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On-line Access: 2025-07-28
Received: 2024-01-24
Revision Accepted: 2024-07-09
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Citations: Bibtex RefMan EndNote GB/T7714
https://orcid.org/0000-0002-5371-4432
Qianhui LI, Hongye LU, Mengyuan ZHANG, Yuting YE, Qianming CHEN, Ping SUN. Epigenetic factors associated with peri-implantitis: a review[J]. Journal of Zhejiang University Science B,in press.Frontiers of Information Technology & Electronic Engineering,in press.https://doi.org/10.1631/jzus.B2400032 @article{title="Epigenetic factors associated with peri-implantitis: a review", %0 Journal Article TY - JOUR
与种植体周炎相关的表观遗传因素:综述浙江大学医学院附属口腔医院,浙江大学口腔医学院,浙江省口腔疾病临床医学研究中心,浙江省口腔生物医学研究重点实验室,浙江大学癌症研究院,口腔生物材料与器械浙江省工程研究中心,中国杭州市,310000 摘要:种植体周病是一类以硬组织吸收和软组织炎症为特征的病症。表观遗传学是指不在DNA序列中编码的基因表达的改变,影响免疫反应、炎症和骨代谢在内的多种生理活动。表观遗传修饰导致个体间组织特异性基因表达的差异,可能引发或加剧炎症和疾病易感性,然而其对种植体周炎的影响尚无定论。为了填补这一空白,我们在PubMed、Web of Science、Scopus和Google Scholar上使用"epigenetics""peri-implantitis""DNA methylation"和"microRNA"等关键词进行文献搜索,探讨表观遗传机制与种植体周炎之间的关系,并特别关注DNA甲基化和microRNAs(miRNAs或miRs)。DNA甲基化和miRNAs在种植体周围形成了一种动态的表观遗传机制。与炎症和成骨相关的基因表观遗传修饰为理解局部和环境因素如何影响种植体周炎的发病机制提供了新的视角。此外,我们评估了DNA甲基化和miRNAs在种植体周炎预防、诊断和治疗中的潜在应用,旨在为未来探索潜在治疗靶点并开发更有效的管理策略提供基础。这些发现对于理解其他口腔炎症性疾病(如牙周炎)的发病机制也具有更广泛的意义。 关键词组: Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article
Reference[1]AlvesCH, RussiKL, RochaNC, et al., 2022. Host-microbiome interactions regarding peri-implantitis and dental implant loss. J Transl Med, 20:425. ![]() [2]AmirhosseiniM, MadsenRV, EscottKJ, et al., 2018. GSK-3β inhibition suppresses instability-induced osteolysis by a dual action on osteoblast and osteoclast differentiation. J Cell Physiol, 233(3):2398-2408. ![]() [3]AstolfiV, Ríos-CarrascoB, Gil-MurFJ, et al., 2022. Incidence of peri-implantitis and relationship with different conditions: a retrospective study. Int J Environ Res Public Health, 19(7):4147. ![]() [4]BerglundhT, ArmitageG, AraujoMG, et al., 2018. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Clin Periodontol, 45(S20):S286-S291. ![]() [5]BerglundhT, MombelliA, SchwarzF, et al., 2024. Etiology, pathogenesis and treatment of peri-implantitis: a European perspective. Periodontol 2000, in press. ![]() [6]BommaritoPA, FryRC, 2019. The role of DNA methylation in gene regulation. In: McCullough SD, Dolinoy DC (Eds.), Toxicoepigenetics. Academic Press, London, p.127-151. ![]() [7]CavalliG, HeardE, 2019. Advances in epigenetics link genetics to the environment and disease. Nature, 571(7766):489-499. ![]() [8]ChaparroA, AtriaP, RealiniO, et al., 2021. Diagnostic potential of peri-implant crevicular fluid microRNA-21-3p and microRNA-150-5p and extracellular vesicles in peri-implant diseases. J Periodontol, 92(6):e11-e21. ![]() [9]ChenRS, LiaoX, ChenFR, et al., 2018. Circulating microRNAs, miR-10b-5p, miR-328-3p, miR-100 and let-7, are associated with osteoblast differentiation in osteoporosis. Int J Clin Exp Pathol, 11(3):1383-1390. ![]() [10]ChengL, FanYL, ChengJ, et al., 2022. Long non-coding RNA ZFY-AS1 represses periodontitis tissue inflammation and oxidative damage via modulating microRNA-129-5p/DEAD-Box helicase 3 X-linked axis. Bioengineered, 13(5):12691-12705. ![]() [11]ChoYD, KimPJ, KimHG, et al., 2020. Transcriptome and methylome analysis of periodontitis and peri-implantitis with tobacco use. Gene, 727:144258. ![]() [12]ChoYD, KimWJ, KimS, et al., 2021. Surface topography of titanium affects their osteogenic potential through DNA methylation. Int J Mol Sci, 22(5):2406. ![]() [13]ChoiSW, BraunT, HenigI, et al., 2017. Vorinostat plus tacrolimus/methotrexate to prevent GVHD after myeloablative conditioning, unrelated donor HCT. Blood, 130(15):1760-1767. ![]() [14]ChoudhuriS, 2011. From Waddington’s epigenetic landscape to small noncoding RNA: some important milestones in the history of epigenetics research. Toxicol Mech Methods, 