How Does Epstein–Barr Virus Contribute to Chronic Periodontitis?
Abstract
:1. Introduction
2. Molecular Mechanism of the Maintenance of EBV Latency
3. Microbial Interaction Between Periodontopathic Bacteria and EBV May Control EBV Reactivation in the Periodontium
4. Etiological Significances of EBV Infection in the Periodontium
5. Concluding Remarks
Author Contributions
Funding
Conflicts of Interest
References
- Thompson, M.P.; Kurzrock, R. Epstein-barr virus and cancer. Clin. Cancer Res. 2004, 10, 803–821. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsurumi, T.; Fujita, M.; Kudoh, A. Latent and lytic epstein-barr virus replication strategies. Rev. Med. Virol. 2005, 15, 3–15. [Google Scholar] [CrossRef] [PubMed]
- Hajishengallis, G. Periodontitis: From microbial immune subversion to systemic inflammation. Nat. Rev. Immunol. 2015, 15, 30–44. [Google Scholar] [CrossRef] [PubMed]
- Darveau, R.P. Periodontitis: A polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 2010, 8, 481–490. [Google Scholar] [CrossRef]
- Imai, K.; Yamada, K.; Tamura, M.; Ochiai, K.; Okamoto, T. Reactivation of latent HIV-1 by a wide variety of butyric acid-producing bacteria. Cell. Mol. Life Sci. 2012, 69, 2583–2592. [Google Scholar] [CrossRef]
- Imai, K.; Ochiai, K.; Okamoto, T. Reactivation of latent HIV-1 infection by the periodontopathic bacterium Porphyromonas gingivalis involves histone modification. J. Immunol. 2009, 182, 3688–3695. [Google Scholar] [CrossRef] [Green Version]
- Abusleme, L.; Dupuy, A.K.; Dutzan, N.; Silva, N.; Burleson, J.A.; Strausbaugh, L.D.; Gamonal, J.; Diaz, P.I. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013, 7, 1016–1025. [Google Scholar] [CrossRef] [Green Version]
- Ledder, R.G.; Gilbert, P.; Huws, S.A.; Aarons, L.; Ashley, M.P.; Hull, P.S.; McBain, A.J. Molecular analysis of the subgingival microbiota in health and disease. Appl. Environ. Microbiol. 2007, 73, 516–523. [Google Scholar] [CrossRef] [Green Version]
- Riep, B.; Edesi-Neuss, L.; Claessen, F.; Skarabis, H.; Ehmke, B.; Flemmig, T.F.; Bernimoulin, J.P.; Gobel, U.B.; Moter, A. Are putative periodontal pathogens reliable diagnostic markers? J. Clin. Microbiol. 2009, 47, 1705–1711. [Google Scholar] [CrossRef] [Green Version]
- Contreras, A.; Nowzari, H.; Slots, J. Herpesviruses in periodontal pocket and gingival tissue specimens. Oral Microbiol. Immunol. 2000, 15, 15–18. [Google Scholar] [CrossRef]
- Lu, H.; Zhu, C.; Li, F.; Xu, W.; Tao, D.; Feng, X. Putative periodontopathic bacteria and herpesviruses in pregnant women: A case-control study. Sci. Rep. 2016, 6, 27796. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slots, J. Herpesviral-bacterial interactions in periodontal diseases. Periodontology 2000 2010, 52, 117–140. [Google Scholar] [CrossRef] [PubMed]
- Saygun, I.; Kubar, A.; Ozdemir, A.; Slots, J. Periodontitis lesions are a source of salivary cytomegalovirus and epstein-barr virus. J. Periodontal Res. 2005, 40, 187–191. [Google Scholar] [CrossRef] [PubMed]
- Konstantinidis, A.; Sakellari, D.; Papa, A.; Antoniadis, A. Real-time polymerase chain reaction quantification of epstein-barr virus in chronic periodontitis patients. J. Periodontal Res. 2005, 40, 294–298. [Google Scholar] [CrossRef] [PubMed]
- Kato, A.; Imai, K.; Ochiai, K.; Ogata, Y. Higher prevalence of epstein-barr virus DNA in deeper periodontal pockets of chronic periodontitis in Japanese patients. PLoS ONE 2013, 8, e71990. [Google Scholar] [CrossRef]
