Oral infection of mice with Fusobacterium nucleatum results in macrophage recruitment to the dental pulp and bone resorption

Dewhirst, 2010, The human oral microbiome, J Bacteriol, 192, 5002, 10.1128/JB.00542-10 Bik, 2010, Bacterial diversity in the oral cavity of 10 healthy individuals, ISME J, 4, 962, 10.1038/ismej.2010.30 Han, 2000, Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells, Infect Immun, 68, 3140, 10.1128/IAI.68.6.3140-3146.2000 Signat, 2011, Fusobacterium nucleatum in periodontal health and disease, Curr Issues Mol Biol, 13, 25 Armitage, 2004, Periodontal diagnoses and classification of periodontal diseases, Periodontology, 34, 9, 10.1046/j.0906-6713.2002.003421.x Silva, 2015, Host response mechanisms in periodontal diseases, J Appl Oral Sci: Revista FOB, 23, 329, 10.1590/1678-775720140259 Arigbede, 2012, Periodontitis and systemic diseases: a literature review, J Indian Soc Periodontol, 16, 487, 10.4103/0972-124X.106878 Hasan, 2014, A clinical guide to periodontology: pathology of periodontal disease, Br Dent J, 216, 457, 10.1038/sj.bdj.2014.299 Karpathy, 2007, Genome sequence of Fusobacterium nucleatum subspecies polymorphum – a genetically tractable fusobacterium, PLoS One, 2, e659, 10.1371/journal.pone.0000659 Al-Ahmad, 2007, The in vivo dynamics of Streptococcus spp., Actinomyces naeslundii, Fusobacterium nucleatum and Veillonella spp. in dental plaque biofilm as analysed by five-colour multiplex fluorescence in situ hybridization, J Med Microbiol, 56, 681, 10.1099/jmm.0.47094-0 Zilm, 2007, Co-adhesion and biofilm formation by Fusobacterium nucleatum in response to growth pH, Anaerobe, 13, 146, 10.1016/j.anaerobe.2007.04.005 Han, 2005, Identification and characterization of a novel adhesin unique to oral fusobacteria, J Bacteriol, 187, 5330, 10.1128/JB.187.15.5330-5340.2005 Tuttle, 1992, A non-lectin-like mechanism by which Fusobacterium nucleatum 10953 adheres to and activates human lymphocytes, Oral Microbiol Immunol, 7, 78, 10.1111/j.1399-302X.1992.tb00513.x Mangan, 1989, Lectinlike interactions of Fusobacterium nucleatum with human neutrophils, Infect Immun, 57, 3601, 10.1128/IAI.57.11.3601-3611.1989 Temoin, 2012, Signal peptide of FadA adhesin from Fusobacterium nucleatum plays a novel structural role by modulating the filament's length and width, FEBS Lett, 586, 1, 10.1016/j.febslet.2011.10.047 Xu, 2007, FadA from Fusobacterium nucleatum utilizes both secreted and nonsecreted forms for functional oligomerization for attachment and invasion of host cells, J Biol Chem, 282, 25000, 10.1074/jbc.M611567200 Martinon, 2002, The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta, Mol Cell, 10, 417, 10.1016/S1097-2765(02)00599-3 Ozaki, 1990, Binding specificity of Fusobacterium nucleatum to human erythrocytes, polymorphonuclear leukocytes, fibroblasts, and HeLa cells, J Periodontal Res, 25, 129, 10.1111/j.1600-0765.1990.tb01034.x Diamond, 2011, Beta-defensins: what are they really doing in the oral cavity?, Oral Dis, 17, 628, 10.1111/j.1601-0825.2011.01799.x Mathews, 1999, Production of beta-defensin antimicrobial peptides by the oral mucosa and salivary glands, Infect Immun, 67, 2740, 10.1128/IAI.67.6.2740-2745.1999 Dale, 2001, Defensin antimicrobial peptides in the oral cavity, J Oral Pathol Med : Off Publ Int Assoc Oral Pathol Am Acad Oral Pathol, 30, 321, 10.1034/j.1600-0714.2001.300601.x Gomes Pde, 2010, Defensins in the oral cavity: distribution and biological role, J Oral Pathol Med: Off Publ Int Assoc Oral Pathol Am Acad Oral Pathol, 39, 1, 10.1111/j.1600-0714.2009.00832.x Rao, 2014, Gingival epithelial cell responses to microbial infections – an overview, J Res Adv Dent, 3, 53 Dale, 2002, Periodontal epithelium: a newly recognized role in health and disease, Periodontology, 30, 70, 10.1034/j.1600-0757.2002.03007.x Laube, 2008, Differential regulation of innate immune response genes in gingival epithelial cells stimulated with Aggregatibacter actinomycetemcomitans, J Periodontal Res, 43, 116 Medzhitov, 2001, Toll-like receptors and innate immunity, Nat Rev Immunol, 1, 135, 10.1038/35100529 