Epstein-Barr virus reactivation by persistent apical periodontal pathogens.
butyric acid
histone deacetylase inhibitor
human herpesvirus 4
periapical granuloma
persistent periapical periodontitis
Journal
International endodontic journal
ISSN: 1365-2591
Titre abrégé: Int Endod J
Pays: England
ID NLM: 8004996
Informations de publication
Date de publication:
Apr 2020
Apr 2020
Historique:
received:
16
07
2019
accepted:
13
11
2019
pubmed:
16
11
2019
medline:
18
3
2020
entrez:
16
11
2019
Statut:
ppublish
Résumé
To assess whether Epstein-Barr virus (EBV) reactivation is triggered by persistent apical periodontitis-related microbes using in vitro and ex vivo methodologies. Surgically removed human periapical granulomas (n = 50) and healthy gingival tissues (n = 10) were analysed to determine the presence of EBV and seven persistent apical periodontitis-related microbes. In addition, real-time polymerase chain reaction was used to detect the mRNA expression of BZLF-1, an immediate-early gene of EBV. Expression of latent membrane protein (LMP)-1 and ZEBRA, an early lytic protein of EBV encoded by BZLF-1, was also examined using triple-colour immunofluorescence staining. n-Butyric acid produced by the microbes was quantified, and luciferase assays were performed in association with bacterial lysates. In addition, Daudi cells were cultured with bacterial lysates, and the expression levels of BZLF-1 mRNA and ZEBRA protein were determined. EBV DNA and BZLF-1 mRNA were detected in 47 out of 50 periapical granulomas, but not in healthy gingival tissues. The EBV DNA copy number and the number of Fusobacterium nucleatum were significantly positively correlated with BZLF-1 expression in periapical granulomas. The number of Prevotella intermedia was slightly correlated with BZLF-1 expression; however, the other microbes were not. CD79a-positive B cells in periapical granulomas, but not those in healthy gingival tissues, expressed both LMP-1 and ZEBRA. n-Butyric acid production was the highest in F. nucleatum and the lowest in P. intermedia. Enterococcus faecalis, Candida albicans and the other tested microbes did not produce n-butyric acid. An F. nucleatum lysate exhibited significantly increased BZLF-1-luciferase activity in the same manner of commercial butyric acid, whereas P. intermedia did not. F. nucleatum also induced the expression of BZLF-1 mRNA and ZEBRA protein by Daudi cells, indicating that EBV reactivation was induced. Among the persistent apical periodontitis-related bacteria that were tested, F. nucleatum most strongly reactivated latent EBV, whereas E. faecalis and C. albicans as well as the other microbes did not.
Banques de données
GENBANK
['MK_540470', 'NR_152150', 'CP_032015', 'CP_008816', 'AE_015929', 'CP_036529', 'CP_028101', 'CP_019300', 'A_P017894']
Types de publication
Journal Article
Langues
eng
Pagination
492-505Subventions
Organisme : Japan Society for the Promotion of Science
ID : Grant-in-Aid for Scientific Research (17K11717)
Organisme : Nihon University Multidisciplinary Research Grant
ID : 2017-2018
Informations de copyright
© 2019 International Endodontic Journal. Published by John Wiley & Sons Ltd.
Références
Bokarewa M, Tarkowski A, Lind M, Dahlberg L, Magnusson M (2008) Arthritogenic dsRNA is present in synovial fluid from rheumatoid arthritis patients with an erosive disease course. European Journal of Immunology 38, 3237-44.
Candy B, Hotopf M (2006) Steroids for symptom control in infectious mononucleosis. Cochrane Database of Systematic Reviews 19, CD004402.
Cárdenas-Mondragón MG, Torres J, Sánchez-Zauco N et al. (2017) Elevated levels of interferon-γ are associated with high levels of Epstein-Barr virus reactivation in patients with the intestinal type of gastric cancer. Journal of Immunology Research 2017, 7069242.
Diehl V, Henle G, Henle W, Kohn G (1968) Demonstration of a herpes group virus in cultures of peripheral leukocytes from patients with infectious mononucleosis. Journal of Virology 2, 663-9.
Dirmeier U, Hoffmann R, Kilger E et al. (2005) Latent membrane protein 1 of Epstein-Barr virus coordinately regulates proliferation with control of apoptosis. Oncogene 24, 1711-17.
Epstein MA, Achong BG, Barr YM (1964) Virus particles in cultured lymphoblasts from Burkitt’s lymphoma. The Lancet 1, 702-3.
