{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T18:26:38Z","timestamp":1787509598690,"version":"build-2736575974"},"reference-count":78,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2024,10,5]],"date-time":"2024-10-05T00:00:00Z","timestamp":1728086400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"German Academic Exchange Service","award":["57589445"],"award-info":[{"award-number":["57589445"]}]},{"name":"German Academic Exchange Service","award":["1593\/5-1"],"award-info":[{"award-number":["1593\/5-1"]}]},{"name":"German Research Foundation","award":["57589445"],"award-info":[{"award-number":["57589445"]}]},{"name":"German Research Foundation","award":["1593\/5-1"],"award-info":[{"award-number":["1593\/5-1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>To better understand the link between periodontitis and metabolic diseases, our in vitro study aimed to assess the influence of the adipokine apelin and\/or the periodontal pathogen Fusobacterium nucleatum on periodontal cells. Periodontal ligament (PDL) cells were exposed to F. nucleatum in the presence and absence of apelin. Scratch assays were used to analyze the in vitro wound healing and velocity of cell migration. To investigate if F. nucleatum and\/or apelin have a regulatory effect on cell proliferation and apoptosis, proliferation and viability assays were performed as well as an analysis of caspase 9 expression. Both the in vitro wound closure and the cell migration rate were significantly reduced by F. nucleatum. Simultaneous incubation with apelin counteracted the adverse effects of F. nucleatum. The proliferation assay demonstrated that neither apelin nor F. nucleatum significantly affected PDL cell proliferation. Furthermore, neither apelin nor F. nucleatum was cytotoxic or affected apoptosis after 48 h. Apelin could play a modulatory role in the pathogenesis of periodontitis, as it was able to compensate for the inhibitory effects of the periodontal pathogen F. nucleatum on PDL cell migration in vitro.<\/jats:p>","DOI":"10.3390\/ijms251910729","type":"journal-article","created":{"date-parts":[[2024,10,7]],"date-time":"2024-10-07T06:23:18Z","timestamp":1728282198000},"page":"10729","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Apelin Counteracts the Effects of Fusobacterium nucleatum on the Migration of Periodontal Ligament Cells In Vitro"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0009-0006-8257-077X","authenticated-orcid":false,"given":"Pablo","family":"Cores Ziskoven","sequence":"first","affiliation":[{"name":"Department of Periodontology and Operative Dentistry, University Medical Center of the Johannes Gutenberg University, 55131 Mainz, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2756-5947","authenticated-orcid":false,"given":"Andressa V. B.","family":"Nogueira","sequence":"additional","affiliation":[{"name":"Department of Periodontology and Operative Dentistry, University Medical Center of the Johannes Gutenberg University, 55131 Mainz, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4619-2461","authenticated-orcid":false,"given":"Sigrun","family":"Eick","sequence":"additional","affiliation":[{"name":"Department of Periodontology, School of Dental Medicine, University of Bern, 3010 Bern, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Deschner","sequence":"additional","affiliation":[{"name":"Department of Periodontology and Operative Dentistry, University Medical Center of the Johannes Gutenberg University, 55131 Mainz, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S173","DOI":"10.1002\/JPER.17-0721","article-title":"Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions","volume":"89","author":"Papapanou","year":"2018","journal-title":"J. Periodontol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1038\/nrmicro2873","article-title":"The keystone-pathogen hypothesis","volume":"10","author":"Hajishengallis","year":"2012","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.it.2013.09.001","article-title":"Immunomicrobial pathogenesis of periodontitis: Keystones, pathobionts, and host response","volume":"35","author":"Hajishengallis","year":"2013","journal-title":"Trends Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1111\/prd.12085","article-title":"Periodontal herpesviruses: Prevalence, pathogenicity, systemic risk","volume":"69","author":"Slots","year":"2015","journal-title":"Periodontology 2000"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"105138","DOI":"10.1016\/j.jdent.2024.105138","article-title":"Candida species in periodontitis: A new villain or a new target?","volume":"148","author":"Hu","year":"2024","journal-title":"J. Dent."