Lipopolysaccharide-Preconditioned Dental Follicle Stem Cells Derived Small Extracellular Vesicles Treating Periodontitis via Reactive Oxygen Species/Mitogen-Activated Protein Kinase Signaling-Mediated Antioxidant Effect

References

• Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol. 1997;14:9–11. doi:10.1111/j.1600-0757.1997.tb00189.x
   Web of Science ®Google Scholar
• Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009;7(2):107–127.
   PubMed Web of Science ®Google Scholar
• Ramírez JH, Parra B, Gutierrez S, et al. Biomarkers of cardiovascular disease are increased in untreated chronic periodontitis: a case control study. Aust Dent J. 2014;59(1):29–36. doi:10.1111/adj.12139
   PubMed Web of Science ®Google Scholar
• Ide M, Harris M, Stevens A, et al. Periodontitis and Cognitive Decline in Alzheimer’s Disease. PLoS One. 2016;11(3):e0151081. doi:10.1371/journal.pone.0151081
   PubMed Web of Science ®Google Scholar
• El Moshy S, Radwan IA, Rady D, et al. Dental stem cell-derived secretome/conditioned medium: the future for regenerative therapeutic applications. Stem Cells Int. 2020;2020:7593402. doi:10.1155/2020/7593402
   PubMed Web of Science ®Google Scholar
• Bi R, Lyu P, Song Y, et al. Function of dental follicle progenitor/stem cells and their potential in regenerative medicine: from mechanisms to applications. Biomolecules. 2021;11(7):997. doi:10.3390/biom11070997
   PubMed Web of Science ®Google Scholar
• Meirelles Lda S, Fontes AM, Covas DT, Caplan AI. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 2009;20(5–6):419–427. doi:10.1016/j.cytogfr.2009.10.002
   PubMed Web of Science ®Google Scholar
• Weiss ARR, Dahlke MH. Immunomodulation by Mesenchymal Stem Cells (MSCs): mechanisms of Action of Living, Apoptotic, and Dead MSCs. Front Immunol. 2019;10:1191. doi:10.3389/fimmu.2019.01191
   PubMed Web of Science ®Google Scholar
• Luan X, Zhou X, Trombetta-eSilva J, et al. MicroRNAs and Periodontal Homeostasis. J Dent Res. 2017;96(5):491–500. doi:10.1177/0022034516685711
   PubMed Web of Science ®Google Scholar
• Garlet GP. Destructive and protective roles of cytokines in periodontitis: a reappraisal from host defense and tissue destruction viewpoints. J Dent Res. 2010;89(12):1349–1363. doi:10.1177/0022034510376402
   PubMed Web of Science ®Google Scholar
• Cardoso EM, Reis C, Manzanares-Céspedes MC. Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases. Postgrad Med. 2018;130(1):98–104. doi:10.1080/00325481.2018.1396876
   PubMed Web of Science ®Google Scholar
• Konopka L, Pietrzak A, Brzezińska-Błaszczyk E. Effect of scaling and root planing on interleukin-1β, interleukin-8 and MMP-8 levels in gingival crevicular fluid from chronic periodontitis patients. J Periodontal Res. 2012;47(6):681–688. doi:10.1111/j.1600-0765.2012.01480.x
   PubMed Web of Science ®Google Scholar
• Katsuda T, Kosaka N, Takeshita F, Ochiya T. The therapeutic potential of mesenchymal stem cell-derived extracellular vesicles. Proteomics. 2013;13(10–11):1637–1653. doi:10.1002/pmic.201200373
   PubMed Web of Science ®Google Scholar
• Song Y, Dou H, Li X, et al. Exosomal miR-146a Contributes to the Enhanced Therapeutic Efficacy of Interleukin-1β-Primed Mesenchymal Stem Cells Against Sepsis. Stem Cells. 2017;35(5):1208–1221. doi:10.1002/stem.2564
   PubMed Web of Science ®Google Scholar
• Kurte M, Vega-Letter AM, Luz-Crawford P, et al. Time-dependent LPS exposure commands MSC immunoplasticity through TLR4 activation leading to opposite therapeutic outcome in EAE. Stem Cell Res Ther. 2020;11(1):416. doi:10.1186/s13287-020-01840-2
