Periapical lesions in two inbred strains of rats differing in immunological reactivity.

Albino Oxford rats Dark Agouti rats immune response periapical lesion strain differences

Journal

International endodontic journal
ISSN: 1365-2591
Titre abrégé: Int Endod J
Pays: England
ID NLM: 8004996

Informations de publication

Date de publication:
Jan 2022
Historique:
revised: 25 09 2021
received: 16 05 2021
accepted: 27 09 2021
pubmed: 7 10 2021
medline: 15 12 2021
entrez: 6 10 2021
Statut: ppublish

Résumé

To investigate the influence of strain differences in immune responses on the pathogenesis of experimental periapical lesions in Dark Agouti (DA) and Albino Oxford (AO) inbred strains of rats. Periapical lesions were induced in male DA and AO rats by pulp exposure of the first mandibular right molars to the oral environment. Animals were killed 21 days after pulp exposure. The mandibular jaws were retrieved and prepared for radiographic, pathohistological, immunohistochemical analysis, real-time PCR and flow cytometry. Blood samples and the supernatant of periapical lesions were collected for measurement of cytokines and oxidative stress marker levels. Statistical analysis was performed using the Kruskal-Wallis H and Mann-Whitney U non-parametric tests or parametric One-Way anova and Independent Samples T-test to determine the differences between groups depending on the normality of the data. A significant difference was considered when p values were <.05. DA rats developed significantly larger (p < .05) periapical lesions compared to AO rats as confirmed by radiographic and pathohistological analysis. The immunohistochemical staining intensity for CD3 was significantly greater in periapical lesions of DA rats compared to AO rats (p < .05). In DA rats, periapical lesions had a significantly higher (p < .05) percentage of CD3+ cells compared to AO rats. Also, the percentage of INF-γ, IL-17 and IL-10 CD3+CD4+ cells was significantly higher in DA rats (p < .05). DA rats had a significantly higher Th17/Th10 ratio. RT-PCR expression of IL-1β, INF-γ and IL-17 genes was significantly higher in periapical lesions of DA compared to AO rats (p < .05). The receptor activator of nuclear factor kappa-Β ligand/osteoprotegerin ratio was higher in DA compared to AO rats with periapical lesions (p < .05). Systemic levels of TNF-α and IL-6 were significantly higher in DA compared to AO rats (p < .05). Levels of lipid peroxidation measured as thiobarbituric acid reactive substances and reduced glutathione were significantly higher (p < .05) in the supernatant in the periapical lesions of DA rats. After pulp exposure, DA rats developed much larger periapical lesions compared to AO rats. Genetically determined differences in immunopathology have been demonstrated to be a significant element defining the severity of periapical lesions.

Identifiants

pubmed: 34614243
doi: 10.1111/iej.13638
doi:

Substances chimiques

Bone Density Conservation Agents 0
Tumor Necrosis Factor-alpha 0

Types de publication

Journal Article

Langues

eng

Pagination

64-78

Subventions

Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON 175071
Organisme : Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
ID : ON 175103
Organisme : Faculty of Medical Sciences, University of Kragujevac, Serbia
ID : JP 06/20
Organisme : Faculty of Medical Sciences, University of Kragujevac, Serbia
ID : JP 24/20
Organisme : Faculty of Medical Sciences, University of Kragujevac, Serbia
ID : JP 25/19

Informations de copyright

© 2021 International Endodontic Journal. Published by John Wiley & Sons Ltd.

