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ORIGINAL RESEARCH

Dental Pulp Stem Cell-Derived Exosomes Regulate Anti-Inflammatory and Osteogenesis in Periodontal Ligament Stem Cells and Promote the Repair of Experimental Periodontitis in Rats

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Pages 4683-4703 | Received 11 May 2023, Accepted 09 Aug 2023, Published online: 17 Aug 2023

References

  • Kinane D, Stathopoulou P, Papapanou P. Periodontal diseases. Nature Rev Dis Primers. 2017;3:17038. doi:10.1038/nrdp.2017.38
  • Meire M, Bronzato J, Bomfim R, et al. Effectiveness of adjunct therapy for the treatment of apical periodontitis: a systematic review and meta-analysis. Int Endod J. 2022. doi:10.1111/iej.13838
  • Tavelli L, Barootchi S, Rasperini G, et al. Clinical and patient-reported outcomes of tissue engineering strategies for periodontal and peri-implant reconstruction. Periodontol 2000. 2022; 91(1):217.
  • Dragana R, Jelena M, Jovan M, et al. Antibacterial efficiency of adjuvant photodynamic therapy and high-power diode laser in the treatment of young permanent teeth with chronic periapical periodontitis. A prospective clinical study. Photodiagnosis Photodyn Ther. 2022;41:103129. doi:10.1016/j.pdpdt.2022.103129
  • Ray R. Periodontitis: an oral disease with severe consequences. Appl Biochem Biotechnol. 2022;195:17.
  • Hagelaars M, Rijns L, Dankers P, et al. Engineering strategies to move from understanding to steering renal tubulogenesis. Tissue Eng Part B Rev. 2022;29:203–216. doi:10.1089/ten.TEB.2022.0120
  • Liu G, Zhou Y, Zhang X, et al. Advances in hydrogels for stem cell therapy: regulation mechanisms and tissue engineering applications. J Materials Chem B. 2022;10:5520–5536. doi:10.1039/D2TB01044E
  • Wen Y, Dai N, Hsu S. Biodegradable water-based polyurethane scaffolds with a sequential release function for cell-free cartilage tissue engineering. Acta Biomaterialia. 2019;88:301–313. doi:10.1016/j.actbio.2019.02.044
  • Park J, Lee J, Yoon B, et al. Additive effect of bFGF and selenium on expansion and paracrine action of human amniotic fluid-derived mesenchymal stem cells. Stem Cell Res Ther. 2018;9:293. doi:10.1186/s13287-018-1058-z
  • Park J, Park G, Hong H. Age affects the paracrine activity and differentiation potential of human adipose-derived stem cells. Mol Med Rep. 2021;23:1.
  • Sikora B, Skubis-Sikora A, Prusek A, et al. Paracrine activity of adipose derived stem cells on limbal epithelial stem cells. Sci Rep. 2021;11:19956. doi:10.1038/s41598-021-99435-1
  • Liu Y, Zhuang X, Yu S, et al. Exosomes derived from stem cells from apical papilla promote craniofacial soft tissue regeneration by enhancing Cdc42-mediated vascularization. Stem Cell Res Ther. 2021;12:76. doi:10.1186/s13287-021-02151-w
  • Chamberlain C, Kink J, Wildenauer L, et al. Exosome-educated macrophages and exosomes differentially improve ligament healing. Stem Cells. 2021;39(1):55–61. doi:10.1002/stem.3291
  • Jafari D, Malih S, Eini M, et al. Improvement, scaling-up, and downstream analysis of exosome production. Crit Rev Biotechnol. 2020;40:1098–1112. doi:10.1080/07388551.2020.1805406
  • Pu X, Ma S, Gao Y, et al. Mesenchymal stem cell-derived exosomes: biological function and their therapeutic potential in radiation damage. Cells. 2020;10:10. doi:10.3390/cells10010010
  • Liu L, Guo S, Shi W, et al. Bone marrow mesenchymal stem cell-derived small extracellular vesicles promote periodontal regeneration. Tissue Eng Part A. 2021;27:962–976. doi:10.1089/ten.tea.2020.0141
  • Song X, Xue Y, Fan S, et al. Lipopolysaccharide-activated macrophages regulate the osteogenic differentiation of bone marrow mesenchymal stem cells through exosomes. PeerJ. 2022;10:e13442. doi:10.7717/peerj.13442
  • Wang M, Li J, Ye Y, et al. SHED-derived conditioned exosomes enhance the osteogenic differentiation of PDLSCs via Wnt and BMP signaling in vitro. Res Biol Diversity. 2020;111:1–11. doi:10.1016/j.diff.2019.10.003
  • Wei J, Song Y, Du Z, et al. Exosomes derived from human exfoliated deciduous teeth ameliorate adult bone loss in mice through promoting osteogenesis. J Mol Histol. 2020;51:455–466. doi:10.1007/s10735-020-09896-3
  • Wu J, Chen L, Wang R, et al. Exosomes secreted by stem cells from human exfoliated deciduous teeth promote alveolar bone defect repair through the regulation of angiogenesis and osteogenesis. ACS biomaterials sci eng. 2019;5:3561–3571. doi:10.1021/acsbiomaterials.9b00607
  • Cui D, Li H, Wan M, et al. The origin and identification of mesenchymal stem cells in teeth: from odontogenic to non-odontogenic. Curr Stem Cell Res Ther. 2018;13:39–45.