- Kato, A.; Imai, K.; Ochiai, K.; Ogata, Y. Prevalence and quantitative analysis of epstein-barr virus DNA and Porphyromonas gingivalis associated with Japanese chronic periodontitis patients. Clin. Oral Investig. 2015, 19, 1605–1610. [Google Scholar] [CrossRef] [Green Version]
- Vincent-Bugnas, S.; Vitale, S.; Mouline, C.C.; Khaali, W.; Charbit, Y.; Mahler, P.; Precheur, I.; Hofman, P.; Maryanski, J.L.; Doglio, A. EBV infection is common in gingival epithelial cells of the periodontium and worsens during chronic periodontitis. PLoS ONE 2013, 8, e80336. [Google Scholar] [CrossRef] [Green Version]
- Chalabi, M.; Rezaie, F.; Moghim, S.; Mogharehabed, A.; Rezaei, M.; Mehraban, B. Periodontopathic bacteria and herpesviruses in chronic periodontitis. Mol. Oral Microbiol. 2010, 25, 236–240. [Google Scholar] [CrossRef]
- Slots, J.; Saygun, I.; Sabeti, M.; Kubar, A. Epstein-barr virus in oral diseases. J. Periodontal Res. 2006, 41, 235–244. [Google Scholar] [CrossRef]
- Sunde, P.T.; Olsen, I.; Enersen, M.; Grinde, B. Patient with severe periodontitis and subgingival epstein-barr virus treated with antiviral therapy. J. Clin. Virol. 2008, 42, 176–178. [Google Scholar] [CrossRef]
- Li, B.; Carey, M.; Workman, J.L. The role of chromatin during transcription. Cell 2007, 128, 707–719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berger, S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447, 407–412. [Google Scholar] [CrossRef] [PubMed]
- Colin, L.; Van Lint, C. Molecular control of HIV-1 postintegration latency: Implications for the development of new therapeutic strategies. Retrovirology 2009, 6, 111. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Imai, K.; Okamoto, T. Transcriptional repression of human immunodeficiency virus type 1 by AP-4. J. Biol. Chem. 2006, 281, 12495–12505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roizman, B. The checkpoints of viral gene expression in productive and latent infection: The role of the HDAC/CoREST/LSD1/REST repressor complex. J. Virol. 2011, 85, 7474–7482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pollicino, T.; Belloni, L.; Raffa, G.; Pediconi, N.; Squadrito, G.; Raimondo, G.; Levrero, M. Hepatitis B virus replication is regulated by the acetylation status of hepatitis B virus cccDNA-bound H3 and H4 histones. Gastroenterology 2006, 130, 823–837. [Google Scholar] [CrossRef] [PubMed]
- Takacs, M.; Banati, F.; Koroknai, A.; Segesdi, J.; Salamon, D.; Wolf, H.; Niller, H.H.; Minarovits, J. Epigenetic regulation of latent epstein-barr virus promoters. Biochim. Biophys. Acta 2010, 1799, 228–235. [Google Scholar] [CrossRef]
- Speck, S.H.; Chatila, T.; Flemington, E. Reactivation of epstein-barr virus: Regulation and function of the bzlf1 gene. Trends Microbiol. 1997, 5, 399–405. [Google Scholar] [CrossRef]
- Liu, S.; Borras, A.M.; Liu, P.; Suske, G.; Speck, S.H. Binding of the ubiquitous cellular transcription factors Sp1 and Sp3 to the ZI domains in the epstein-barr virus lytic switch bzlf1 gene promoter. Virology 1997, 228, 11–18. [Google Scholar] [CrossRef] [Green Version]
- Gruffat, H.; Manet, E.; Sergeant, A. MEF2-mediated recruitment of class II HDAC at the EBV immediate early gene bzlf1 links latency and chromatin remodeling. EMBO Rep. 2002, 3, 141–146. [Google Scholar] [CrossRef] [Green Version]
- Liu, S.; Liu, P.; Borras, A.; Chatila, T.; Speck, S.H. Cyclosporin a-sensitive induction of the epstein-barr virus lytic switch is mediated via a novel pathway involving a MEF2 family member. EMBO J. 1997, 16, 143–153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Imai, K.; Kamio, N.; Cueno, M.E.; Saito, Y.; Inoue, H.; Saito, I.; Ochiai, K. Role of the histone H3 lysine 9 methyltransferase suv39 h1 in maintaining epsteinn-barr virus latency in B95-8 cells. FEBS J. 2014, 281, 281–2148. [Google Scholar] [CrossRef] [PubMed]