21(4):252-274. ![]() [15]DaubertDM, PozhitkovAE, SafiotiLM, et al., 2019. Association of global DNA methylation to titanium and peri-implantitis: a case-control study. JDR Clin Trans Res, 4(3):284-291. ![]() [16]de la RicaL, García-GómezA, CometNR, et al., 2015. NF-κB-direct activation of microRNAs with repressive effects on monocyte-specific genes is critical for osteoclast differentiation. Genome Biol, 16:2. ![]() [17]DerksJ, IchiokaY, DionigiC, et al., 2023. Prevention and management of peri-implant mucositis and peri-implantitis: a systematic review of outcome measures used in clinical studies in the last 10 years. J Clin Periodontol, 50(S25):55-66. ![]() [18]DumitrescuRG, 2018. Early epigenetic markers for precision medicine. In: Dumitrescu RG, Verma M (Eds.), Cancer Epigenetics for Precision Medicine. Humana Press, New York, p.3-17. ![]() [19]FarsettiA, IlliB, GaetanoC, 2023. How epigenetics impacts on human diseases. Eur J Intern Med, 114:15-22. ![]() [20]GanesanSM, DabdoubSM, NagarajaHN, et al., 2022. Biome-microbiome interactions in peri-implantitis: a pilot investigation. J Periodontol, 93(6):814-823. ![]() [21]GaoCS, RenCM, LiuZX, et al., 2019. GAS5, a FoxO1-actived long noncoding RNA, promotes propofol-induced oral squamous cell carcinoma apoptosis by regulating the miR-1297-GSK3β axis. Artif Cells Nanomed Biotechnol, 47(1):3985-3993. ![]() [22]GengZ, WangXG, ZhaoJ, et al., 2018. The synergistic effect of strontium-substituted hydroxyapatite and microRNA-21 on improving bone remodeling and osseointegration. Biomater Sci, 6(10):2694-2703. ![]() [23]GengZ, YuYM, LiZY, et al., 2020. miR-21 promotes osseointegration and mineralization through enhancing both osteogenic and osteoclastic expression. Mater Sci Eng C Mater Biol Appl, 111:110785. ![]() [24]GuanHB, FanDP, MrelashviliD, et al., 2013. MicroRNA let-7e is associated with the pathogenesis of experimental autoimmune encephalomyelitis. Eur J Immunol, 43(1):104-114. ![]() [25]GuglielmottiMB, OlmedoDG, CabriniRL, 2019. Research on implants and osseointegration. Periodontol 2000, 79(1):178-189. ![]() [26]HiersNM, LiTQ, TraugotCM, et al., 2024. Target-directed microRNA degradation: mechanisms, significance, and functional implications. WIREs RNA, 15(2):e1832. ![]() [27]HoPTB, ClarkIM, LeLTT, 2022. MicroRNA-based diagnosis and therapy. Int J Mol Sci, 23(13):7167. ![]() [28]HodgesAJ, HudsonNO, Buck-KoehntopBA, 2020. Cys2His2 zinc finger methyl-CpG binding proteins: getting a handle on methylated DNA. J Mol Biol, 432(6):1640-1660. ![]() [29]HoggSJ, BeavisPA, DawsonMA, et al., 2020. Targeting the epigenetic regulation of antitumour immunity. Nat Rev Drug Discov, 19(11):776-800. ![]() [30]HollidayR, PughJE, 1975. DNA modification mechanisms and gene activity during development. Science, 187(4173):226-232. ![]() [31]IsolaG, TartagliaGM, SantonocitoS, et al., 2023. Impact of N-terminal pro-B-type natriuretic peptide and related inflammatory biomarkers on periodontal treatment outcomes in patients with periodontitis: an explorative human randomized-controlled clinical trial. J Periodontol, 94(12):1414-1424. ![]() [32]JiangSY, XueD, XieYF, et al., 2015. The negative feedback regulation of microRNA-146a in human periodontal ligament cells after Porphyromonas gingivalis lipopolysaccharide stimulation. Inflamm Res, 64(6):441-451. ![]() [33]JiangSY, HuY, DengS, et al., 2018. miR-146a regulates inflammatory cytokine production in Porphyromonas gingivalis lipopolysaccharide-stimulated B cells by targeting IRAK1 but not TRAF6. Biochim Biophys Acta Mol Basis Dis, 1864(3):925-933. ![]() [34]JinYC, HongFL, BaoQY, et al., 2020. MicroRNA-145 suppresses osteogenic differentiation of human jaw bone marrow mesenchymal stem cells partially via targeting semaphorin 3A. Connect Tissue Res, 61(6):577-585. ![]() [35]JurdzińskiKT, PotempaJ, GrabiecAM, 2020. Epigenetic regulation of inflammation in periodontitis: cellular mechanisms and therapeutic potential. Clin