Protective Actions in Apical Periodontitis: The Regenerative Bioactivities Led by Mesenchymal Stem Cells
Abstract
:1. Introduction
2. The Pathogenic Factors of the Periapical Microbial Community
3. Components Related to Inflammatory Bone Loss
3.1. RANKL/RANK/OPG System
3.2. Neutrophils
3.3. Macrophages
3.4. T Cells
3.5. Mast Cells
4. The Regulatory Network of Dental MSCs in AP
4.1. Orofacial Bone/Bone-Marrow-Derived MSCs (OMSCs)
4.2. Stem Cells from Apical Papilla (SCAPs)
4.3. Dental Follicle Progenitor Cells (DFPCs)
5. The Immunoregulatory Functions of Other Dental MSCs
5.1. Dental Pulp Stem Cells (DPSCs)
5.2. Stem Cells from Human Exfoliated Deciduous Teeth (SHEDs)
5.3. Gingival Mesenchymal Stem Cells (GMSCs)
5.4. Periodontal Ligament Stem Cells (PDLSCs)
6. MSC-Based Treatment for Apical Periodontitis
6.1. MSC-Based Regenerative Endodontics
6.2. Treatment Based on Extracellular Vesicles
6.3. The Aid of Dentine Extracellular Matrix Proteins in MSC-Based Therapies
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Tiburcio-Machado, C.S.; Michelon, C.; Zanatta, F.B.; Gomes, M.S.; Marin, J.A.; Bier, C.A. The global prevalence of apical periodontitis: A systematic review and meta-analysis. Int. Endod. J. 2021, 54, 712–735. [Google Scholar] [CrossRef] [PubMed]
- Buonavoglia, A.; Latronico, F.; Pirani, C.; Greco, M.F.; Corrente, M.; Prati, C. Symptomatic and asymptomatic apical periodontitis associated with red complex bacteria: Clinical and microbiological evaluation. Odontology 2013, 101, 84–88. [Google Scholar] [CrossRef] [PubMed]
- Gazivoda, D.; Dzopalic, T.; Bozic, B.; Tatomirovic, Z.; Brkic, Z.; Colic, M. Production of proinflammatory and immunoregulatory cytokines by inflammatory cells from periapical lesions in culture. J. Oral. Pathol. Med. 2009, 38, 605–611. [Google Scholar] [CrossRef] [PubMed]
- Márton, I.J.; Kiss, C. Overlapping protective and destructive regulatory pathways in apical periodontitis. J. Endod. 2014, 40, 155–163. [Google Scholar] [CrossRef] [PubMed]
- Lyu, P.; Li, B.; Li, P.; Bi, R.; Cui, C.; Zhao, Z.; Zhou, X.; Fan, Y. Parathyroid Hormone 1 Receptor Signaling in Dental Mesenchymal Stem Cells: Basic and Clinical Implications. Front. Cell Dev. Biol. 2021, 9, 654715. [Google Scholar] [CrossRef] [PubMed]
- Zhou, L.L.; Liu, W.; Wu, Y.M.; Sun, W.L.; Dörfer, C.E.; Fawzy El-Sayed, K.M. Oral Mesenchymal Stem/Progenitor Cells: The Immunomodulatory Masters. Stem Cells Int. 2020, 2020, 1327405. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, Y.; Xie, J.; Fu, Y.; Li, C.; Zheng, L.; Huang, D.; Zhou, C.; Sun, J.; Zhou, X. Berberine mediates root remodeling in an immature tooth with apical periodontitis by regulating stem cells from apical papilla differentiation. Int. J. Oral. Sci. 2020, 12, 18. [Google Scholar] [CrossRef]
- Chrepa, V.; Pitcher, B.; Henry, M.A.; Diogenes, A. Survival of the Apical Papilla and Its Resident Stem Cells in a Case of Advanced Pulpal Necrosis and Apical Periodontitis. J. Endod. 2017, 43, 561–567. [Google Scholar] [CrossRef]
- Liu, X.M.; Liu, Y.; Yu, S.; Jiang, L.M.; Song, B.; Chen, X. Potential immunomodulatory effects of stem cells from the apical papilla on Treg conversion in tissue regeneration for regenerative endodontic treatment. Int. Endod. J. 2019, 52, 1758–1767. [Google Scholar] [CrossRef]
- Li, M.; Wei, L.; Zhou, W.; He, Z.; Ran, S.; Liang, J. miR-200a contributes to the migration of BMSCs induced by the secretions of E. faecalis via FOXJ1/NFκB/MMPs axis. Stem Cell Res. Ther. 2020, 11, 317. [Google Scholar] [CrossRef]
- Xiao, L.; Zhou, Y.; Zhu, L.; Yang, S.; Huang, R.; Shi, W.; Peng, B.; Xiao, Y. SPHK1-S1PR1-RANKL Axis Regulates the Interactions Between Macrophages and BMSCs in Inflammatory Bone Loss. J. Bone Miner. Res. 2018, 33, 1090–1104. [Google Scholar] [CrossRef] [PubMed]
- Tang, Y.; Zhou, X.; Gao, B.; Xu, X.; Sun, J.; Cheng, L.; Zhou, X.; Zheng, L. Modulation of Wnt/β-catenin signaling attenuates periapical bone lesions. J. Dent. Res. 2014, 93, 175–182. [Google Scholar] [CrossRef] [PubMed]