  • Morsczeck C, Reichert T. Dental stem cells in tooth regeneration and repair in the future. Expert Opin Biol Ther. 2018;18:187–196. doi:10.1080/14712598.2018.1402004
  • Ziauddin S, Nakashima M, Watanabe H, et al. Biological characteristics and pulp regeneration potential of stem cells from canine deciduous teeth compared with those of permanent teeth. Stem Cell Res Ther. 2022;13:439. doi:10.1186/s13287-022-03124-3
  • Gupta S, Rawat S, Krishnakumar V, et al. Hypoxia preconditioning elicit differential response in tissue-specific MSCs via immunomodulation and exosomal secretion. Cell Tissue Res. 2022;388:535–548. doi:10.1007/s00441-022-03615-y
  • Paliwal S, Chaudhuri R, Agrawal A, et al. Human tissue-specific MSCs demonstrate differential mitochondria transfer abilities that may determine their regenerative abilities. Stem Cell Res Ther. 2018;9:298. doi:10.1186/s13287-018-1012-0
  • Shoushrah S, Transfeld J, Tonk C, et al. Sinking our teeth in getting dental stem cells to clinics for bone regeneration. Int J Mol Sci;2021. 22. doi:10.3390/ijms23010022
  • Ma L, Hu J, Cao Y, et al. Maintained properties of aged dental pulp stem cells for superior periodontal tissue regeneration. Aging Dis. 2019;10:793–806. doi:10.14336/AD.2018.0729
  • Shen Z, Kuang S, Zhang Y, et al. Chitosan hydrogel incorporated with dental pulp stem cell-derived exosomes alleviates periodontitis in mice via a macrophage-dependent mechanism. Bioactive Materials. 2020;5:1113–1126. doi:10.1016/j.bioactmat.2020.07.002
  • Swanson W, Gong T, Zhang Z, et al. Controlled release of odontogenic exosomes from a biodegradable vehicle mediates dentinogenesis as a novel biomimetic pulp capping therapy. J Control Release. 2020;324:679–694. doi:10.1016/j.jconrel.2020.06.006
  • Xian X, Gong Q, Li C, et al. Exosomes with highly angiogenic potential for possible use in pulp regeneration. J Endod. 2018;44:751–758. doi:10.1016/j.joen.2017.12.024
  • Li H, Deng Y, Tan M, et al. Low-intensity pulsed ultrasound upregulates osteogenesis under inflammatory conditions in periodontal ligament stem cells through unfolded protein response. Stem Cell Res Ther. 2020;11:215. doi:10.1186/s13287-020-01732-5
  • Shi J, Zhang Y, Zhang X, et al. Remodeling immune microenvironment in periodontitis using resveratrol liposomes as an antibiotic-free therapeutic strategy. J Nanobiotechnology. 2021;19:429. doi:10.1186/s12951-021-01175-x
  • Zhang X, Xu M, Xue Q, et al. A modified method for constructing experimental rat periodontitis model. Front bioeng biotechnol. 2022;10:1098015. doi:10.3389/fbioe.2022.1098015
  • Kotova A, Lobov A, Dombrovskaya J, et al. Comparative analysis of dental pulp and periodontal stem cells: differences in morphology, functionality, osteogenic differentiation and proteome. Biomedicines. 2021;9(11):1606. doi:10.3390/biomedicines9111606
  • Amghar-Maach S, Gay-Escoda C, Sánchez-Garcés M. Regeneration of periodontal bone defects with dental pulp stem cells grafting: systematic Review. J Clin Exp Dentistry. 2019;11:e373–e381. doi:10.4317/jced.55574
  • Chen Q, Liu X, Wang D, et al. Periodontal inflammation-triggered by periodontal ligament stem cell pyroptosis exacerbates periodontitis. Front Cell Dev Biol. 2021;9:663037. doi:10.3389/fcell.2021.663037
  • Buschow S, van Balkom B, Aalberts M, et al. MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol Cell Biol. 2010;88:851–856. doi:10.1038/icb.2010.64