Faggioni A, Zompetta C, Grimaldi S, Barile G, Frati L, Lazdins J (1986) Calcium modulation activates Epstein-Barr virus genome in latently infected cells. Science 232, 1554-6.
Fang CY, Huang SY, Wu CC et al. (2012) The synergistic effect of chemical carcinogens enhances Epstein-Barr virus reactivation and tumor progression of nasopharyngeal carcinoma cells. PLoS ONE 7, e44810.
Farina A, Peruzzi G, Lacconi V et al. (2017) Epstein-Barr virus lytic infection promotes activation of Toll-like receptor 8 innate immune response in systemic sclerosis monocytes. Arthritis Research & Therapy 19, 39.
Fujii R, Saito Y, Tokura Y, Nakagawa KI, Okuda K, Ishihara K (2009) Characterization of bacterial flora in persistent apical periodontitis lesions. Oral Microbiology and Immunology 24, 502-5.
Gastaldello S, Chen X, Callegari S, Masucci MG (2013) Caspase-1 promotes Epstein-Barr virus replication by targeting the large tegument protein deneddylase to the nucleus of productively infected cells. PLoS Path 9, e1003664.
Harley JB, Zoller EE (2014) Editorial: What caused all these troubles, anyway? Epstein-Barr virus in Sjögren's syndrome reevaluated. Arthritis & Rheumatology 66, 2328-30.
Hassani A, Corboy JR, Al-Salam S, Khan G (2018) Epstein-Barr virus is present in the brain of most cases of multiple sclerosis and may engage more than just B cell. PLoS ONE 13, e0192109.
Henle W, Henle G (1970) Evidence for a relation of Epstein-Barr virus to Burkitt's lymphoma and nasopharyngeal carcinoma. Bibliotheca Haematologica 36, 706-13.
Inoue H, Mishima K, Yamamoto-Yoshida S et al. (2012) Aryl hydrocarbon receptor-mediated induction of EBV reactivation as a risk factor for Sjögren's syndrome. The Journal of Immunology 188, 4654-62.
Ishihara S, Okada S, Wakiguchi H, Kurashige T, Morishima T, Kawa-Ha K (1995) Chronic active Epstein-Barr virus infection in children in Japan. Acta Paediatrica 84, 1271-5.
Jakovljevic A, Andric M, Knezevic A et al. (2018a) Herpesviral infection in periapical periodontitis. Current Oral Health Reports 5, 255-63.
Jakovljevic A, Andric M, Nikolic N et al. (2018b) Levels of oxidative stress biomarkers and bone resorption regulators in apical periodontitis lesions infected by Epstein-Barr virus. International Endodontic Journal 51, 593-604.
Jakovljevic A, Knezevic A, Nikolic N et al. (2018c) Herpesviruses viral loads and levels of proinflammatory cytokines in apical periodontitis. Oral Diseases 24, 840-6.
Jones JF, Shurin S, Abramowsky C et al. (1988) T-cell lymphomas containing Epstein-Barr viral DNA in patients with chronic Epstein-Barr virus infections. The New England Journal of Medicine 318, 733-41.
Kudo H, Takeichi O, Makino K, Hatori K, Ogiso B (2018) Expression of silent information regulator 2 homolog 1 (SIRT1) in periapical granulomas. Journal of Oral Science 60, 411-7.
Liebowitz D, Kieff E (1989) Epstein-Barr virus latent membrane protein: induction of B-cell activation antigens and membrane patch formation does not require vimentin. Journal of Virology 63, 4051-4.
Luzuriaga K, Sullivan JL (2010) Infectious mononucleosis. The New England Journal of Medicine 362, 1993-2000.
Makino K, Takeichi O, Hatori K, Imai K, Ochiai K, Ogiso B (2015) Epstein-Barr virus infection in chronically inflamed periapical granulomas. PLoS ONE 10, e0121548.
Mochanko K, Fejes M, Breazavscek DM, Suarez A, Bachmann AE (1979) The relation between Epstein-Barr virus antibodies and clinical symptomatology and immunodeficiency in patients with Hodgkin's disease. Cancer 44, 2065-70.
Pagano JS, Whitehurst CB, Andrei G (2018) Antiviral Drugs for EBV. Cancers 10, e197.
Rasmussen NS, Draborg AH, Nielsen CT, Jacobsen S, Houen G (2015) Antibodies to early EBV, CMV, and HHV6 antigens in systemic lupus erythematosus patients. Scandinavian Journal of Rheumatology 44, 143-9.