- Maeda, H.; Wada, N.; Nakamuta, H.; Akamine, A. Human periapical granulation tissue contains osteogenic cells. Cell Tissue Res. 2004, 315, 203–208. [Google Scholar] [CrossRef] [PubMed]
- Marrelli, M.; Paduano, F.; Tatullo, M. Cells isolated from human periapical cysts express mesenchymal stem cell-like properties. Int. J. Biol. Sci. 2013, 9, 1070–1078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marrelli, M.; Paduano, F.; Tatullo, M. Human periapical cyst-mesenchymal stem cells differentiate into neuronal cells. J. Dent. Res. 2015, 94, 843–852. [Google Scholar] [CrossRef] [PubMed]
- Jiang, W.; Xu, J. Immune modulation by mesenchymal stem cells. Cell Prolif. 2020, 53, e12712. [Google Scholar] [CrossRef] [Green Version]
- Nair, P.N. Apical periodontitis: A dynamic encounter between root canal infection and host response. Periodontology 2000 1997, 13, 121–148. [Google Scholar] [CrossRef]
- Gomes, B.; Herrera, D.R. Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology. Braz. Oral Res. 2018, 32 (Suppl. S1), e69. [Google Scholar] [CrossRef] [Green Version]
- Siqueira, J.F., Jr.; Rôças, I.N. Microbiology and treatment of acute apical abscesses. Clin. Microbiol. Rev. 2013, 26, 255–273. [Google Scholar] [CrossRef] [Green Version]
- Bergamini, M.L.; Mardegan, A.P.; CS, D.E.R.; Palmieri, M.; Sarmento, D.J.S.; Hiraki, K.R.N.; Costa, A.L.F.; HassEus, B.; Jonasson, P.; Braz-Silva, P.H. Presence of langerhans cells, regulatory T cells (Treg) and mast cells in asymptomatic apical periodontitis. Braz. Oral Res. 2020, 34, e108. [Google Scholar] [CrossRef]
- Amin, N.; Boccardi, V.; Taghizadeh, M.; Jafarnejad, S. Probiotics and bone disorders: The role of RANKL/RANK/OPG pathway. Aging Clin. Exp. Res. 2020, 32, 363–371. [Google Scholar] [CrossRef] [PubMed]
- Udagawa, N.; Koide, M.; Nakamura, M.; Nakamichi, Y.; Yamashita, T.; Uehara, S.; Kobayashi, Y.; Furuya, Y.; Yasuda, H.; Fukuda, C.; et al. Osteoclast differentiation by RANKL and OPG signaling pathways. J. Bone Miner. Metab. 2020, 39, 19–26. [Google Scholar] [CrossRef] [PubMed]
- Cavalla, F.; Letra, A.; Silva, R.M.; Garlet, G.P. Determinants of Periodontal/Periapical Lesion Stability and Progression. J. Dent. Res. 2021, 100, 29–36. [Google Scholar] [CrossRef]
- Francisconi, C.F.; Vieira, A.E.; Biguetti, C.C.; Glowacki, A.J.; Trombone, A.P.; Letra, A.; Menezes Silva, R.; Sfeir, C.S.; Little, S.R.; Garlet, G.P. Characterization of the Protective Role of Regulatory T Cells in Experimental Periapical Lesion Development and Their Chemoattraction Manipulation as a Therapeutic Tool. J. Endod. 2016, 42, 120–126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fine, N.; Tasevski, N.; McCulloch, C.A.; Tenenbaum, H.C.; Glogauer, M. The Neutrophil: Constant Defender and First Responder. Front. Immunol. 2020, 11, 571085. [Google Scholar] [CrossRef] [PubMed]
- Braz-Silva, P.H.; Bergamini, M.L.; Mardegan, A.P.; De Rosa, C.S.; Hasseus, B.; Jonasson, P. Inflammatory profile of chronic apical periodontitis: A literature review. Acta Odontol. Scand. 2019, 77, 173–180. [Google Scholar] [CrossRef] [Green Version]
- Eming, S.A.; Krieg, T.; Davidson, J.M. Inflammation in wound repair: Molecular and cellular mechanisms. J. Investig. Dermatol. 2007, 127, 514–525. [Google Scholar] [CrossRef] [Green Version]
- De Rossi, A.; Lucisano, M.P.; De Rossi, M.; Nelson-Filho, P.; Silva, R.A.B.; Silva, L.A.B.; Saraiva, M.C.P.; Fukada, S.Y. Effect of intercellular adhesion molecule 1 deficiency on the development of apical periodontitis. Int. Endod. J. 2020, 53, 354–365. [Google Scholar] [CrossRef]
- Marçal, J.R.; Samuel, R.O.; Fernandes, D.; de Araujo, M.S.; Napimoga, M.H.; Pereira, S.A.; Clemente-Napimoga, J.T.; Alves, P.M.; Mattar, R.; Rodrigues, V., Jr.; et al. T-helper cell type 17/regulatory T-cell immunoregulatory balance in human radicular cysts and periapical granulomas. J. Endod. 2010, 36, 995–999. [Google Scholar] [CrossRef]