   PubMed Web of Science ®Google Scholar
• Kim WJ, Park SY, Kim OS, Park HS, Jung JY. Autophagy upregulates inflammatory cytokines in gingival tissue of patients with periodontitis and lipopolysaccharide-stimulated human gingival fibroblasts. J Periodontol Epub. 2021. doi:10.1002/JPER.21-0178
   Google Scholar
• Lee MK, Ide M, Coward PY, Wilson RF. Effect of ultrasonic debridement using a chlorhexidine irrigant on circulating levels of lipopolysaccharides and interleukin-6. J Clin Periodontol. 2008;35(5):415–419. doi:10.1111/j.1600-051X.2008.01221.x
   PubMed Web of Science ®Google Scholar
• Shi W, Guo S, Liu L, et al. Small Extracellular Vesicles from Lipopolysaccharide-Preconditioned Dental Follicle Cells Promote Periodontal Regeneration in an Inflammatory Microenvironment. ACS Biomater Sci Eng. 2020;6(10):5797–5810. doi:10.1021/acsbiomaterials.0c00882
   PubMed Web of Science ®Google Scholar
• Greening DW, Gopal SK, Xu R, Simpson RJ, Chen W. Exosomes and their roles in immune regulation and cancer. Semin Cell Dev Biol. 2015;40:72–81. doi:10.1016/j.semcdb.2015.02.009
   PubMed Web of Science ®Google Scholar
• He X, Dong Z, Cao Y, et al. MSC-Derived Exosome Promotes M2 Polarization and Enhances Cutaneous Wound Healing. Stem Cells Int. 2019;2019:7132708. doi:10.1155/2019/7132708
   PubMed Web of Science ®Google Scholar
• Maia J, Caja S, Strano Moraes MC, Couto N, Costa-Silva B. Exosome-Based Cell–Cell Communication in the Tumor Microenvironment. Front Cell Dev Biol. 2018;6:18. doi:10.3389/fcell.2018.00018
   PubMed Web of Science ®Google Scholar
• Javeed N, Mukhopadhyay D. Exosomes and their role in the micro/macroenvironment: a comprehensive review. J Biomed Res. 2017;31(5):386–394. doi:10.7555/JBR.30.20150162
   PubMed Web of Science ®Google Scholar
• Eldh M, Ekstrom K, Valadi H, et al. Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS One. 2010;5(12):e15353. doi:10.1371/journal.pone.0015353
   PubMed Web of Science ®Google Scholar
• Guo S, Guo W, Ding Y, et al. Comparative study of human dental follicle cell sheets and periodontal ligament cell sheets for periodontal tissue regeneration. Cell Transplant. 2013;22(6):1061–1073. doi:10.3727/096368912X656036
   PubMed Web of Science ®Google Scholar
• Yang H, Li J, Hu Y, et al. Treated dentin matrix particles combined with dental follicle cell sheet stimulate periodontal regeneration. Dent Mater. 2019;35(9):1238–1253. doi:10.1016/j.dental.2019.05.016
   PubMed Web of Science ®Google Scholar
• Guo S, Kang J, Ji B, et al. Periodontal-Derived Mesenchymal Cell Sheets Promote Periodontal Regeneration in Inflammatory Microenvironment. Tissue Eng Part A. 2017;23(13–14):585–596. doi:10.1089/ten.tea.2016.0334
   PubMed Web of Science ®Google Scholar
• Van Tuyl LH, Voskuyl AE, Boers M, et al. Baseline RANKL:OPG ratio and markers of bone and cartilage degradation predict annual radiological progression over 11 years in rheumatoid arthritis. Ann Rheum Dis. 2010;69(9):1623–1628. doi:10.1136/ard.2009.121764
   PubMed Web of Science ®Google Scholar
• Chio IIC, Tuveson DA. ROS in Cancer: the Burning Question. Trends Mol Med. 2017;23(5):411–429. doi:10.1016/j.molmed.2017.03.004
   PubMed Web of Science ®Google Scholar
• Lee K, Seo I, Choi MH, Jeong D. Roles of Mitogen-Activated Protein Kinases in Osteoclast Biology. Int J Mol Sci. 2018;19(10):3004. doi:10.3390/ijms19103004