Kawai, 2007, Signaling to NF-kappaB by Toll-like receptors, Trends Mol Med, 13, 460, 10.1016/j.molmed.2007.09.002 Kelk, 2008, IL-1beta secretion induced by Aggregatibacter (Actinobacillus) actinomycetemcomitans is mainly caused by the leukotoxin, Int J Medical Microbiol: IJMM, 298, 529, 10.1016/j.ijmm.2007.06.005 Hung, 2017, NLRX1 modulates differentially NLRP3 inflammasome activation and NF-kappaB signaling during Fusobacterium nucleatum infection, Microbes Infect, 1 Bui, 2016, Fusobacterium nucleatum infection of gingival epithelial cells leads to NLRP3 inflammasome-dependent secretion of IL-1β and the danger signals ASC and HMGB1, Cell Microbiol, 18, 970, 10.1111/cmi.12560 Griffin, 2012, IL-17 and TNF-alpha sustain neutrophil recruitment during inflammation through synergistic effects on endothelial activation, J Immunol, 188, 6287, 10.4049/jimmunol.1200385 McGee, 1995, A synergistic relationship between TNF-alpha, IL-1 beta, and TGF-beta 1 on IL-6 secretion by the IEC-6 intestinal epithelial cell line, Immunology, 86, 6 Guilloteau, 2010, Skin inflammation induced by the synergistic action of IL-17A, IL-22, Oncostatin M, IL-1{alpha}, and TNF-{alpha} recapitulates some features of psoriasis, J Immunol, 184, 5263, 10.4049/jimmunol.0902464 Awane, 1999, NF-kappa B-inducing kinase is a common mediator of IL-17-, TNF-alpha-, and IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells, J Immunol, 162, 5337, 10.4049/jimmunol.162.9.5337 Palmqvist, 2008, IL-1beta and TNF-alpha regulate IL-6-type cytokines in gingival fibroblasts, J Dental Res, 87, 558, 10.1177/154405910808700614 Saperstein, 2009, IL-1beta augments TNF-alpha-mediated inflammatory responses from lung epithelial cells, J Interferon Cytokine Res: Off J Int Soc Interferon Cytokine Res, 29, 273, 10.1089/jir.2008.0076 Vignery, 1980, Dynamic histomorphometry of alveolar bone remodeling in the adult rat, Anat Rec, 196, 191, 10.1002/ar.1091960210 Hienz, 2015, Mechanisms of bone resorption in periodontitis, J Immunol Research, 2015, 615486, 10.1155/2015/615486 Soysa, 2012, Osteoclast formation and differentiation: an overview, J Med Dent Sci, 59, 65 Goltzman, 2002, Discoveries, drugs and skeletal disorders, Nat Rev, 1, 784 Boyce, 2005, TNF-alpha and pathologic bone resorption, Keio J Med, 54, 127, 10.2302/kjm.54.127 Hwang, 2011, Calcium signaling in osteoclasts, Biochim Biophys Acta, 1813, 979, 10.1016/j.bbamcr.2010.11.002 Blair, 2005, Osteoclast signalling pathways, Biochem Biophys Res Commun, 328, 728, 10.1016/j.bbrc.2004.11.077 Hayman, 2008, Tartrate-resistant acid phosphatase (TRAP) and the osteoclast/immune cell dichotomy, Autoimmunity, 41, 218, 10.1080/08916930701694667 Lee, 2011, In-vivo-induced antigenic determinants of Fusobacterium nucleatum subsp. nucleatum, Mol Oral Microbiol, 26, 164, 10.1111/j.2041-1014.2010.00594.x Bui, 2016, Fusobacterium nucleatum infection of gingival epithelial cells leads to NLRP3 inflammasome-dependent secretion of IL-1beta and the danger signals ASC and HMGB1, Cell Microbiol, 18, 970, 10.1111/cmi.12560 Kostic, 2013, Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment, Cell Host Microbe, 14, 207, 10.1016/j.chom.2013.07.007 Dharmani, 2011, Fusobacterium nucleatum infection of colonic cells stimulates MUC2 mucin and tumor necrosis factor alpha, Infect Immun, 79, 2597, 10.1128/IAI.05118-11 Zaborina, 1999, Secretion of ATP-utilizing enzymes, nucleoside diphosphate kinase and ATPase, by Mycobacterium bovis BCG: sequestration of ATP from macrophage P2Z receptors?, Mol Microbiol, 31, 1333, 10.1046/j.1365-2958.1999.01240.x Baker, 2000, Heterogeneity of Porphyromonas gingivalis strains in the induction of alveolar bone loss in mice, Oral Microbiol Immunol, 15, 27, 10.1034/j.1399-302x.2000.150105.x Mizraji, 2013, Isolation, processing and analysis of murine gingival cells, JoVE, 77 Ramos-Junior, 2015, A dual role for P2X7 receptor during Porphyromonas gingivalis infection, J Dental Res, 94, 1233, 10.1177/0022034515593465 Liu, 2014, Detection of fusobacterium nucleatum and fadA adhesin gene in patients with orthodontic gingivitis and non-orthodontic