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Quadri, M.F.A., Kamel, A.M., Nayeem, M., John, T., Thacheril, A., Tartaglia, G., and Tadakamadla, S. (2024). Smokeless tobacco and periodontitis: A systematic review with meta-analysis. J. Periodontal Res.","DOI":"10.1111\/jre.13274"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1016\/j.amepre.2018.02.014","article-title":"Effect of Smoking on Periodontitis: A Systematic Review and Meta-regression","volume":"54","author":"Leite","year":"2018","journal-title":"Am. J. Prev. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/jre.12639","article-title":"Is the use of Cannabis associated with periodontitis? A systematic review and meta-analysis","volume":"54","author":"Chisini","year":"2019","journal-title":"J. Periodontal Res."},{"key":"ref_9","first-page":"dyw021\u201343","article-title":"The effects of waterpipe tobacco smoking on health outcomes: An updated systematic review and meta-analysis: Table 1","volume":"46","author":"Waziry","year":"2016","journal-title":"Leuk. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1111\/jcpe.12556","article-title":"Alcohol consumption and risk of periodontitis: A meta-analysis","volume":"43","author":"Wang","year":"2016","journal-title":"J. Clin. Periodontol."},{"key":"ref_11","first-page":"144","article-title":"Effect of anxiety and psychologic stress on periodontal health: A systematic review and meta-analysis","volume":"53","author":"Aggarwal","year":"2022","journal-title":"Quintessence Int."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1111\/prd.12381","article-title":"The psychobiological links between chronic stress-related diseases, periodontal\/peri-implant diseases, and wound healing","volume":"87","author":"Decker","year":"2021","journal-title":"Periodontology 2000"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1902\/jop.2001.72.4.495","article-title":"The Effect of Occlusal Discrepancies on Periodontitis. II. Relationship of Occlusal Treatment to the Progression of Periodontal Disease","volume":"72","author":"Harrel","year":"2001","journal-title":"J. Periodontol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"12","DOI":"10.2174\/1871530316666160107111301","article-title":"The Gender Bender effect in Periodontal Immune Response","volume":"16","author":"Grover","year":"2016","journal-title":"Endocrine, Metab. Immune Disord.-Drug Targets"},{"key":"ref_15","first-page":"17","article-title":"The Effects of Patient Compliance in Supportive Periodontal Therapy on Tooth Loss: A systematic Review and Meta-analysis","volume":"23","author":"Campos","year":"2021","journal-title":"J. Int. Acad. Periodontol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1111\/cdoe.12278","article-title":"Socioeconomic position during life and periodontitis in adulthood: A systematic review","volume":"45","author":"Schuch","year":"2016","journal-title":"Community Dent. Oral Epidemiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1111\/j.1600-0757.2011.00415.x","article-title":"Genetic susceptibility to periodontitis","volume":"58","author":"Laine","year":"2011","journal-title":"Periodontology 2000"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1111\/j.1600-051X.2005.00806.x","article-title":"Identification of genetic risk factors for periodontitis and possible mechanisms of action","volume":"32","author":"Loos","year":"2005","journal-title":"J. Clin. Periodontol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1111\/prd.12453","article-title":"Influence of epigenetics on periodontitis and peri-implantitis pathogenesis","volume":"90","author":"Larsson","year":"2022","journal-title":"Periodontology 2000"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/prd.12000","article-title":"Modifiable risk factors in periodontal disease","volume":"64","author":"Barros","year":"2013","journal-title":"Periodontology 2000"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1111\/prd.12297","article-title":"The role of inflammation and genetics in periodontal disease","volume":"83","author":"Loos","year":"2020","journal-title":"Periodontology 2000"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1111\/jcpe.12534","article-title":"Clinical research activity in periodontal medicine: A systematic mapping of trial registers","volume":"43","author":"Monsarrat","year":"2016","journal-title":"J. Clin. Periodontol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/j.1469-0691.2007.01798.x","article-title":"Relationship between periodontal infections and systemic disease","volume":"13","author":"Seymour","year":"2007","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Liccardo, D., Cannavo, A., Spagnuolo, G., Ferrara, N., Cittadini, A., Rengo, C., and Rengo, G. (2019). Periodontal Disease: A Risk Factor for Diabetes and Cardiovascular Disease. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20061414"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.jdsr.2023.08.002","article-title":"Periodontitis and periodontopathic bacteria as risk factors for rheumatoid arthritis: A review of the last 10 years","volume":"59","author":"Kobayashi","year":"2023","journal-title":"Jpn. Dent. Sci. Rev."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/s00125-011-2342-y","article-title":"Periodontitis and diabetes: A two-way relationship","volume":"55","author":"Preshaw","year":"2012","journal-title":"Diabetologia"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5557","DOI":"10.1007\/s00784-022-04583-x","article-title":"Association between components of metabolic syndrome and periodontitis: A systematic review and meta-analysis","volume":"26","author":"Campos","year":"2022","journal-title":"Clin. Oral Investig."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1038\/nri2921","article-title":"Adipokines in inflammation and metabolic disease","volume":"11","author":"Ouchi","year":"2011","journal-title":"Nat. Rev. Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1111\/omi.12070","article-title":"The role of adipokines in periodontal infection and healing","volume":"29","author":"Deschner","year":"2014","journal-title":"Mol. Oral Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.ando.2016.01.001","article-title":"New adipokines","volume":"77","author":"Bastard","year":"2016","journal-title":"Ann. d\u2019Endocrinologie"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Clemente-Su\u00e1rez, V.J., Redondo-Fl\u00f3rez, L., Beltr\u00e1n-Velasco, A.I., Mart\u00edn-Rodr\u00edguez, A., Mart\u00ednez-Guardado, I., Navarro-Jim\u00e9nez, E., Laborde-C\u00e1rdenas, C.C., and Tornero-Aguilera, J.F. (2023). The Role of Adipokines in Health and Disease. Biomedicines, 11.","DOI":"10.3390\/biomedicines11051290"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/j.tips.2015.04.014","article-title":"Adipokines in health and disease","volume":"36","author":"Fasshauer","year":"2015","journal-title":"Trends Pharmacol. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1007\/s00394-012-0370-0","article-title":"The role of adipokines in connective tissue diseases","volume":"51","author":"Krysiak","year":"2012","journal-title":"Eur. J. Nutr."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Kraus, D., Winter, J., Jepsen, S., J\u00e4ger, A., Meyer, R., and Deschner, J. (2012). Interactions of Adiponectin and Lipopolysaccharide from Porphyromonas gingivalis on Human Oral Epithelial Cells. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030716"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2014\/796565","article-title":"Beneficial Effects of Adiponectin on Periodontal Ligament Cells under Normal and Regenerative Conditions","volume":"2014","author":"Nokhbehsaim","year":"2014","journal-title":"J. Diabetes Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2020\/9817095","article-title":"Resistin Is Increased in Periodontal Cells and Tissues: In Vitro and In Vivo Studies","volume":"2020","author":"Nogueira","year":"2020","journal-title":"Mediat. Inflamm."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s00784-013-0935-1","article-title":"Regulation of visfatin by microbial and biomechanical signals in PDL cells","volume":"18","author":"Nogueira","year":"2013","journal-title":"Clin. Oral Investig."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Nogueira, A.V.B., Nokhbehsaim, M., Damanaki, A., Eick, S., Kirschneck, C., Schr\u00f6der, A., Jantsch, J., and Deschner, J. (2021). Filifactor alocis and Tumor Necrosis Factor-Alpha Stimulate Synthesis of Visfatin by Human Macrophages. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22031235"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2014\/180304","article-title":"Leptin Effects on the Regenerative Capacity of Human Periodontal Cells","volume":"2014","author":"Nokhbehsaim","year":"2014","journal-title":"Int. J. Endocrinol."},{"key":"ref_40","first-page":"1","article-title":"Stimulation of MMP-1 and CCL2 by NAMPT in PDL Cells","volume":"2013","author":"Nokhbehsaim","year":"2013","journal-title":"Mediat. Inflamm."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"182","DOI":"10.4103\/AIHB.AIHB_84_20","article-title":"Expression of apelin among the individuals of chronic periodontitis, with and without type ii diabetes mellitus: A study using enzyme-linked immunosorbent assay","volume":"10","author":"Kumar","year":"2020","journal-title":"Adv. Hum. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"135","DOI":"10.36295\/ASRO.2020.23118","article-title":"Changes of Salivary Interleukine-17, Apelin, Omentin and Vaspin Levels in Normal Subjects and Diabetic Patients with Chronic periodontitis","volume":"23","author":"Sarhat","year":"2020","journal-title":"Ann. Trop. Med. Pub. Health"},{"key":"ref_43","first-page":"1","article-title":"Gingival crevicular fluid levels of apelin correlates with clinical periodontal diagnosis","volume":"28","author":"Nogueira","year":"2023","journal-title":"Clin. Oral Investig."