- Cintra, L.T.; Samuel, R.O.; Azuma, M.M.; Ribeiro, C.P.; Narciso, L.G.; de Lima, V.M.; Sumida, D.H.; Coclete, G.A.; Dezan-Júnior, E.; Gomes-Filho, J.E. Apical periodontitis and periodontal disease increase serum IL-17 levels in normoglycemic and diabetic rats. Clin. Oral Investig. 2014, 18, 2123–2128. [Google Scholar] [CrossRef]
- Lu, D.; Xu, Y.; Liu, Q.; Zhang, Q. Mesenchymal Stem Cell-Macrophage Crosstalk and Maintenance of Inflammatory Microenvironment Homeostasis. Front. Cell Dev. Biol. 2021, 9, 681171. [Google Scholar] [CrossRef] [PubMed]
- Paula-Silva, F.W.G.; Ribeiro-Santos, F.R.; Petean, I.B.F.; Manfrin Arnez, M.F.; Almeida-Junior, L.A.; Carvalho, F.K.; Silva, L.; Faccioli, L.H. Root canal contamination or exposure to lipopolysaccharide differentially modulate prostaglandin E 2 and leukotriene B 4 signaling in apical periodontitis. J. Appl. Oral Sci. 2020, 28, e20190699. [Google Scholar] [CrossRef] [PubMed]
- Souto, G.R.; Queiroz-Junior, C.M.; de Abreu, M.H.; Costa, F.O.; Mesquita, R.A. Pro-inflammatory, Th1, Th2, Th17 cytokines and dendritic cells: A cross-sectional study in chronic periodontitis. PLoS ONE 2014, 9, e91636. [Google Scholar] [CrossRef]
- Kimura, T.; Kobiyama, K.; Winkels, H.; Tse, K.; Miller, J.; Vassallo, M.; Wolf, D.; Ryden, C.; Orecchioni, M.; Dileepan, T.; et al. Regulatory CD4(+) T Cells Recognize Major Histocompatibility Complex Class II Molecule-Restricted Peptide Epitopes of Apolipoprotein B. Circulation 2018, 138, 1130–1143. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Yang, F.; Qiu, Y.; Ye, L.; Song, D.; Huang, D. The Potential Roles of T Cells in Periapical Lesions. J. Endod. 2022, 48, 70–79. [Google Scholar] [CrossRef]
- Trinchieri, G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003, 3, 133–146. [Google Scholar] [CrossRef]
- Mosmann, T.R.; Cherwinski, H.; Bond, M.W.; Giedlin, M.A.; Coffman, R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. 1986. J. Immunol. 2005, 175, 5–14. [Google Scholar]
- de Brito, L.C.; Teles, F.R.; Teles, R.P.; Totola, A.H.; Vieira, L.Q.; Sobrinho, A.P. T-lymphocyte and cytokine expression in human inflammatory periapical lesions. J. Endod. 2012, 38, 481–485. [Google Scholar] [CrossRef]
- Kabashima, H.; Nagata, K.; Maeda, K.; Iijima, T. Presence of IFN-gamma and IL-4 in human periapical granulation tissues and regeneration tissues. Cytokine 2001, 14, 289–293. [Google Scholar] [CrossRef]
- Araujo-Pires, A.C.; Francisconi, C.F.; Biguetti, C.C.; Cavalla, F.; Aranha, A.M.; Letra, A.; Trombone, A.P.; Faveri, M.; Silva, R.M.; Garlet, G.P. 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. J. Appl. Oral Sci. 2014, 22, 336–346. [Google Scholar] [CrossRef] [Green Version]
- Colić, M.; Vasilijić, S.; Gazivoda, D.; Vucević, D.; Marjanović, M.; Lukić, A. Interleukin-17 plays a role in exacerbation of inflammation within chronic periapical lesions. Eur. J. Oral Sci. 2007, 115, 315–320. [Google Scholar] [CrossRef] [PubMed]
- Xiong, H.; Wei, L.; Peng, B. Immunohistochemical localization of IL-17 in induced rat periapical lesions. J. Endod. 2009, 35, 216–220. [Google Scholar] [CrossRef] [PubMed]
- AlShwaimi, E.; Berggreen, E.; Furusho, H.; Rossall, J.C.; Dobeck, J.; Yoganathan, S.; Stashenko, P.; Sasaki, H. IL-17 receptor A signaling is protective in infection-stimulated periapical bone destruction. J. Immunol. 2013, 191, 1785–1791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colić, M.; Gazivoda, D.; Vucević, D.; Majstorović, I.; Vasilijić, S.; Rudolf, R.; Brkić, Z.; Milosavljević, P. Regulatory T-cells in periapical lesions. J. Dent. Res. 2009, 88, 997–1002. [Google Scholar] [CrossRef]
- Andrade, A.L.; Santos, E.M.; Carmo, A.F.; Freitas, R.A.; Galvao, H.C. Analysis of tryptase-positive mast cells and immunoexpression of MMP-9 and MMP-13 in periapical lesions. Int. Endod. J. 2017, 50, 446–454. [Google Scholar] [CrossRef]