- Murata, T.; Kondo, Y.; Sugimoto, A.; Kawashima, D.; Saito, S.; Isomura, H.; Kandam, T.; Tsurumi, T. Epigenetic histone modification of epstein-barr virus bzlf1 promoter during latency and reactivation in Raji cells. J. Virol. 2012, 86, 4752–4761. [Google Scholar] [CrossRef] [Green Version]
- Imai, K.; Inoue, H.; Tamura, M.; Cueno, M.E.; Inoue, H.; Takeichi, O.; Kusamam, K.; Saito, I.; Ochiai, K. The periodontal pathogen Porphyromonas gingivalis induces the epstein-barr virus lytic switch transactivator zebra by histone modification. Biochimie 2012, 94, 839–846. [Google Scholar] [CrossRef] [PubMed]
- Berni Canani, R.; Di Costanzo, M.; Leone, L. The epigenetic effects of butyrate: Potential therapeutic implications for clinical practice. Clin. Epigenetics 2012, 4, 4. [Google Scholar] [CrossRef]
- Louis, P.; Young, P.; Holtrop, G.; Flint, H.J. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:Acetate CoA-transferase gene. Environ. Microbiol. 2010, 12, 304–314. [Google Scholar] [CrossRef]
- Imai, K.; Victoriano, A.F.; Ochiai, K.; Okamoto, T. Microbial interaction of periodontopathic bacterium Porphyromonas gingivalis and HIV-possible causal link of periodontal diseases to aids progression. Curr. HIV Res. 2012, 10, 238–244. [Google Scholar] [CrossRef]
- Birx, D.L.; Redfield, R.R.; Tosato, G. Defective regulation of epstein-barr virus infection in patients with acquired immunodeficiency syndrome (AIDS) or AIDS-related disorders. N. Engl. J. Med. 1986, 314, 874–879. [Google Scholar] [CrossRef]
- Lam, K.M.; Syed, N.; Whittle, H.; Crawford, D.H. Circulating epstein-barr virus-carrying Bcells in acute malaria. Lancet 1991, 337, 876–878. [Google Scholar] [CrossRef]
- Niederman, R.; Buyle-Bodin, Y.; Lu, B.Y.; Robinson, P.; Naleway, C. Short-chain carboxylic acid concentration in human gingival crevicular fluid. J. Dent. Res. 1997, 76, 575–579. [Google Scholar] [CrossRef]
- Margolis, H.C.; Duckworth, J.H.; Moreno, E.C. Composition and buffer capacity of pooled starved plaque fluid from caries-free and caries-susceptible individuals. J. Dent. Res. 1988, 67, 1476–1482. [Google Scholar] [CrossRef] [PubMed]
- Moreno, E.C.; Margolis, H.C. Composition of human plaque fluid. J. Dent. Res. 1988, 67, 1181–1189. [Google Scholar] [CrossRef] [PubMed]
- Silwood, C.J.; Lynch, E.; Claxson, A.W.; Grootveld, M.C. 1H and (13)C NMR spectroscopic analysis of human saliva. J. Dent. Res. 2002, 81, 422–427. [Google Scholar] [CrossRef] [PubMed]
- Westphal, E.M.; Blackstock, W.; Feng, W.; Israel, B.; Kenney, S.C. Activation of lytic epstein-barr virus (EBV) infection by radiation and sodium butyrate in vitro and in vivo: A potential method for treating EBV-positive malignancies. Cancer Res. 2000, 60, 5781–5788. [Google Scholar]
- Westphal, E.M.; Mauser, A.; Swenson, J.; Davis, M.G.; Talarico, C.L.; Kenney, S.C. Induction of lytic epstein-barr virus (EBV) infection in EBV-associated malignancies using adenovirus vectors in vitro and in vivo. Cancer Res. 1999, 59, 1485–1491. [Google Scholar]
- Koike, R.; Nodomi, K.; Watanabe, N.; Ogata, Y.; Takeichi, O.; Takei, M.; Kaneko, T.; Tonogi, M.; Kotani, A.; Imai, K. Butyric acid in saliva of chronic periodontitis patients induces transcription of the EBV lytic switch activator BZLF1: A pilot study. In. Vivo. 2020, 34, 587–594. [Google Scholar] [CrossRef] [Green Version]