   PubMed Web of Science ®Google Scholar
• Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med. 1992;176(1):287–292. doi:10.1084/jem.176.1.287
   PubMed Web of Science ®Google Scholar
• Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13. doi:10.12703/P6-13
   PubMedGoogle Scholar
• Yin C, Zhao Q, Li W, et al. Biomimetic anti-inflammatory nanocapsule serves as a cytokine blocker and M2 polarization inducer for bone tissue repair. Acta Biomater. 2020;102:416–426. doi:10.1016/j.actbio.2019.11.025
   PubMed Web of Science ®Google Scholar
• Vašíček O, Lojek A, Číž M. Serotonin and its metabolites reduce oxidative stress in murine RAW264.7 macrophages and prevent inflammation. J Physiol Biochem. 2020;76(1):49–60. doi:10.1007/s13105-019-00714-3
   PubMed Web of Science ®Google Scholar
• Zhang Y, Choksi S, Chen K, Pobezinskaya Y, Linnoila I, Liu ZG. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res. 2013;23(7):898–914. doi:10.1038/cr.2013.75
   PubMed Web of Science ®Google Scholar
• Damiano S, Petrozziello T, Ucci V, Amente S, Santillo M, Mondola P. Cu-Zn superoxide dismutase activates muscarinic acetylcholine M1 receptor pathway in neuroblastoma cells. Mol Cell Neurosci. 2013;52:31–37. doi:10.1016/j.mcn.2012.11.001
   PubMed Web of Science ®Google Scholar
• Munir S, Basu A, Maity P, et al. TLR4-dependent shaping of the wound site by MSCs accelerates wound healing. EMBO Rep. 2020;21(5):e48777. doi:10.15252/embr.201948777
   PubMed Web of Science ®Google Scholar
• Shah SA, Khan M, Jo M-H, Jo MG, Amin FU, Kim MO. Melatonin Stimulates the SIRT1/Nrf2 Signaling Pathway Counteracting Lipopolysaccharide (LPS)-Induced Oxidative Stress to Rescue Postnatal Rat Brain. CNS Neurosci Ther. 2017;23(1):33–44. doi:10.1111/cns.12588
   PubMed Web of Science ®Google Scholar
• Lamont RJ, Koo H, Hajishengallis G. The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol. 2018;16(12):745–759. doi:10.1038/s41579-018-0089-x
   PubMed Web of Science ®Google Scholar
• Wang Y, Andrukhov O, Rausch-Fan X. Oxidative Stress and Antioxidant System in Periodontitis. Front Physiol. 2017;8:910. doi:10.3389/fphys.2017.00910
   PubMed Web of Science ®Google Scholar
• Wilson C. Bone: oxidative stress and osteoporosis. Nat Rev Endocrinol. 2014;10(1):3.doi:10.1038/nrendo.2013.225
   Google Scholar
• Zhao MJ, Yuan S, Zi H, Gu JM, Fang C, Zeng XT. Oxidative Stress Links Aging-Associated Cardiovascular Diseases and Prostatic Diseases. Oxid Med Cell Longev. 2021;2021:5896136. doi:10.1155/2021/5896136
   PubMed Web of Science ®Google Scholar
• Jomova K, Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology. 2011;283(2–3):65–87. doi:10.1016/j.tox.2011.03.001
   PubMed Web of Science ®Google Scholar
• Qiu X, Yu Y, Liu H, et al. Remodeling the periodontitis microenvironment for osteogenesis by using a reactive oxygen species-cleavable nanoplatform. Acta Biomater. 2021;135:593–605. doi:10.1016/j.actbio.2021.08.009
   PubMed Web of Science ®Google Scholar
• Lee KE, Mo S, Lee HS, et al. Deferoxamine Reduces Inflammation and Osteoclastogenesis in Avulsed Teeth. Int J Mol Sci. 2021;22(15):8225. doi:10.3390/ijms22158225
   PubMed Web of Science ®Google Scholar
• Corrêa MG, Absy S, Tenenbaum H, et al. Resveratrol attenuates oxidative stress during experimental periodontitis in rats exposed to cigarette smoke inhalation. J Periodontal Res. 2019;54(3):225–232. doi:10.1111/jre.12622
   Google Scholar