- Estrela, C.; Carmo Souza, P.O.; Barbosa, M.G.; Aburad de Carvalhosa, A.; Batista, A.C.; Pinto Júnior, D.D.S.; Yamamoto-Silva, F.P.; de Freitas Silva, B.S. Mesenchymal Stem Cell Marker Expression in Periapical Abscess. J. Endod. 2019, 45, 716–723. [Google Scholar] [CrossRef]
- Estrela, C.; Freitas Silva, B.S.; Silva, J.A.; Yamamoto-Silva, F.P.; Pinto-Júnior, D.D.; Gomez, R.S. Stem Cell Marker Expression in Persistent Apical Periodontitis. J. Endod. 2017, 43, 63–68. [Google Scholar] [CrossRef]
- Liao, J.; Al Shahrani, M.; Al-Habib, M.; Tanaka, T.; Huang, G.T. Cells isolated from inflamed periapical tissue express mesenchymal stem cell markers and are highly osteogenic. J. Endod. 2011, 37, 1217–1224. [Google Scholar] [CrossRef] [Green Version]
- Zeb Khan, S.; Mirza, S.; Sadiq, M.S.K.; Karim, S.; Alkahtany, M.F.; Almadi, K.H.; Aldahian, N.; Abdulwahed, A.; Almutairi, B.; Mustafa, M.; et al. Immunohistochemical expression of PCNA, STRO-1 and CD 44 in the healing of experimentally induced periapical lesions in rats. Eur. Rev. Med. Pharmacol. Sci. 2021, 25, 7679–7686. [Google Scholar]
- Paduano, F.; Marrelli, M.; Palmieri, F.; Tatullo, M. CD146 Expression Influences Periapical Cyst Mesenchymal Stem Cell Properties. Stem Cell Rev. Rep. 2016, 12, 592–603. [Google Scholar] [CrossRef]
- Tatullo, M.; Falisi, G.; Amantea, M.; Rastelli, C.; Paduano, F.; Marrelli, M. Dental Pulp Stem Cells and Human Periapical Cyst Mesenchymal Stem Cells in Bone Tissue Regeneration: Comparison of Basal and Osteogenic Differentiated Gene Expression of a Newly Discovered Mesenchymal Stem Cell Lineage. J. Biol. Regul. Homeost. Agents 2015, 29, 713–718. [Google Scholar] [PubMed]
- Dokić, J.; Tomić, S.; Cerović, S.; Todorović, V.; Rudolf, R.; Colić, M. Characterization and immunosuppressive properties of mesenchymal stem cells from periapical lesions. J. Clin. Periodontol. 2012, 39, 807–816. [Google Scholar] [CrossRef] [PubMed]
- Araujo-Pires, A.C.; Biguetti, C.C.; Repeke, C.E.; Rodini Cde, O.; Campanelli, A.P.; Trombone, A.P.; Letra, A.; Silva, R.M.; Garlet, G.P. Mesenchymal stem cells as active prohealing and immunosuppressive agents in periapical environment: Evidence from human and experimental periapical lesions. J. Endod. 2014, 40, 1560–1565. [Google Scholar] [CrossRef] [PubMed]
- Dokić, J.; Tomić, S.; Marković, M.; Milosavljević, P.; Colić, M. Mesenchymal stem cells from periapical lesions modulate differentiation and functional properties of monocyte-derived dendritic cells. Eur. J. Immunol. 2013, 43, 1862–1872. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Chen, X.; Cao, W.; Shi, Y. Plasticity of mesenchymal stem cells in immunomodulation: Pathological and therapeutic implications. Nat. Immunol. 2014, 15, 1009–1016. [Google Scholar] [CrossRef]
- Li, W.; Ren, G.; Huang, Y.; Su, J.; Han, Y.; Li, J.; Chen, X.; Cao, K.; Chen, Q.; Shou, P.; et al. Mesenchymal stem cells: A double-edged sword in regulating immune responses. Cell Death Differ. 2012, 19, 1505–1513. [Google Scholar] [CrossRef] [Green Version]
- Gronthos, S.; Mankani, M.; Brahim, J.; Robey, P.G.; Shi, S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2000, 97, 13625–13630. [Google Scholar] [CrossRef] [Green Version]
- Miura, M.; Gronthos, S.; Zhao, M.; Lu, B.; Fisher, L.W.; Robey, P.G.; Shi, S. SHED: Stem cells from human exfoliated deciduous teeth. Proc. Natl. Acad. Sci. USA 2003, 100, 5807–5812. [Google Scholar] [CrossRef] [Green Version]
- Seo, B.M.; Miura, M.; Gronthos, S.; Bartold, P.M.; Batouli, S.; Brahim, J.; Young, M.; Robey, P.G.; Wang, C.Y.; Shi, S. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004, 364, 149–155. [Google Scholar] [CrossRef]
- Morsczeck, C.; Götz, W.; Schierholz, J.; Zeilhofer, F.; Kühn, U.; Möhl, C.; Sippel, C.; Hoffmann, K.H. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol. 2005, 24, 155–165. [Google Scholar] [CrossRef]