  • Lu M, Peng L, Ming X, et al. Enhanced wound healing promotion by immune response-free monkey autologous iPSCs and exosomes vs. their allogeneic counterparts. EBioMedicine. 2019;42:443–457. doi:10.1016/j.ebiom.2019.03.011
  • Singh K, Nalabotala R, Koo K, et al. Separation of distinct exosome subpopulations: isolation and characterization approaches and their associated challenges. Analyst. 2021;146:3731–3749. doi:10.1039/D1AN00024A
  • Ding L, Yang X, Gao Z, et al. A holistic review of the state-of-the-art microfluidics for exosome separation: an overview of the current status, existing obstacles, and future outlook. Small. 2021;17:e2007174. doi:10.1002/smll.202007174
  • Huang S, Ji X, Jackson K, et al. Rapid separation of blood plasma exosomes from low-density lipoproteins via a hydrophobic interaction chromatography method on a polyester capillary-channeled polymer fiber phase. Anal Chim Acta. 2021;1167:338578. doi:10.1016/j.aca.2021.338578
  • Yang D, Zhang W, Zhang H, et al. Progress, opportunity, and perspective on exosome isolation - efforts for efficient exosome-based theranostics. Theranostics. 2020;10:3684–3707. doi:10.7150/thno.41580
  • Tang Y, Huang Y, Zheng L, et al. Comparison of isolation methods of exosomes and exosomal RNA from cell culture medium and serum. Int J Mol Med. 2017;40:834–844. doi:10.3892/ijmm.2017.3080
  • Zhao X, Wu D, Ma X, et al. Exosomes as drug carriers for cancer therapy and challenges regarding exosome uptake. Biomed Pharmacother. 2020;128:110237. doi:10.1016/j.biopha.2020.110237
  • Liesveld J, Sharma N, Aljitawi O. Stem cell homing: from physiology to therapeutics. Stem Cells. 2020;38:1241–1253. doi:10.1002/stem.3242
  • Wang S, Niu Y, Jia P, et al. Alkaline activation of endogenous latent TGFβ1 by an injectable hydrogel directs cell homing for in situ complex tissue regeneration. Bioactive Materials. 2022;15:316–329. doi:10.1016/j.bioactmat.2021.12.015
  • Chen H, Wang Z, He Y, et al. Pyroptosis may play a crucial role in modifications of the immune microenvironment in periodontitis. J Periodontal Res. 2022;57:977–990. doi:10.1111/jre.13035
  • Bartold P, Van Dyke T. An appraisal of the role of specific bacteria in the initial pathogenesis of periodontitis. J Clin Periodontol. 2019;46:6–11. doi:10.1111/jcpe.13046
  • Ma J, Kageyama S, Takeshita T, et al. Clinical utility of subgingival plaque-specific bacteria in salivary microbiota for detecting periodontitis. PLoS One. 2021;16:e0253502. doi:10.1371/journal.pone.0253502
  • Almubarak A, Tanagala K, Papapanou P, et al. Disruption of Monocyte and Macrophage Homeostasis in Periodontitis. Front Immunol. 2020;11:330. doi:10.3389/fimmu.2020.00330
  • Zhang B, Yang Y, Yi J, et al. Hyperglycemia modulates M1/M2 macrophage polarization via reactive oxygen species overproduction in ligature-induced periodontitis. J Periodontal Res. 2021;56:991–1005. doi:10.1111/jre.12912
  • Alam M, Mae M, Farhana F, et al. NLRP3 inflammasome negatively regulates rankl-induced osteoclastogenesis of mouse bone marrow macrophages but positively regulates it in the presence of lipopolysaccharides. Int J Mol Sci. 2022;23(11):6096. doi:10.3390/ijms23116096
  • Zhu H, Tamura A, Zhang S, et al. Mitigating RANKL-induced cholesterol overload in macrophages with β-cyclodextrin-threaded polyrotaxanes suppresses osteoclastogenesis. Biomaterials Science. 2022;10(18):5230–5242. doi:10.1039/D2BM00833E
  • Lundahl M, Mitermite M, Ryan D, et al. Macrophage innate training induced by IL-4 and IL-13 activation enhances OXPHOS driven anti-mycobacterial responses. eLife. 2022;11.