Références

Álvares, P.R., de Arruda, J.A.A., Oliveira Silva, L.V., da Silva, L.P., do Nascimento, G.J.F., da Silveira, M.M.F. et al. (2018) Immunohistochemical analysis of cyclooxygenase-2 and tumor necrosis factor alpha in periapical lesions. Journal of Endodontics, 44, 1783-1787.
Andrukhov, O., Haririan, H., Bertl, K., Rausch, W.-D., Bantleon, H.-P., Moritz, A. et al. (2013) Nitric oxide production, systemic inflammation and lipid metabolism in periodontitis patients: possible gender aspect. Journal of Clinical Periodontology, 40, 916-923.
Araujo-pires, A.C., Francisconi, C.F., Biguetti, C.C., Cavalla, F., Aranha, A.M.F., Letra, A. et al. (2014) Simultaneous analysis of T helper subsets (Th1, Th2, Th9, Th17, Th22, Tfh, Tr1 and Tregs) markers expression in periapical lesions reveals multiple cytokine clusters accountable for lesions activity and inactivity status. Journal of Applied Oral Science, 22, 336-346.
Belibasakis, G.N., Rechenberg, D.K. & Zehnder, M. (2013) The receptor activator of NF-κB ligand-osteoprotegerin system in pulpal and periapical disease. International Endodontic Journal, 46, 99-111.
Berar, A.M., Bondor, C.I., Matroş, L. & Câmpian, R.S. (2016) Radiological, histological and immunohistochemical evaluation of periapical inflammatory lesions. Romanian Journal of Morphology and Embryology, 57, 419-425.
Berlin-Broner, Y., Alexiou, M., Levin, L. & Febbraio, M. (2020) Characterization of a mouse model to study the relationship between apical periodontitis and atherosclerosis. International Endodontic Journal, 53, 812-823.
Brekalo Pršo, I., Kocjan, W., Šimic, H., Brumini, G., Pezelj-Ribaric, S., Borcic, J. et al. (2007) Tumor necrosis factor-alpha and interleukin 6 in human periapical lesions. Mediators of Inflammation, 2007, 1-4.
de Brito, L.C.N., Teles, F.R.F., Teles, R.P., Totola, A.H., Vieira, L.Q. & Sobrinho, A.P.R. (2012) T-lymphocyte and cytokine expression in human inflammatory periapical lesions. Journal of Endodontics, 38, 481-485.
Cavalla, F., Letra, A., Silva, R.M. & Garlet, G.P. (2021) Determinants of periodontal/periapical lesion stability and progression. Journal of Dental Research, 100, 29-36.
Cintra, L.T.A., Samuel, R.O., Azuma, M.M., de Queiróz, A.O.S., Ervolino, E., Sumida, D.H. et al. (2016) Multiple apical periodontitis influences serum levels of cytokines and nitric oxide. Journal of Endodontics, 42, 747-751.
Colić, M., Gazivoda, D., Majstorović, I., Dragicević, A., Vasilijić, S., Rudolf, R. et al. (2009) Immunomodulatory activity of IL-27 in human periapical lesions. Journal of Dental Research, 88, 1142-1147.
Čolić, M., Gazivoda, D., Vučević, D., Vasilijić, S., Rudolf, R. & Lukić, A. (2009) Proinflammatory and immunoregulatory mechanisms in periapical lesions. Molecular Immunology, 47, 101-113.
Colic, M., Gazivoda, D., Vasilijic, S., Vucevic, D. & Lukic, A. (2010) Production of IL-10 and IL-12 by antigen-presenting cells in periapical lesions. Journal of Oral Pathology & Medicine, 39, 690-696.
Čolić, M., Lukić, A., Vučević, D., Milosavljević, P., Majstorović, I., Marjanović, M. et al. (2006) Correlation between phenotypic characteristics of mononuclear cells isolated from human periapical lesions and their in vitro production of Th1 and Th2 cytokines. Archives of Oral Biology, 51, 1120-1130.
Čolić, M., Vasilijić, S., Gazivoda, D., Vučević, D., Marjanović, M. & Lukić, A. (2007) Interleukin-17 plays a role in exacerbation of inflammation within chronic periapical lesions. European Journal of Oral Sciences, 115, 315-320.
Duka, M., Eraković, M., Dolićanin, Z., Stefanović, D. & Čolić, M. (2019) Production of soluble receptor activator of nuclear factor kappa-Β ligand and osteoprotegerin by apical periodontitis cells in culture and their modulation by cytokines. Mediators of Inflammation, 2019, 1-11.
Garlet, G.P. (2010) Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. Journal of Dental Research, 89, 1349-1363.
Graves, D.T., Oates, T. & Garlet, G.P. (2011) Review of osteoimmunology and the host response in endodontic and periodontal lesions. Journal of Oral Microbiology, 3, 5304.
Hernández-Ríos, P., Pussinen, P.J., Vernal, R. & Hernández, M. (2017) Oxidative stress in the local and systemic events of apical periodontitis. Frontiers in Physiology, 8, 869.