- Sonoyama, W.; Liu, Y.; Fang, D.; Yamaza, T.; Seo, B.M.; Zhang, C.; Liu, H.; Gronthos, S.; Wang, C.Y.; Wang, S.; et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 2006, 1, e79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamaza, T.; Ren, G.; Akiyama, K.; Chen, C.; Shi, Y.; Shi, S. Mouse mandible contains distinctive mesenchymal stem cells. J. Dent. Res. 2011, 90, 317–324. [Google Scholar] [CrossRef] [PubMed]
- Fan, Y.; Cui, C.; Rosen, C.J.; Sato, T.; Xu, R.; Li, P.; Wei, X.; Bi, R.; Yuan, Q.; Zhou, C. Klotho in Osx(+)-mesenchymal progenitors exerts pro-osteogenic and anti-inflammatory effects during mandibular alveolar bone formation and repair. Signal Transduct. Target. Ther. 2022, 7, 155. [Google Scholar] [CrossRef]
- Walker, E.C.; Johnson, R.W.; Hu, Y.; Brennan, H.J.; Poulton, I.J.; Zhang, J.G.; Jenkins, B.J.; Smyth, G.K.; Nicola, N.A.; Sims, N.A. Murine Oncostatin M Acts via Leukemia Inhibitory Factor Receptor to Phosphorylate Signal Transducer and Activator of Transcription 3 (STAT3) but Not STAT1, an Effect That Protects Bone Mass. J. Biol. Chem. 2016, 291, 21703–21716. [Google Scholar] [CrossRef] [Green Version]
- Stuart, C.H.; Schwartz, S.A.; Beeson, T.J.; Owatz, C.B. Enterococcus faecalis: Its role in root canal treatment failure and current concepts in retreatment. J. Endod. 2006, 32, 93–98. [Google Scholar] [CrossRef] [PubMed]
- Dai, X.; Ma, R.; Jiang, W.; Deng, Z.; Chen, L.; Liang, Y.; Shao, L.; Zhao, W. Enterococcus faecalis-Induced Macrophage Necroptosis Promotes Refractory Apical Periodontitis. Microbiol. Spectr. 2022, 10, e0104522. [Google Scholar] [CrossRef]
- Akintoye, S.O.; Lam, T.; Shi, S.; Brahim, J.; Collins, M.T.; Robey, P.G. Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 2006, 38, 758–768. [Google Scholar] [CrossRef]
- Zhang, D.; Zhang, S.; Wang, J.; Li, Q.; Xue, H.; Sheng, R.; Xiong, Q.; Qi, X.; Wen, J.; Fan, Y.; et al. LepR-Expressing Stem Cells Are Essential for Alveolar Bone Regeneration. J. Dent. Res. 2020, 99, 1279–1286. [Google Scholar] [CrossRef]
- Cui, C.; Bi, R.; Liu, W.; Guan, S.; Li, P.; Song, D.; Xu, R.; Zheng, L.; Yuan, Q.; Zhou, X.; et al. Role of PTH1R Signaling in Prx1(+) Mesenchymal Progenitors during Eruption. J. Dent. Res. 2020, 99, 1296–1305. [Google Scholar] [CrossRef]
- Huang, G.T.; Sonoyama, W.; Liu, Y.; Liu, H.; Wang, S.; Shi, S. The hidden treasure in apical papilla: The potential role in pulp/dentin regeneration and bioroot engineering. J. Endod. 2008, 34, 645–651. [Google Scholar] [CrossRef] [Green Version]
- Sonoyama, W.; Liu, Y.; Yamaza, T.; Tuan, R.S.; Wang, S.; Shi, S.; Huang, G.T. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: A pilot study. J. Endod. 2008, 34, 166–171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Songsaad, A.; Gonmanee, T.; Ruangsawasdi, N.; Phruksaniyom, C.; Thonabulsombat, C. Potential of resveratrol in enrichment of neural progenitor-like cell induction of human stem cells from apical papilla. Stem Cell Res. Ther. 2020, 11, 542. [Google Scholar] [CrossRef] [PubMed]
- Yoo, Y.J.; Oh, J.H.; Lee, W.; Woo, K.M. Regenerative Characteristics of Apical Papilla-derived Cells from Immature Teeth with Pulpal and Periapical Pathosis. J. Endod. 2016, 42, 1626–1632. [Google Scholar] [CrossRef]
- Shen, Z.; Wichnieski, C.; Carneiro, E.; Garlet, G.P.; Letra, A.; Silva, R.M. Expression Profiling and Functional Characterization of MicroRNAs in Apical Periodontitis. J. Endod. 2021, 47, 263–271. [Google Scholar] [CrossRef] [PubMed]
- Chai, Y.; Jiang, X.; Ito, Y.; Bringas, P., Jr.; Han, J.; Rowitch, D.H.; Soriano, P.; McMahon, A.P.; Sucov, H.M. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 2000, 127, 1671–1679. [Google Scholar] [CrossRef]
- Bi, R.; Lyu, P.; Song, Y.; Li, P.; Song, D.; Cui, C.; Fan, Y. Function of Dental Follicle Progenitor/Stem Cells and Their Potential in Regenerative Medicine: From Mechanisms to Applications. Biomolecules 2021, 11, 997. [Google Scholar] [CrossRef] [PubMed]