• Bakır B, Yetkin AZ, Büyükbayram Hİ, et al. Effect of curcumin on systemic T helper 17 cell response; gingival expressions of interleukin-17 and retinoic acid receptor-related orphan receptor γt; and alveolar bone loss in experimental periodontitis. J Periodontol. 2016;87(11):e183–e191. doi:10.1902/jop.2016.150722
   PubMed Web of Science ®Google Scholar
• Elavarasu S, Suthanthiran T, Thangavelu A, Alex S, Palanisamy VK, Kumar TS. Evaluation of superoxide dismutase levels in local drug delivery system containing 0.2% curcumin strip as an adjunct to scaling and root planing in chronic periodontitis: a clinical and biochemical study. J Pharm Bioallied Sci. 2016;8(Suppl 1):S48–S52. doi:10.4103/0975-7406.191967
   PubMedGoogle Scholar
• Hoffmann C, Dietrich M, Herrmann AK, Schacht T, Albrecht P, Methner A. Dimethyl Fumarate Induces Glutathione Recycling by Upregulation of Glutathione Reductase. Oxid Med Cell Longev. 2017;2017:6093903. doi:10.1155/2017/6093903
   PubMed Web of Science ®Google Scholar
• Hwang J, Jin J, Jeon S, et al. SOD1 suppresses pro-inflammatory immune responses by protecting against oxidative stress in colitis. Redox Bio. 2020;37:101760. doi:10.1016/j.redox.2020.101760
   PubMed Web of Science ®Google Scholar
• Liao N, Shi Y, Zhang C, et al. Antioxidants inhibit cell senescence and preserve stemness of adipose tissue-derived stem cells by reducing ROS generation during long-term in vitro expansion. Stem Cell Res Ther. 2019;10(1):306. doi:10.1186/s13287-019-1404-9
   PubMed Web of Science ®Google Scholar
• Climent M, Viggiani G, Chen YW, Coulis G, Castaldi A. MicroRNA and ROS Crosstalk in Cardiac and Pulmonary Diseases. Int J Mol Sci. 2020;21(12):4370. doi:10.3390/ijms21124370
   PubMed Web of Science ®Google Scholar
• Yao Y, Zhang F, Wang L, et al. Lipopolysaccharide preconditioning enhances the efficacy of mesenchymal stem cells transplantation in a rat model of acute myocardial infarction. J Biomed Sci. 2009;16(1):74. doi:10.1186/1423-0127-16-74
   PubMed Web of Science ®Google Scholar
• Wang ZJ, Zhang FM, Wang LS, Yao YW, Zhao Q, Gao X. Lipopolysaccharides can protect mesenchymal stem cells (MSCs) from oxidative stress-induced apoptosis and enhance proliferation of MSCs via Toll-like receptor (TLR)-4 and PI3K/Akt. Cell Biol Int. 2009;33(6):665–674. doi:10.1016/j.cellbi.2009.03.006
   PubMed Web of Science ®Google Scholar
• Chen K, Qiu P, Yuan Y, et al. Pseurotin An Inhibits Osteoclastogenesis and Prevents Ovariectomized-Induced Bone Loss by Suppressing Reactive Oxygen Species. Theranostics. 2019;9(6):1634–1650. doi:10.7150/thno.30206
   PubMed Web of Science ®Google Scholar
• Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000;103(2):239–252. doi:10.1016/S0092-8674(00)00116-1
   PubMed Web of Science ®Google Scholar
• Lee SE, Chung WJ, Kwak HB, et al. Tumor necrosis factor-alpha supports the survival of osteoclasts through the activation of Akt and ERK. J Biol Chem. 2001;276(52):49343–49349. doi:10.1074/jbc.M103642200
   PubMed Web of Science ®Google Scholar
• Ha H, Kwak HB, Lee SW, et al. Reactive oxygen species mediate RANK signaling in osteoclasts. Exp Cell Res. 2004;301(2):119–127. doi:10.1016/j.yexcr.2004.07.035
   PubMed Web of Science ®Google Scholar
• Lee NK, Choi YG, Baik JY, et al. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood. 2005;106(3):852–859. doi:10.1182/blood-2004-09-3662
   PubMed Web of Science ®Google Scholar