  • Shang N, Wu J. Egg-Derived Tripeptide IRW Attenuates LPS-Induced Osteoclastogenesis in RAW 264.7 Macrophages via Inhibition of Inflammatory Responses and NF-κB/MAPK Activation. J Agric Food Chem. 2020;68:6132–6141. doi:10.1021/acs.jafc.0c01159
  • Zhu K, Yang C, Dai H, et al. Crocin inhibits titanium particle-induced inflammation and promotes osteogenesis by regulating macrophage polarization. Int Immunopharmacol. 2019;76:105865. doi:10.1016/j.intimp.2019.105865
  • Menon P, Doudin A, Gregus A, et al. The anti-parallel dimer binding interface in STAT3 transcription factor is required for the inactivation of cytokine-mediated signal transduction. Biochimica et biophysica acta Mol cell res. 2021;1868:119118. doi:10.1016/j.bbamcr.2021.119118
  • Mohassab A, Hassan H, Abdelhamid D, et al. STAT3 transcription factor as target for anti-cancer therapy. Pharmacol Rep. 2020;72:1101–1124. doi:10.1007/s43440-020-00156-5
  • Nikolskii A, Shilovskiy I, Barvinskaia E, et al. Role of STAT3 Transcription Factor in Pathogenesis of Bronchial Asthma. Biochemistry (Mosc). 2021;86:1489–1501. doi:10.1134/S0006297921110122
  • Hu Y, Zhang X, Zhang J, et al. Activated STAT3 signaling pathway by ligature-induced periodontitis could contribute to neuroinflammation and cognitive impairment in rats. J Neuroinflammation. 2021;18:80. doi:10.1186/s12974-021-02071-9
  • de Los Fayos Alonso I G, Zujo L, Wiest I, et al. PDGFRβ promotes oncogenic progression via STAT3/STAT5 hyperactivation in anaplastic large cell lymphoma. Mol Cancer. 2022;21:172. doi:10.1186/s12943-022-01640-7
  • Yan M, Han M, Yang X, et al. Dual inhibition of EGFR and IL-6-STAT3 signalling by miR-146b: a potential targeted therapy for epithelial ovarian cancer. J Enzyme Inhib Med Chem. 2021;36:1905–1915. doi:10.1080/14756366.2021.1963240
  • Zhao K, Dai Q, Wu J, et al. Morusin enhances the antitumor activity of MAPK pathway inhibitors in BRAF-mutant melanoma by inhibiting the feedback activation of STAT3. Eur j Cancer. 2022;165:58–70. doi:10.1016/j.ejca.2022.01.004
  • Huang Y, Liu Q, Liu L, et al. Lipopolysaccharide-preconditioned dental follicle stem cells derived small extracellular vesicles treating periodontitis via reactive oxygen species/mitogen-activated protein kinase signaling-mediated antioxidant effect. Int J Nanomedicine. 2022;17:799–819. doi:10.2147/IJN.S350869
  • Lei F, Li M, Lin T, et al. Treatment of inflammatory bone loss in periodontitis by stem cell-derived exosomes. Acta Biomater. 2022;141:333–343. doi:10.1016/j.actbio.2021.12.035