- Yao, S.; Pan, F.; Prpic, V.; Wise, G.E. Differentiation of stem cells in the dental follicle. J. Dent. Res. 2008, 87, 767–771. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wise, G.E.; Fan, W. Changes in the tartrate-resistant acid phosphatase cell population in dental follicles and bony crypts of rat molars during tooth eruption. J. Dent. Res. 1989, 68, 150–156. [Google Scholar] [CrossRef]
- Volejnikova, S.; Laskari, M.; Marks, S.C., Jr.; Graves, D.T. Monocyte recruitment and expression of monocyte chemoattractant protein-1 are developmentally regulated in remodeling bone in the mouse. Am. J. Pathol. 1997, 150, 1711–1721. [Google Scholar]
- Meng, M.; Chen, Y.; Chen, X.; Zhang, Q.; Guo, W.; Zhou, X.; Zou, J. IL-1α Regulates Osteogenesis and Osteoclastic Activity of Dental Follicle Cells Through JNK and p38 MAPK Pathways. Stem Cells Dev. 2020, 29, 1552–1566. [Google Scholar] [CrossRef]
- Hong, H.; Chen, X.; Li, K.; Wang, N.; Li, M.; Yang, B.; Yu, X.; Wei, X. Dental follicle stem cells rescue the regenerative capacity of inflamed rat dental pulp through a paracrine pathway. Stem Cell Res. Ther. 2020, 11, 333. [Google Scholar] [CrossRef] [PubMed]
- Gronthos, S.; Brahim, J.; Li, W.; Fisher, L.W.; Cherman, N.; Boyde, A.; DenBesten, P.; Robey, P.G.; Shi, S. Stem cell properties of human dental pulp stem cells. J. Dent. Res. 2002, 81, 531–535. [Google Scholar] [CrossRef] [PubMed]
- La Noce, M.; Stellavato, A.; Vassallo, V.; Cammarota, M.; Laino, L.; Desiderio, V.; Del Vecchio, V.; Nicoletti, G.F.; Tirino, V.; Papaccio, G.; et al. Hyaluronan-Based Gel Promotes Human Dental Pulp Stem Cells Bone Differentiation by Activating YAP/TAZ Pathway. Cells 2021, 10, 2899. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Xu, H.; Xia, K.; Cheng, S.; Zhang, Q. Resolvin E1 accelerates pulp repair by regulating inflammation and stimulating dentin regeneration in dental pulp stem cells. Stem Cell Res. Ther. 2021, 12, 75. [Google Scholar] [CrossRef]
- Cui, S.J.; Zhang, T.; Fu, Y.; Liu, Y.; Gan, Y.H.; Zhou, Y.H.; Yang, R.L.; Wang, X.D. DPSCs Attenuate Experimental Progressive TMJ Arthritis by Inhibiting the STAT1 Pathway. J. Dent. Res. 2020, 99, 446–455. [Google Scholar] [CrossRef]
- Shen, Z.; Kuang, S.; Zhang, Y.; Yang, M.; Qin, W.; Shi, X.; Lin, Z. Chitosan hydrogel incorporated with dental pulp stem cell-derived exosomes alleviates periodontitis in mice via a macrophage-dependent mechanism. Bioact. Mater. 2020, 5, 1113–1126. [Google Scholar] [CrossRef]
- Rosa, V.; Dubey, N.; Islam, I.; Min, K.S.; Nör, J.E. Pluripotency of Stem Cells from Human Exfoliated Deciduous Teeth for Tissue Engineering. Stem Cells Int. 2016, 2016, 5957806. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.; Ma, Y.; Guo, W.; Yang, B.; Tian, W. Stem cells from human exfoliated deciduous teeth as an alternative cell source in bio-root regeneration. Theranostics 2019, 9, 2694–2711. [Google Scholar] [CrossRef]
- Gao, X.; Shen, Z.; Guan, M.; Huang, Q.; Chen, L.; Qin, W.; Ge, X.; Chen, H.; Xiao, Y.; Lin, Z. Immunomodulatory Role of Stem Cells from Human Exfoliated Deciduous Teeth on Periodontal Regeneration. Tissue Eng. Part A 2018, 24, 1341–1353. [Google Scholar] [CrossRef]
- Yang, N.; Liu, X.; Chen, X.; Yu, S.; Yang, W.; Liu, Y. Stem cells from exfoliated deciduous teeth transplantation ameliorates Sjögren’s syndrome by secreting soluble PD-L1. J. Leukoc. Biol. 2022, 111, 1043–1055. [Google Scholar] [CrossRef]
- Kim, D.; Lee, A.E.; Xu, Q.; Zhang, Q.; Le, A.D. Gingiva-Derived Mesenchymal Stem Cells: Potential Application in Tissue Engineering and Regenerative Medicine—A Comprehensive Review. Front. Immunol. 2021, 12, 667221. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Shi, S.; Liu, Y.; Uyanne, J.; Shi, Y.; Shi, S.; Le, A.D. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J. Immunol. 2009, 183, 7787–7798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakao, Y.; Fukuda, T.; Zhang, Q.; Sanui, T.; Shinjo, T.; Kou, X.; Chen, C.; Liu, D.; Watanabe, Y.; Hayashi, C.; et al. Exosomes from TNF-α-treated human gingiva-derived MSCs enhance M2 macrophage polarization and inhibit periodontal bone loss. Acta Biomater. 2021, 122, 306–324. [Google Scholar] [CrossRef]