Sabeti M, Slots J (2004) Herpesviral-bacterial coinfection in periapical pathosis. Journal of Endodontics 30, 69-72.
Sabeti M, Valles Y, Nowzari H, Simon JH, Kermani-Arab V, Slots J (2003) Cytomegalovirus and Epstein-Barr virus DNA transcription in endodontic symptomatic lesions. Oral Microbiology and Immunology 18, 104-8.
Sabeti M, Kermani V, Sabeti S, Simon JH (2012) Significance of human cytomegalovirus and Epstein-Barr virus in inducing cytokine expression in periapical lesions. Journal of Endodontology 38, 47-50.
Saboia-Dantas CJ, Coutrin de Toledo LF, Sampaio-Filho HR, Siqueira JF Jr (2007) Herpesviruses in asymptomatic apical periodontitis lesions: an immunohistochemical approach. Oral Microbiology and Immunology 22, 320-5.
Schwarzmann F, Jäger M, Hornef M, Prang N, Wolf H (1998) Epstein-Barr viral gene expression in B-lymphocytes. Leukemia and Lymphoma 30, 123-9.
Shimizu N, Takada K (1993) Analysis of the BZLF1 promoter of Epstein-Barr virus: identification of an anti-immunoglobulin response sequence. Journal of Virology 67, 3240-5.
Siqueira JF Jr, Rôças IN (2009) Diversity of endodontic microbiota revisited. Journal of Dental Research 88, 969-81.
Siqueira JF Jr, Rôças IN (2016) Microbiology of endodontic infections. In: Hargreaves KM, Berman LH, eds. Pathways of the pulp, 11th edn. Philadelphia, PA: Elsevier, pp 599-629.
Siqueira JF Jr, Rôças IN, Ricucci D, Hülsmann M (2014) Causes and management of post-treatment apical periodontitis. British Dental Journal 216, 305-12.
Sjögren U, Figdor D, Persson S, Sundqvist G (1997) Influence of infection at the time of root filling on the outcome of endodontic treatment of teeth with apical periodontitis. International Endodontic Journal 30, 297-306.
Sunde PT, Olsen I, Enersen M, Beiske K, Grinde B (2008) Human cytomegalovirus and Epstein-Barr virus in apical and marginal periodontitis: a role in pathology? Journal of Medical Virology 80, 1007-11.
Sundqvist G, Figdor D, Persson S, Sjögren U (1998) Microbiologic analysis of teeth with failed endodontic treatment and the outcome of conservative re-treatment. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology 85, 86-93.
Tabtieng T, Gaglia MM (2018) Emerging Proviral Roles of Caspases during Lytic Replication of Gammaherpesviruses. Journal of Virology 92, e01011-7.
Tedeschi R, Pin E, Martorelli D et al. (2007) Serum antibody response to lytic and latent Epstein-Barr virus antigens in undifferentiated nasopharyngeal carcinoma patients from an area of nonendemicity. Clinical and Vaccine Immunology 14, 435-41.
Tennert C, Fuhrmann M, Wittmer A et al. (2014) New bacterial composition in primary and persistent/secondary endodontic infections with respect to clinical and radiographic findings. Journal of Endodontics 40, 670-7.
Torii Y, Kawada JI, Murata T, Yoshiyama H, Kimura H, Ito Y (2017) Epstein-Barr virus infection-induced inflammasome activation in human monocytes. PLoS ONE 12, e0175053.
Tsai PF, Lin SJ, Weng PL et al. (2011) Interplay between PKCδ and Sp1 on histone deacetylase inhibitor-mediated Epstein-Barr virus reactivation. Journal of Virology 85, 2373-85.
Tsukahara T, Matsukawa N, Tomonaga S, Inoue R, Ushida K, Ochiai K (2014) High-sensitivity detection of short-chain fatty acids in porcine ileal, cecal, portal and abdominal blood by gas chromatography-mass spectrometry. Animal Science Journal 85, 494-8.
Vengerfeldt V, Špilka K, Saag M et al. (2014) Highly diverse microbiota in dental root canals in cases of apical periodontitis (data of illumina sequencing). Journal of Endodontics 40, 1778-83.
Waltimo TM, Sirén EK, Torkko HL, Olsen I, Haapasalo MP (1997) Fungi in therapy-resistant apical periodontitis. International Endodontic Journal 30, 96-101.
Waltimo TM, Sirén EK, Ørstavik D, Haapasalo MP (1999) Susceptibility of oral Candida species to calcium hydroxide in vitro. International Endodontic Journal 32, 94-8.