Jakovljevic, A., Andric, M., Nikolic, N., Coric, V., Krezovic, S., Carkic, J. et al. (2018) Levels of oxidative stress biomarkers and bone resorption regulators in apical periodontitis lesions infected by Epstein-Barr virus. International Endodontic Journal, 51, 593-604.
Kawashima, N., Suzuki, N., Yang, G., Ohi, C., Okuhara, S., Nakano-Kawanishi, H. et al. (2007) Kinetics of RANKL, RANK and OPG expressions in experimentally induced rat periapical lesions. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, 103, 707-711.
Kitaura, H., Marahleh, A., Ohori, F., Noguchi, T., Shen, W.-R., Qi, J. et al. (2020) Osteocyte-related cytokines regulate osteoclast formation and bone resorption. International Journal of Molecular Sciences, 21, 5169.
Leite, M.F., De Lima, A., Massuyama, M.M. & Otton, R. (2010) In vivo astaxanthin treatment partially prevents antioxidant alterations in dental pulp from alloxan-induced diabetic rats. International Endodontic Journal, 43, 959-967.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408.
Loos, B.G. & Van Dyke, T.E. (2020) The role of inflammation and genetics in periodontal disease. Periodontology 2000, 83, 26-39.
Love, R.M. & Firth, N. (2009) Histopathological profile of surgically removed persistent periapical radiolucent lesions of endodontic origin. International Endodontic Journal, 42, 198-202.
Lukic, A., Vasilijic, S., Majstorovic, I., Vucevic, D., Mojsilovic, S., Gazivoda, D. et al. (2006) Characterization of antigen-presenting cells in human apical periodontitis lesions by flow cytometry and immunocytochemistry. International Endodontic Journal, 39, 626-636.
Lukić, M., Mostarica-Stojković, M., Kostić, M., Tucić, N. & Vukmanović, S. (1987) Cellular and genetic basis of the strain differences in IL-2 production in rats. Transplantation Proceedings, 19, 3137-3139.
Marahleh, A., Kitaura, H., Ohori, F., Kishikawa, A., Ogawa, S., Shen, W.-R. et al. (2019) TNF-α directly enhances osteocyte RANKL expression and promotes osteoclast formation. Frontiers in Immunology, 10, 2925.
Markovic, M., Miljkovic, D., Momcilovic, M., Popadic, D., Miljkovic, Z., Savic, E. et al. (2009) Strain difference in susceptibility to experimental autoimmune encephalomyelitis in rats correlates with T(H)1 and T(H)17-inducing cytokine profiles. Molecular Immunology, 47, 141-146.
Menezes, R., Garlet, T.P., Letra, A., Bramante, C.M., Campanelli, A.P., Figueira, R.D.C. et al. (2008) Differential patterns of receptor activator of nuclear factor kappa B ligand/osteoprotegerin expression in human periapical granulomas: possible association with progressive or stable nature of the lesions. Journal of Endodontics, 34, 932-938.
Mensah-Brown, E.P., Shahin, A., Al Shamisi, M. & Lukic, M.L. (2011) Early influx of macrophages determines susceptibility to experimental allergic encephalomyelitis in Dark Agouti (DA) rats. Journal of Neuroimmunology, 232, 68-74.
Metzger, Z., Klein, H., Klein, A. & Tagger, M. (2002) Periapical lesion development in rats inhibited by dexamethasone. Journal of Endodontics, 28, 643-645.
Morsani, J.M., Aminoshariae, A., Han, Y.W., Montagnese, T.A. & Mickel, A. (2011) Genetic predisposition to persistent apical periodontitis. Journal of Endodontics, 37, 455-459.
Mostarica-Stojković, M., Petrović, M. & Lukić, M.L. (1982) Resistance to the induction of EAE in AO rats: its prevention by the pre-treatment with cyclophosphamide or low dose of irradiation. Clinical and Experimental Immunology, 50, 311-317.
Nagendrababu, V., Kishen, A., Murray, P.E., Nekoofar, M.H., Figueiredo, J.A.P., Priya, E. et al. (2021) PRIASE 2021 guidelines for reporting animal studies in Endodontology: a consensus-based development. International Endodontic Journal, 54, 848-857.
Nibali, L., Di Iorio, A., Tu, Y.-K. & Vieira, A.R. (2017) Host genetics role in the pathogenesis of periodontal disease and caries. Journal of Clinical Periodontology, 44, S52-S78.
Oseko, F., Yamamoto, T., Akamatsu, Y., Kanamura, N., Iwakura, Y., Imanishi, J. et al. (2009) IL-17 is involved in bone resorption in mouse periapical lesions. Microbiology and Immunology, 53, 287-294.
Peterson, J.D., Herzenberg, L.A., Vasquez, K. & Waltenbaugh, C. (1998) Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proceedings of the National Academy of Sciences of the United States of America, 95, 3071-3076.