- Gu, Y.; Shi, S. Transplantation of gingiva-derived mesenchymal stem cells ameliorates collagen-induced arthritis. Arthritis Res. Ther. 2016, 18, 262. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Chen, B.; Bao, J.; Zhang, Y.; Lei, L.; Yan, F. Macrophage polarization in periodontal ligament stem cells enhanced periodontal regeneration. Stem Cell Res. Ther. 2019, 10, 320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Wang, H.; Zhang, L.; Li, X.; Ding, X.; Ding, G.; Wei, F. Periodontal ligament stem cells promote polarization of M2 macrophages. J. Leukoc. Biol. 2022, 111, 1185–1197. [Google Scholar] [CrossRef] [PubMed]
- Del Fabbro, M.; Corbella, S.; Sequeira-Byron, P.; Tsesis, I.; Rosen, E.; Lolato, A.; Taschieri, S. Endodontic procedures for retreatment of periapical lesions. Cochrane Database Syst. Rev. 2016, 10, Cd005511. [Google Scholar] [CrossRef]
- Caplan, D.J.; Cai, J.; Yin, G.; White, B.A. Root canal filled versus non-root canal filled teeth: A retrospective comparison of survival times. J. Public Health Dent. 2005, 65, 90–96. [Google Scholar] [CrossRef]
- Chrepa, V.; Henry, M.A.; Daniel, B.J.; Diogenes, A. Delivery of Apical Mesenchymal Stem Cells into Root Canals of Mature Teeth. J. Dent. Res. 2015, 94, 1653–1659. [Google Scholar] [CrossRef]
- Paryani, K.; Kim, S.G. Regenerative endodontic treatment of permanent teeth after completion of root development: A report of 2 cases. J. Endod. 2013, 39, 929–934. [Google Scholar] [CrossRef]
- Cordero, C.B.; Santander, G.M.; González, D.U.; Quezada, A.; Silva, C.I.; Vásquez, C.; Jara, R.; Jara, D.; Khoury, M. Allogeneic Cellular Therapy in a Mature Tooth with Apical Periodontitis and Accidental Root Perforation: A Case Report. J. Endod. 2020, 46, 1920–1927.e1. [Google Scholar] [PubMed]
- Gomez-Sosa, J.F.; Diaz-Solano, D.; Wittig, O.; Cardier, J.E. Dental Pulp Regeneration Induced by Allogenic Mesenchymal Stromal Cell Transplantation in a Mature Tooth: A Case Report. J. Endod. 2022, 48, 736–740. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.J.; Kwon, J.; Current, L.; Yoon, K.; Zalal, R.; Hu, X.; Xue, P.; Ko, C.C. Osteogenic potential of mesenchymal stem cells from rat mandible to regenerate critical sized calvarial defect. J. Tissue Eng. 2019, 10, 2041731419830427. [Google Scholar] [CrossRef] [PubMed]
- Hallal, S.; Tűzesi, Á.; Grau, G.E.; Buckland, M.E.; Alexander, K.L. Understanding the extracellular vesicle surface for clinical molecular biology. J. Extracell. Vesicles 2022, 11, e12260. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.; Liu, Q.; Chen, S.; Zhang, F.; Li, Y.; Fan, W.; Mai, L.; He, H.; Huang, F. Extracellular vesicles delivering nuclear factor I/C for hard tissue engineering: Treatment of apical periodontitis and dentin regeneration. J. Tissue Eng. 2022, 13, 20417314221084095. [Google Scholar] [CrossRef]
- Luo, X.; Wan, Q.; Cheng, L.; Xu, R. Mechanisms of bone remodeling and therapeutic strategies in chronic apical periodontitis. Front. Cell Infect. Microbiol. 2022, 12, 908859. [Google Scholar] [CrossRef]
- Virtej, A.; Papadakou, P.; Sasaki, H.; Bletsa, A.; Berggreen, E. VEGFR-2 reduces while combined VEGFR-2 and -3 signaling increases inflammation in apical periodontitis. J. Oral Microbiol. 2016, 8, 32433. [Google Scholar] [CrossRef]
- Demiralp, B.; Keçeli, H.G.; Muhtaroğullar, M.; Serper, A.; Demiralp, B.; Eratalay, K. Treatment of periapical inflammatory lesion with the combination of platelet-rich plasma and tricalcium phosphate: A case report. J. Endod. 2004, 30, 796–800. [Google Scholar] [CrossRef]
- Virdee, S.S.; Bashir, N.; Camilleri, J.; Cooper, P.R.; Tomson, P.L. Exploiting Dentine Matrix Proteins in Cell-Free Approaches for Periradicular Tissue Engineering. Tissue Eng. Part B Rev. 2022, 28, 707–732. [Google Scholar] [CrossRef]