periodontal inflammation, PLoS One, 9 Park, 2014, Diverse Toll-like receptors mediate cytokine production by Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans in macrophages, Infect Immun, 82, 1914, 10.1128/IAI.01226-13 Andersson, 2002, HMGB1 as a DNA-binding cytokine, J Leukoc Biol, 72, 1084, 10.1189/jlb.72.6.1084 Lotze, 2005, High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal, Nat Rev Immunol, 5, 331, 10.1038/nri1594 Erlandsson Harris, 2004, Mini-review: the nuclear protein HMGB1 as a proinflammatory mediator, Eur J Immunol, 34, 1503, 10.1002/eji.200424916 Kalinina, 2004, Increased expression of the DNA-binding cytokine HMGB1 in human atherosclerotic lesions: role of activated macrophages and cytokines, Arterioscler Thromb Vasc Biol, 24, 2320, 10.1161/01.ATV.0000145573.36113.8a Lam, 2014, Macrophage depletion abates Porphyromonas gingivalis-induced alveolar bone resorption in mice, J Immunol, 193, 2349, 10.4049/jimmunol.1400853 Vaananen, 2005, Mechanism of osteoclast mediated bone resorption–rationale for the design of new therapeutics, Adv Drug Deliv Rev, 57, 959, 10.1016/j.addr.2004.12.018 Teitelbaum, 2000, Bone resorption by osteoclasts, Science, 289, 1504, 10.1126/science.289.5484.1504 Gao, 2007, IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation, J Clin Investig, 117, 122, 10.1172/JCI30074 Zupan, 2013, Osteoimmunology and the influence of pro-inflammatory cytokines on osteoclasts, Biochem Med, 23, 43, 10.11613/BM.2013.007 Diaz, 2002, Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments, Microbiology, 148, 467, 10.1099/00221287-148-2-467 Saito, 2008, Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis, Oral Microbiol Immunol, 23, 1, 10.1111/j.1399-302X.2007.00380.x Periasamy, 2009, Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva, Infect Immun, 77, 3542, 10.1128/IAI.00345-09 Metzger, 2009, Synergistic pathogenicity of Porphyromonas gingivalis and Fusobacterium nucleatum in the mouse subcutaneous chamber model, J Endod, 35, 86, 10.1016/j.joen.2008.10.015 Johnson, 2015, Porphyromonas gingivalis attenuates ATP-mediated inflammasome activation and HMGB1 release through expression of a nucleoside-diphosphate kinase, Microbes Infect, 17, 369, 10.1016/j.micinf.2015.03.010 Toussi, 2012, The FomA porin from Fusobacterium nucleatum is a Toll-like receptor 2 agonist with immune adjuvant activity, Clin Vaccine Immunol, 19, 1093, 10.1128/CVI.00236-12 Liu, 2007, Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response, J Immunol, 179, 2501, 10.4049/jimmunol.179.4.2501 Quah, 2014, Fusobacterium nucleatum induces cytokine production through Toll-like-receptor-independent mechanism, Int Endod J, 47, 550, 10.1111/iej.12185 Iwasaki, 2011, In situ proliferation and differentiation of macrophages in dental pulp, Cell Tissue Res, 346, 99, 10.1007/s00441-011-1231-5 Mosser, 2008, Activation of murine macrophages Mosser, 2008, Exploring the full spectrum of macrophage activation, Nat Rev Immunol, 8, 958, 10.1038/nri2448 Mosser, 2003, The many faces of macrophage activation, J Leukoc Biol, 73, 209, 10.1189/jlb.0602325 Schroder, 2004, Interferon-gamma: an overview of signals, mechanisms and functions, J Leukoc Biol, 75, 163, 10.1189/jlb.0603252 Kamijo, 1993, Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guerin and subsequent challenge with lipopolysaccharide, J Exp Med, 178, 1435, 10.1084/jem.178.4.1435 Shtrichman, 2001, The role of gamma interferon in antimicrobial immunity, Curr Opin Microbiol, 4, 251, 10.1016/S1369-5274(00)00199-5 Takayanagi, 2000, T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma, Nature, 408, 600, 10.1038/35046102 Boyle, 2003, Osteoclast differentiation and activation, Nature, 423, 337, 10.1038/nature01658 Yago, 2009, IL-17 induces osteoclastogenesis from human monocytes alone in the absence of osteoblasts, which is potently inhibited by anti-TNF-alpha antibody: a novel mechanism of osteoclastogenesis by IL-17, J Cell Biochem, 108, 947, 10.1002/jcb.22326 Kotake, 1999, IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis, J Clin Investig, 103, 1345, 10.1172/JCI5703