechnology and Genetic Engineering Reviews · doi:10.1080/02648725.2022.2102877 · Cited by 35 · see citing works
Periodontal treatment prevents arthritis in mice and methotrexate ameliorates periodontal bone loss
Lübcke, P. M., Ebbers, M., Volzke, J., Bull, J., Kneitz, S., Engelmann, R., Lang, H., Kreikemeyer, B., & Müller‐Hilke, B. (2019) · Scientific Reports · doi:10.1038/s41598-019-44512-9 · Cited by 31 · see citing works
Self-citation
Ins and Outs: Recent Advancements in Membrane Protein-Mediated Prokaryotic Ferrous Iron Transport
Brown, J. B., Lee, M. A., & Smith, A. T. (2021) · Biochemistry · doi:10.1021/acs.biochem.1c00586 · Cited by 31 · see citing works
Functional profile of oral plaque microbiome: Further insight into the bidirectional relationship between type 2 diabetes and periodontitis
Favale, N., Fariña, R., Carrieri, A., Simonelli, A., Severi, M., Sabbioni, S., Trombelli, L., & Scapoli, C. (2023) · Molecular Oral Microbiology · doi:10.1111/omi.12418 · Cited by 28 · see citing works
The composition of microbial communities in inflammatory periodontal diseases in young adults Tatars
Харитонова, М. А., Vankov, P., Abdrakhmanov, A. K., Мамаева, Е. В., Yakovleva, G., & Ilinskaya, O. N. (2021) · AIMS Microbiology · doi:10.3934/microbiol.2021005 · Cited by 26 · see citing works
Microbial dysbiosis and immune dysregulation in periodontitis and peri-implantitis
Mehrnia, N., & Dyke, T. E. V. (2026) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1678163 · Cited by 24 · see citing works
In-vitro polymicrobial oral biofilm model represents clinical microbial profile and disease progression during implant-related infections
Dini, C., Costa, R. C., Bertolini, M., Shibli, J. A., Feres, M., Klein, M. I., de Ávila, É. D., Souza, J. G. S., & Barão, V. A. R. (2023) · Journal of Applied Microbiology · doi:10.1093/jambio/lxad265 · Cited by 25 · see citing works
The contribution of maternal factors to the oral microbiota of the child: Influence from early life and clinical relevance
Azevedo, M. J., Garcia, A., Costa, C. F. F. A., Ferreira, A. F., Falcão‐Pires, I., Brandt, B. W., Ramalho, C. M. A., Zaura, E., & Sampaio‐Maia, B. (2023) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2023.06.002 · Cited by 23 · see citing works
Bacterial infections in cancer: A bilateral relationship
Basu, A., Singh, R., & Gupta, S. (2022) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1771 · Cited by 19 · see citing works
Approaches to Modulate Biofilm Ecology
Nascimento, M. M. (2019) · Dental Clinics of North America · doi:10.1016/j.cden.2019.07.002 · Cited by 18 · see citing works
The Influence of Salivary pH on the Prevalence of Dental Caries
Rusu, L.-C., Roi, A., Roi, C.-I., Țigmeanu, C. V., & Ardelean, L. C. (2022) · Dentistry · doi:10.5772/intechopen.106154 · Cited by 17 · see citing works
Comparison of three qPCR-based commercial tests for detection of periodontal pathogens
van der Weijden, G. A., Rijnen, M. E., & Valkenburg, C. (2021) · Scientific Reports · doi:10.1038/s41598-021-85305-3 · Cited by 15 · see citing works
Porphyromonas gingivalis Peptidyl Arginine Deiminase Can Modulate Neutrophil Activity via Infection of Human Dental Stem Cells
Kriebel, K., Hieke, C., Engelmann, R., Potempa, J., Müller‐Hilke, B., Lang, H., & Kreikemeyer, B. (2018) · Journal of Innate Immunity · doi:10.1159/000489020 · Cited by 15 · see citing works
Self-citation
Comparing the effectiveness of water flosser and dental floss in plaque reduction among adults: A systematic review
Mohapatra, S., Rajpurohit, L., Mohandas, R., & Patil, S. K. (2023) · Journal of Indian Society of Periodontology · doi:10.4103/jisp.jisp_597_22 · Cited by 14 · see citing works
Oral microbial profiles of extrinsic black tooth stain in primary dentition: A literature review
Dong, X., Zhao, W., Ma, S., Li, X., Li, G., & Zhang, S. (2024) · Journal of Dental Sciences · doi:10.1016/j.jds.2024.02.028 · Cited by 13 · see citing works
A Porphyromonas gingivalis Capsule-Conjugate Vaccine Protects From Experimental Oral Bone Loss
Rocha, F. R. G., Berges, A., Sedra, A., Ghods, S., Kapoor, N., Pill, L., Davey, M. E., Fairman, J., & Gibson, F. C. (2021) · Frontiers in Oral Health · doi:10.3389/froh.2021.686402 · Cited by 13 · see citing works
Effect of Exo/Endogenous Prophylaxis Dentifrice/Drug and Cariogenic Conditions of Patient on Molecular Property of Dental Biofilm: Synchrotron FTIR Spectroscopic Study
Seredin, P. V., Goloshchapov, D. L., Михайлович, К. В., Nesterov, D. N., Ippolitov, Y. A., Ippolitov, I. Y., & Vongsvivut, J. P. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14071355 · Cited by 12 · see citing works
Modelling periodontitis in vitro: engineering strategies and biofilm model development
Wang, C., Xu, T., Seneviratne, C. J., Ong, L. J. Y., & Zhou, Y. (2024) · Frontiers in Biomaterials Science · doi:10.3389/fbiom.2024.1380153 · Cited by 11 · see citing works
Enterococcus faecalis Shields Porphyromonas gingivalis in Dual-Species Biofilm in Oxic Condition