Radonjic, T., Rankovic, M., Ravic, M., Zivkovic, V., Srejovic, I., Jeremic, J. et al. (2020) The effects of thiamine hydrochloride on cardiac function, redox status and morphometric alterations in doxorubicin-treated rats. Cardiovascular Toxicology, 20, 111-120.
Sarıtekin, E., Üreyen Kaya, B., Aşcı, H. & Özmen, Ö. (2019) Anti-inflammatory and antiresorptive functions of melatonin on experimentally induced periapical lesions. International Endodontic Journal, 52, 1466-1478.
Sasaki, H., Hirai, K., Martins, C.M., Furusho, H., Battaglino, R. & Hashimoto, K. (2016) Interrelationship between periapical lesion and systemic metabolic disorders. Current Pharmaceutical Design, 22, 2204-2215.
Sato, K., Suematsu, A., Okamoto, K., Yamaguchi, A., Morishita, Y., Kadono, Y. et al. (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. The Journal of Experimental Medicine, 203, 2673-2682.
Segura-Egea, J.J., Martín-González, J. & Castellanos-Cosano, L. (2015) Endodontic medicine: connections between apical periodontitis and systemic diseases. International Endodontic Journal, 48, 933-951.
Silva, M.J.B., Kajiya, M., AlShwaimi, E., Sasaki, H., Hong, J., Ok, P. et al. (2012) Bacteria-reactive immune response may induce RANKL-expressing T cells in the mouse periapical bone loss lesion. Journal of Endodontics, 38, 346-350.
Stankovic, M., Ljujic, B., Babic, S., Maravic-Stojkovic, V., Mitrovic, S., Arsenijevic, N. et al. (2019) IL-33/IL-33R in various types of carotid artery atherosclerotic lesions. Cytokine, 120, 242-250.
Taira, T.M., Lima, V., Prado, D.S., Silva, T.A., Issa, J., da Silva, L. et al. (2019) NLRP12 attenuates inflammatory bone loss in experimental apical periodontitis. Journal of Dental Research, 98, 476-484.
Tani-Ishii, N., Wang, C.-Y., Tanner, A. & Stashenko, P. (1994) Changes in root canal microbiota during the development of rat periapical lesions. Oral Microbiology and Immunology, 9, 129-135.
Velickovic, M., Pejnovic, N., Mitrovic, S., Radosavljevic, G., Jovanovic, I., Kanjevac, T. et al. (2015) ST2 deletion increases inflammatory bone destruction in experimentally induced periapical lesions in mice. Journal of Endodontics, 41, 369-375.
Wang, C.Y. & Stashenko, P. (1991) Kinetics of bone-resorbing activity in developing periapical lesions. Journal of Dental Research, 70, 1362-1366.
Wu, S.C., Ma, X.X., Zhang, Z.Y., Lo, E., Wang, X., Wang, B. et al. (2021) Ethnic disparities in dental caries among adolescents in China. Journal of Dental Research, 100, 496-506.
Xiao, L., Zhu, L., Yang, S., Lei, D., Xiao, Y. & Peng, B. (2015) Different correlation of sphingosine-1-phosphate receptor 1 with receptor activator of nuclear factor kappa B ligand and regulatory T cells in rat periapical lesions. Journal of Endodontics, 41, 479-486.
Xiong, B., Shirai, K., Matsumoto, K., Abiko, Y. & Furuichi, Y. (2021) The potential of a surface pre-reacted glass root canal dressing for treating apical periodontitis in rats. International Endodontic Journal, 54, 255-267.

Auteurs

Suzana Zivanovic (S)

Department of Dentistry, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Milos Papic (M)

Department of Dentistry, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Tamara Vucicevic (T)

Department of Dentistry, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Marina Miletic Kovacevic (M)

Department of Histology and Embryology, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Nemanja Jovicic (N)

Department of Histology and Embryology, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Nadja Nikolic (N)

Department of Biology and Human Genetics, School of Dental Medicine, University of Belgrade, Belgrade, Serbia.

Jelena Milasin (J)

Department of Biology and Human Genetics, School of Dental Medicine, University of Belgrade, Belgrade, Serbia.

Verica Paunovic (V)

Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.

Vladimir Trajkovic (V)

Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.

Slobodanka Mitrovic (S)

Department of Pathology, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Miodrag L Lukic (ML)

Center for Molecular Medicine and Stem Cell Research, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Aleksandra Lukic (A)

Department of Dentistry, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

Biljana Ljujic (B)

Department of Genetics, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.

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