- Galler, K.M.; Buchalla, W.; Hiller, K.A.; Federlin, M.; Eidt, A.; Schiefersteiner, M.; Schmalz, G. Influence of root canal disinfectants on growth factor release from dentin. J. Endod. 2015, 41, 363–368. [Google Scholar] [CrossRef]
- Zeng, Q.; Nguyen, S.; Zhang, H.; Chebrolu, H.P.; Alzebdeh, D.; Badi, M.A.; Kim, J.R.; Ling, J.; Yang, M. Release of Growth Factors into Root Canal by Irrigations in Regenerative Endodontics. J. Endod. 2016, 42, 1760–1766. [Google Scholar] [CrossRef]
- Chae, Y.; Yang, M.; Kim, J. Release of TGF-β1 into root canals with various final irrigants in regenerative endodontics: An in vitro analysis. Int. Endod. J. 2018, 51, 1389–1397. [Google Scholar] [CrossRef] [PubMed]
- Graham, L.; Cooper, P.R.; Cassidy, N.; Nor, J.E.; Sloan, A.J.; Smith, A.J. The effect of calcium hydroxide on solubilisation of bio-active dentine matrix components. Biomaterials 2006, 27, 2865–2873. [Google Scholar] [CrossRef] [PubMed]
- Tomson, P.L.; Lumley, P.J.; Smith, A.J.; Cooper, P.R. Growth factor release from dentine matrix by pulp-capping agents promotes pulp tissue repair-associated events. Int. Endod. J. 2017, 50, 281–292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duncan, H.F.; Smith, A.J.; Fleming, G.J.; Reid, C.; Smith, G.; Cooper, P.R. Release of bio-active dentine extracellular matrix components by histone deacetylase inhibitors (HDACi). Int. Endod. J. 2017, 50, 24–38. [Google Scholar] [CrossRef]
- Ferracane, J.L.; Cooper, P.R.; Smith, A.J. Dentin matrix component solubilization by solutions of pH relevant to self-etching dental adhesives. J. Adhes. Dent. 2013, 15, 407–412. [Google Scholar]
- Kim, S.G.; Malek, M.; Sigurdsson, A.; Lin, L.M.; Kahler, B. Regenerative endodontics: A comprehensive review. Int. Endod. J. 2018, 51, 1367–1388. [Google Scholar] [CrossRef]
- Sadaghiani, L.; Gleeson, H.B.; Youde, S.; Waddington, R.J.; Lynch, C.D.; Sloan, A.J. Growth Factor Liberation and DPSC Response Following Dentine Conditioning. J. Dent. Res. 2016, 95, 1298–1307. [Google Scholar] [CrossRef] [Green Version]
- Widbiller, M.; Eidt, A.; Lindner, S.R.; Hiller, K.A.; Schweikl, H.; Buchalla, W.; Galler, K.M. Dentine matrix proteins: Isolation and effects on human pulp cells. Int. Endod. J. 2018, 51 (Suppl. S4), e278–e290. [Google Scholar] [CrossRef] [Green Version]
- Gonçalves, L.F.; Fernandes, A.P.; Cosme-Silva, L.; Colombo, F.A.; Martins, N.S.; Oliveira, T.M.; Araujo, T.H.; Sakai, V.T. Effect of EDTA on TGF-β1 released from the dentin matrix and its influence on dental pulp stem cell migration. Braz. Oral Res. 2016, 30, e131. [Google Scholar] [CrossRef] [Green Version]
- He, M.; Chen, T.; Lv, Y.; Song, P.; Deng, B.; Guo, X.; Rui, S.; Boey, J.; Armstrong, D.G.; Ma, Y.; et al. The role of allogeneic platelet-rich plasma in patients with diabetic foot ulcer: Current perspectives and future challenges. Front. Bioeng. Biotechnol. 2022, 10, 993436. [Google Scholar] [CrossRef] [PubMed]
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Lyu, P.; Song, Y.; Bi, R.; Li, Z.; Wei, Y.; Huang, Q.; Cui, C.; Song, D.; Zhou, X.; Fan, Y. Protective Actions in Apical Periodontitis: The Regenerative Bioactivities Led by Mesenchymal Stem Cells. Biomolecules 2022, 12, 1737. https://doi.org/10.3390/biom12121737
Lyu P, Song Y, Bi R, Li Z, Wei Y, Huang Q, Cui C, Song D, Zhou X, Fan Y. Protective Actions in Apical Periodontitis: The Regenerative Bioactivities Led by Mesenchymal Stem Cells. Biomolecules. 2022; 12(12):1737. https://doi.org/10.3390/biom12121737
Chicago/Turabian StyleLyu, Ping, Yiming Song, Ruiye Bi, Zucen Li, Yali Wei, Qin Huang, Chen Cui, Dongzhe Song, Xuedong Zhou, and Yi Fan. 2022. "Protective Actions in Apical Periodontitis: The Regenerative Bioactivities Led by Mesenchymal Stem Cells" Biomolecules 12, no. 12: 1737. https://doi.org/10.3390/biom12121737