• Yang G, Chang CC, Yang Y, et al. Resveratrol Alleviates Rheumatoid Arthritis via Reducing ROS and Inflammation, Inhibiting MAPK Signaling Pathways, and Suppressing Angiogenesis. J Agric Food Chem. 2018;66(49):12953–12960. doi:10.1021/acs.jafc.8b05047
   PubMed Web of Science ®Google Scholar
• Zhu QY, Tai S, Tang L, et al. N-acetyl cysteine ameliorates aortic fibrosis by promoting M2 macrophage polarization in aging mice. Redox Rep. 2021;26(1):170–175. doi:10.1080/13510002.2021.1976568
   PubMed Web of Science ®Google Scholar
• Nakao Y, Fukuda T, Zhang Q, 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. doi:10.1016/j.actbio.2020.12.046
   PubMed Web of Science ®Google Scholar
• Kim J, Kim HY, Song SY, et al. Synergistic Oxygen Generation and Reactive Oxygen Species Scavenging by Manganese Ferrite/Ceria Codecorated Nanoparticles for Rheumatoid Arthritis Treatment. ACS Nano. 2019;13(3):3206–3217. doi:10.1021/acsnano.8b08785
   PubMed Web of Science ®Google Scholar
• Vasamsetti SB, Karnewar S, Gopoju R, et al. Resveratrol attenuates monocyte-to-macrophage differentiation and associated inflammation via modulation of intracellular GSH homeostasis: relevance in atherosclerosis. Free Radic Biol Med. 2016;96:392–405. doi:10.1016/j.freeradbiomed.2016.05.003
   PubMed Web of Science ®Google Scholar
• Roberts CP, Murphy AA, Santanam N, Parthasarathy S. Regulation of monocyte to macrophage differentiation by antiglucocorticoids and antioxidants. Am J Obstet Gynecol. 1998;179(2):354–362. doi:10.1016/S0002-9378(98)70364-3
   PubMed Web of Science ®Google Scholar
• Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat Liver. J Biol Chem. 2001;276(42):38388–38393. doi:10.1074/jbc.M105395200
   PubMed Web of Science ®Google Scholar
• Gupta S, Kediege SD, Gupta A, Jain K. Evaluation of Gengigel® Application in the Management of Furcation with Coronally Advanced Flap through Surgical Re-Entry-A Split Mouth Clinical Study. J Clin Diagn Res. 2017;11(1):ZC27–ZC32. doi:10.7860/JCDR/2017/21938.9169
   PubMedGoogle Scholar
• Forte L, Torricelli P, Boanini E, Rubini K, Fini M, Bigi A. Quercetin and alendronate multifunctionalized materials as tools to hinder oxidative stress damage. J Biomed Mater Res A. 2017;105(12):3293–3303. doi:10.1002/jbm.a.36192
   PubMed Web of Science ®Google Scholar
• Huang CC, Narayanan R, Alapati S, Ravindran S. Exosomes as biomimetic tools for stem cell differentiation: applications in dental pulp tissue regeneration. Biomaterials. 2016;1:111,103–115. doi:10.1016/j.biomaterials.2016.09.029
   Web of Science ®Google Scholar
• Zhang S, Chuah SJ, Lai RC, Hui JHP, Lim SK, Toh WS. MSC exosomes mediate cartilage repair by enhancing proliferation, attenuating apoptosis and modulating immune reactivity. Biomaterials. 2018;156:16–27. doi:10.1016/j.biomaterials.2017.11.028
   PubMed Web of Science ®Google Scholar
• Wang B, Wang J, Shao J, et al. A tunable and injectable local drug delivery system for personalized periodontal application. J Control Release. 2020;324:134–145. doi:10.1016/j.jconrel.2020.05.004
   PubMed Web of Science ®Google Scholar
• Chew JRJ, Chuah SJ, Teo KYW, et al. Mesenchymal stem cell exosomes enhance periodontal ligament cell functions and promote periodontal regeneration. Acta Biomater. 2019;89:252–264. doi:10.1016/j.actbio.2019.03.021
   PubMed Web of Science ®Google Scholar
• Phinney DG, Pittenger MF. Concise Review: MSC-Derived Exosomes for Cell-Free Therapy. Stem Cells. 2017;35(4):851–858. doi:10.1002/stem.2575
   PubMed Web of Science ®Google Scholar