Tan, H. C., Cheung, G. S. P., Chang, J. W. W., Zhang, C., & Lee, A. H. C. (2022) · Microorganisms · doi:10.3390/microorganisms10091729 · Cited by 11 · see citing works
Bacterial Populations in Subgingival Plaque Under Healthy and Diseased Conditions: Genomic Insights into Oral Adaptation Strategies by Lactobacillus sp. Strain DISK7
Urvashi, U., Sharma, D., Sharma, S., Pal, V. K., Lal, R., Patil, P. B., Grover, V., & Korpole, S. (2019) · Indian Journal of Microbiology · doi:10.1007/s12088-019-00828-8 · Cited by 10 · see citing works
Comprehensive strategies for overcoming dental biofilms: Microbial dynamics and innovative methods
Bharathi, S., Ganapathy, D., Sundramurthy, V. P., & Mohanasundaram, S. (2025) · Microbial Pathogenesis · doi:10.1016/j.micpath.2025.107690 · Cited by 9 · see citing works
The Effect of Probiotic Lactobacillus Strains on Porphyromonas gingivalis, the Etiological Factor of Periodontal Diseases—A Systematic Review
Kamianowski, C., Kamianowski, A., Nikitiuk, J., Tomczyk, T., Kindeusz, K., Sierpińska, T., & Kamianowska, M. (2025) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-025-10607-1 · Cited by 9 · see citing works
The Feasibility of Phage Therapy for Periodontitis
Zhen, C., Guo, Z., Lin, H., Tian, Y., Zhang, P., Chen, H., Wang, Y., & Shen, Y. (2021) · Future Microbiology · doi:10.2217/fmb-2020-0161 · Cited by 8 · see citing works
Apical Periodontitis in Patients With Inflammatory Bowel Disease: A Puppet Master?
Barta, Z. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izz129 · Cited by 8 · see citing works
Competitive advantage of oral streptococci for colonization of the middle ear mucosa
Jacob, K. M., & Reguera, G. (2022) · Biofilm · doi:10.1016/j.bioflm.2022.100067 · Cited by 7 · see citing works
Periodontal bacteria and the rheumatoid arthritis-related antigen RA-A47: the cross-reactivity potential
Lucchese, A. (2019) · Current Opinion in Rheumatology · doi:10.1097/bor.0000000000000611 · Cited by 6 · see citing works
Measurement of the Level of Nitric Oxide in Exhaled Air in Patients Using Acrylic Complete Dentures and with Oral Pathologies
Wyszyńska, M., Czelakowska, A., Rój, R., Zajac, M., Mielnik, M., Kasperski, J., & Skucha-Nowak, M. (2021) · Coatings · doi:10.3390/coatings11020169 · Cited by 6 · see citing works
Emerging avenues linking myeloid-derived suppressor cells to periodontal disease
Leija-Montoya, A. G., González-Ramírez, J., Serafín-Higuera, I. R., Sandoval-Basilio, J., Isiordia‐Espinoza, M. A., & Serafín‐Higuera, N. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2022.12.001 · Cited by 6 · see citing works
Recent developments in antimicrobial polymers for biofilm inhibition
Kropp, G. A., McMillian, C. N., Mase, J. D., Kandagiri, S., Nowak, E. S., & Schulz, M. D. (2026) · Chemical Communications · doi:10.1039/d5cc06617d · Cited by 5 · see citing works
Potent anti-inflammatory responses: Role of hydrogen in IL-1α dominated early phase systemic inflammation
Wei, Y., Wang, K., Zhang, Y., Duan, Y., Tian, Y., Yin, H., Fu, X., Ma, Z., Zhou, J., Yu, M., et al. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1138762 · Cited by 5 · see citing works
Tip Modification for Interaction Studies Between Polysaccharides and Dental Materials
Ehnert, S., Müller−Renno, C., Hannig, M., & Ziegler, C. (2023) · physica status solidi (a) · doi:10.1002/pssa.202200834 · Cited by 5 · see citing works
Epigenetics and the role of nutraceuticals in health and disease
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Authors: Kriebel, K., Hieke, C., Müller-Hilke, B., Nakata, M., & Kreikemeyer, B.
Affiliations: University of Rostock (DE)
The University of Osaka (JP)
Corresponding author: Nakata, Masanobu
Kreikemeyer, Bernd
ORCID: Nakata, Masanobu
Kreikemeyer, Bernd
Venue: Frontiers in Microbiology
Publisher: Frontiers Media SA
Published: 2018-01-30
Volume: 9
Pages: 53-53
ISSN: 1664-302X (ISSN-L)
DOI: 10.3389/fmicb.2018.00053
PMC: PMC5797574
OpenAlex: W2791797299
Cited by: 118
References: 170
Citations by year: 2026: 9 · 2025: 17 · 2024: 8 · 2023: 15 · 2022: 19 · 2021: 16 · 2020: 12 · 2019: 17 · 2018: 5
FWCI: 1.83
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: Frontiers in Microbiology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Japan Society for the Promotion of Science (17H04369, 17K19751, 15KK0306, 17K11610, 18K19643, 15H05012)
Topics: Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Health Sciences › Dentistry › Periodontics › Oral Health Pathology and Treatment
Keywords: dental plaque, periodontitis, rheumatoid arthritis, peptidylarginine deiminase, Porphyromonas gingivalis, oral pathobionts, oral microbiota, dental stem cells, immunomodulation, host-pathogen interaction, systemic disease

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Oral Biofilms from Symbiotic to Pathogenic Interactions and Associated Disease –Connection of Periodontitis and Rheumatic Arthritis by Peptidylarginine Deiminase

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