- Yu, X.; Shahir, A.M.; Sha, J.; Feng, Z.; Eapen, B.; Nithianantham, S.; Das, B.; Karn, J.; Weinberg, A.; Bissada, N.F.; et al. Short-chain fatty acids from periodontal pathogens suppress histone deacetylases, ezh2, and suv39h1 to promote kaposi’s sarcoma-associated herpesvirus replication. J. Virol. 2014, 88, 4466–4479. [Google Scholar] [CrossRef] [Green Version]
- Tonoyan, L.; Vincent-Bugnas, S.; Olivieri, C.V.; Doglio, A. New viral facets in oral diseases: The EBV paradox. Int. J. Mol. Sci. 2019, 20, 5861. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, N.; Nodomi, K.; Koike, R.; Kato, A.; Takeichi, O.; Kotani, A.; Kaneko, T.; Sakagami, H.; Takei, M.; Ogata, Y.; et al. EBV LMP1 in gingival epithelium potentially contributes to human chronic periodontitis via inducible IL8 production. In. Vivo. 2019, 33, 1793–1800. [Google Scholar] [CrossRef] [Green Version]
- Kato, A.; Imai, K.; Sato, H.; Ogata, Y. Prevalence of epstein-barr virus DNA and Porphyromonas gingivalis in Japanese peri-implantitis patients. BMC Oral Health 2017, 17, 148. [Google Scholar] [CrossRef]
- Verdugo, F.; Castillo, A.; Castillo, F.; Uribarri, A. Epstein-barr virus associated peri-implantitis: A split-mouth study. Clin. Oral Investig. 2015, 19, 535–543. [Google Scholar] [CrossRef] [PubMed]
- Makino, K.; Takeichi, O.; Hatori, K.; Imai, K.; Ochiai, K.; Ogiso, B. Epstein-barr virus infection in chronically inflamed periapical granulomas. PLoS ONE 2015, 10, e0121548. [Google Scholar] [CrossRef] [PubMed]
- Makino, K.; Takeichi, O.; Imai, K.; Inoue, H.; Hatori, K.; Himi, K.; Saito, I.; Ochiai, K.; Ogiso, B. Porphyromonas endodontalis reactivates latent epstein-barr virus. Int. Endod. J. 2018, 51, 1410–1419. [Google Scholar] [PubMed]
- Himi, K.; Takeichi, O.; Imai, K.; Hatori, K.; Tamura, T.; Ogiso, B. Epstein-barr virus reactivation by persistent apical periodontal pathogens. Int. Endod. J. 2019, in press. [Google Scholar] [CrossRef]
- Jakovljevic, A.; Andric, M.; Nikolic, N.; Coric, V.; Krezovic, S.; Carkic, J.; Knezevic, A.; Beljic-Ivanovic, K.; Pljesa-Ercegovac, M.; Miletic, M.; et al. Levels of oxidative stress biomarkers and bone resorption regulators in apical periodontitis lesions infected by epstein-barr virus. Int. Endod. J. 2018, 51, 593–604. [Google Scholar] [CrossRef]
- Pihlstrom, B.L.; Michalowicz, B.S.; Johnson, N.W. Periodontal diseases. Lancet 2005, 366, 1809–1820. [Google Scholar] [CrossRef] [Green Version]
- Fiola, S.; Gosselin, D.; Takada, K.; Gosselin, J. TLR9 contributes to the recognition of EBV by primary monocytes and plasmacytoid dendritic cells. J. Immunol. 2010, 185, 3620–3631. [Google Scholar] [CrossRef] [Green Version]
- Gaudreault, E.; Fiola, S.; Olivier, M.; Gosselin, J. Epstein-barr virus induces MCP-1 secretion by human monocytes via TLR2. J. Virol. 2007, 81, 8016–8024. [Google Scholar] [CrossRef] [Green Version]
- Hajnicka, V.; Kudelova, M.; Stibraniova, I.; Slovak, M.; Bartikova, P.; Halasova, Z.; Pancik, P.; Belvoncikova, P.; Vrbova, M.; Holikova, V.; et al. Tick-borne transmission of murine gammaherpesvirus 68. Front. Cell Infect. Microbiol. 2017, 7, 458. [Google Scholar] [CrossRef]
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Imai, K.; Ogata, Y. How Does Epstein–Barr Virus Contribute to Chronic Periodontitis? Int. J. Mol. Sci. 2020, 21, 1940. https://doi.org/10.3390/ijms21061940
Imai K, Ogata Y. How Does Epstein–Barr Virus Contribute to Chronic Periodontitis? International Journal of Molecular Sciences. 2020; 21(6):1940. https://doi.org/10.3390/ijms21061940
Chicago/Turabian StyleImai, Kenichi, and Yorimasa Ogata. 2020. "How Does Epstein–Barr Virus Contribute to Chronic Periodontitis?" International Journal of Molecular Sciences 21, no. 6: 1940. https://doi.org/10.3390/ijms21061940