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Ziskoven, P.C., Nogueira, A.V.B., Gutierrez, L.S., Weusmann, J., Eick, S., Buduneli, N., and Deschner, J. (2023). Apelin Enhances the Effects of Fusobacterium nucleatum on Periodontal Ligament Cells In Vitro. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24054733"},{"key":"ref_45","first-page":"417","article-title":"Apelin\u2014A New Kid on the Block in Periodontology","volume":"22","author":"Ziskoven","year":"2024","journal-title":"Oral Health Prev. Dent."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1034\/j.1600-0757.2000.2220104.x","article-title":"Biology of wound healing","volume":"22","author":"Aukhil","year":"2000","journal-title":"Periodontology 2000"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1034\/j.1600-0757.2000.2240107.x","article-title":"Cell biology of gingival wound healing","volume":"24","author":"Uitto","year":"2000","journal-title":"Periodontology 2000"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2014\/638936","article-title":"Obesity and Surgical Wound Healing: A Current Review","volume":"2014","author":"Pierpont","year":"2014","journal-title":"ISRN Obes."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Alma, A., Marconi, G.D., Rossi, E., Magnoni, C., and Paganelli, A. (2023). Obesity and Wound Healing: Focus on Mesenchymal Stem Cells. Life, 13.","DOI":"10.3390\/life13030717"},{"key":"ref_50","first-page":"84","article-title":"Factors That Impair Wound Healing","volume":"4","author":"Anderson","year":"2012","journal-title":"J. Am. Coll. Clin. Wound Spe\u00e9c."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1111\/prd.12326","article-title":"The association of periodontal diseases with metabolic syndrome and obesity","volume":"83","author":"Jepsen","year":"2020","journal-title":"Periodontology 2000"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1007\/s00784-010-0505-8","article-title":"Anti-inflammatory effects of EMD in the presence of biomechanical loading and interleukin-1\u03b2 in vitro","volume":"16","author":"Nokhbehsaim","year":"2011","journal-title":"Clin. Oral Investig."},{"key":"ref_53","first-page":"CD003875","article-title":"Enamel matrix derivative (Emdogain\u00ae) for periodontal tissue regeneration in intrabony defects","volume":"2009","author":"Esposito","year":"2009","journal-title":"Cochrane Database Syst. Rev."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1902\/annals.2003.8.1.193","article-title":"Growth and Amelogenin-Like Factors in Periodontal Wound Healing. A Systematic Review","volume":"8","author":"Giannobile","year":"2003","journal-title":"Ann. Periodontol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1902\/jop.2005.76.9.1601","article-title":"Periodontal regeneration","volume":"76","author":"Wang","year":"2005","journal-title":"J. Periodontol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1007\/s00784-011-0570-7","article-title":"Human periodontal ligament fibroblasts stimulated by nanocrystalline hydroxyapatite paste or enamel matrix derivative. An in vitro assessment of PDL attachment, migration, and proliferation","volume":"16","author":"Kasaj","year":"2011","journal-title":"Clin. Oral Investig."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1034\/j.1600-051X.1999.260109.x","article-title":"Effects of nicotine on periodontal ligament fibroblasts in vitro","volume":"26","author":"Giannopoulou","year":"1999","journal-title":"J. Clin. Periodontol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Ramenzoni, L.L., Russo, G., Moccia, M.D., Attin, T., and Schmidlin, P.R. (2019). Periodontal bacterial supernatants modify differentiation, migration and inflammatory cytokine expression in human periodontal ligament stem cells. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0219181"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"3203","DOI":"10.1242\/jcs.036525","article-title":"Mechanisms of collective cell migration at a glance","volume":"122","author":"Ilina","year":"2009","journal-title":"J. Cell Sci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1593\/neo.06280","article-title":"CCL2 is a Potent Regulator of Prostate Cancer Cell Migration and Proliferation","volume":"8","author":"Loberg","year":"2006","journal-title":"Neoplasia"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1111\/jop.12869","article-title":"CCL2 promotes cell migration by inducing epithelial-mesenchymal transition in oral squamous cell carcinoma","volume":"48","author":"Ling","year":"2019","journal-title":"J. Oral Pathol. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.cyto.2016.02.001","article-title":"Effect of CCL2 on BV2 microglial cell migration: Involvement of probable signaling pathways","volume":"81","author":"Bose","year":"2016","journal-title":"Cytokine"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1111\/prd.12079","article-title":"In vitro models for evaluation of periodontal wound healing\/regeneration","volume":"68","author":"Weinreb","year":"2015","journal-title":"Periodontology 2000"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.2174\/1570159X20666220327222921","article-title":"Inhibition of Caspase 3 and Caspase 9 Mediated Apoptosis: A Multimodal Therapeutic Target in Traumatic Brain Injury","volume":"21","author":"Unnisa","year":"2023","journal-title":"Curr. Neuropharmacol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/j.bbrc.2008.02.008","article-title":"A putative role for apelin in the etiology of obesity","volume":"368","author":"Rayalam","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2015\/976847","article-title":"Apelin Protects Primary Rat Retinal Pericytes from Chemical Hypoxia-Induced Apoptosis","volume":"2015","author":"Chen","year":"2015","journal-title":"J. Ophthalmol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Chen, Y., Shi, T., Li, Y., Huang, L., and Yin, D. (2022). Fusobacterium nucleatum: The Opportunistic Pathogen of Periodontal and Peri-Implant Diseases. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.860149"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/prd.12296","article-title":"The role of the microbiota in periodontal disease","volume":"83","author":"Curtis","year":"2020","journal-title":"Periodontology 2000"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.tice.2019.01.003","article-title":"Apelin receptor (Aplnr) signaling promotes fibroblast migration","volume":"56","year":"2019","journal-title":"Tissue Cell"},{"key":"ref_70","first-page":"10711","article-title":"Apelin induces the proliferation, migration and expression of cytoskeleton and tight junction proteins in human RPE cells via PI-3K\/Akt and MAPK\/Erk signaling pathways","volume":"10","author":"Li","year":"2017","journal-title":"Int. J. Clin. Exp. Pathol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.jare.2023.04.007","article-title":"The exoprotein Gbp of Fusobacterium nucleatum promotes THP-1 cell lipid deposition by binding to CypA and activating PI3K-AKT\/MAPK\/NF-\u03baB pathways","volume":"57","author":"Shen","year":"2024","journal-title":"J. Adv. Res."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41368-022-00213-0","article-title":"Study of the inflammatory activating process in the early stage of Fusobacterium nucleatum infected PDLSCs","volume":"15","author":"Wang","year":"2023","journal-title":"Int. J. Oral Sci."},{"key":"ref_73","first-page":"151648","article-title":"CXCL5, CXCL8, and CXCL10 regulation by bacteria and mechanical forces in periodontium","volume":"234","author":"Memmert","year":"2020","journal-title":"Ann. Anat.\u2014Anat. Anz."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2019\/7810320","article-title":"Fusobacterium nucleatumFacilitates Apoptosis, ROS Generation, and Inflammatory Cytokine Production by Activating AKT\/MAPK and NF-\u03baB Signaling Pathways in Human Gingival Fibroblasts","volume":"2019","author":"Kang","year":"2019","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Rath-Deschner, B., Nogueira, A.V.B., Memmert, S., Nokhbehsaim, M., Cirelli, J.A., Eick, S., Miosge, N., Kirschneck, C., Kesting, M., and Deschner, J. (2021). Regulation of Anti-Apoptotic SOD2 and BIRC3 in Periodontal Cells and Tissues. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22020591"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1177\/0022034514559128","article-title":"The Pathology of Bone Tissue during Peri-Implantitis","volume":"94","author":"Schminke","year":"2014","journal-title":"J. Dent. Res."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 Years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Suarez-Arnedo, A., Figueroa, F.T., Clavijo, C., Arbel\u00e1ez, P., Cruz, J.C., and Mu\u00f1oz-Camargo, C. (2020). An image J plugin for the high throughput image analysis of in vitro scratch wound healing assays. PLoS ONE, 15.","DOI":"10.1101\/2020.04.20.050831"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/19\/10729\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:11:08Z","timestamp":1760112668000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/19\/10729"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,5]]},"references-count":78,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["ijms251910729"],"URL":"https:\/\/doi.org\/10.3390\/ijms251910729","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,5]]}}}