Epigenet, 12:186. ![]() [36]KadkhodazadehM, JafariAR, AmidR, et al., 2013. MiR146a and MiR499 gene polymorphisms in Iranian periodontitis and peri-implantitis patients. J Long-Term Eff Med Implants, 23(1):9-16. ![]() [37]KaurP, KotruS, SinghS, et al., 2022. Role of miRNAs in diabetic neuropathy: mechanisms and possible interventions. Mol Neurobiol, 59(3):1836-1849. ![]() [38]KhalidM, PetroianuG, AdemA, 2022. Advanced glycation end products and diabetes mellitus: mechanisms and perspectives. Biomolecules, 12(4):542. ![]() [39]KhoulyI, Pardiñas LópezS, Díaz PradoSM, et al., 2022. Global DNA methylation in dental implant failure due to peri-implantitis: an exploratory clinical pilot study. Int J Environ Res Public Health, 19(2):1020. ![]() [40]LarssonL, 2017. Current concepts of epigenetics and its role in periodontitis. Curr Oral Health Rep, 4(4):286-293. ![]() [41]LiY, ZhengJN, GongCJ, et al., 2020. Development of an immunogenomic landscape for the competing endogenous RNAs network of peri-implantitis. BMC Med Genet, 21:208. ![]() [42]LiYF, DuZB, XieXT, et al., 2021. Epigenetic changes caused by diabetes and their potential role in the development of periodontitis. J Diabetes Investig, 12(8):1326-1335. ![]() [43]LiYM, ChenGH, HeY, et al., 2021. Selenomethionine-modified polyethylenimine-based nanoparticles loaded with miR-132-3p inhibitor-biofunctionalized titanium implants for improved osteointegration. ACS Biomater Sci Eng, 7(10):4933-4945. ![]() [44]LiuHM, LiuP, 2021. Kartogenin promotes the BMSCs chondrogenic differentiation in osteoarthritis by down-regulation of miR-145-5p targeting Smad4 pathway. Tissue Eng Regen Med, 18(6):989-1000. ![]() [45]LiuXM, SuK, KuangSJ, et al., 2020. miR-16-5p and miR-145-5p trigger apoptosis in human gingival epithelial cells by down-regulating BACH2. Int J Clin Exp Pathol, 13(5):901-911. ![]() [46]LiuY, WangXX, YangDP, et al., 2014. MicroRNA-21 affects proliferation and apoptosis by regulating expression of PTEN in human keloid fibroblasts. Plast Reconstr Surg, 134(4):561e-573e. ![]() [47]LuanX, ZhouX, Trombetta-EsilvaJ, et al., 2017. MicroRNAs and periodontal homeostasis. J Dent Res, 96(5):491-500. ![]() [48]MatareseG, IsolalG, AnastaspGP, et al., 2013. Transforming growth factor beta 1 and vascular endothelial growth factor levels in the pathogenesis of periodontal disease. Eur J Inflamm, 11(2):479-488. ![]() [49]MazziottaC, BadialeG, CervelleraCF, et al., 2024. Regulatory mechanisms of circular RNAs during human mesenchymal stem cell osteogenic differentiation. Theranostics, 14(1):143-158. ![]() [50]MengYB, LiX, LiZY, et al., 2016. Surface functionalization of titanium alloy with miR-29b nanocapsules to enhance bone regeneration. ACS Appl Mater Interfaces, 8(9):5783-5793. ![]() [51]MeniniM, DellepianeE, BaldiD, et al., 2017. Microarray expression in peri-implant tissue next to different titanium implant surfaces predicts clinical outcomes: a split-mouth study. Clin Oral Implants Res, 28(9):e121-e134. ![]() [52]MeniniM, PesceP, BaldiD, et al., 2019. Prediction of titanium implant success by analysis of microRNA expression in peri-implant tissue. A 5-year follow-up study. J Clin Med, 8(6):888. ![]() [53]MeniniM, PesceP, PeraF, et al., 2021. MicroRNAs in peri-implant crevicular fluid can predict peri-implant bone resorption: clinical trial with a 5-year follow-up. Int J Oral Maxillofac Implants, 36(6):1148-1157. ![]() [54]MeteranH, KnudsenAØ, JørgensenTL, et al., 2024. Carboplatin plus paclitaxel in combination with the histone deacetylate inhibitor, vorinostat, in patients with recurrent platinum-sensitive ovarian cancer. J Clin Med, 13(3):897. ![]() [55]MichouL, 2018. Epigenetics of bone diseases. Joint Bone Spine, 85(6):701-707. ![]() [56]MijiritskyE, FerroniL, GardinC, et al., 2019. Presence of ROS in inflammatory environment of peri-implantitis tissue: in vitro and in vivo human evidence. J Clin Med, 9(1):38. ![]() [57]Millán-ZambranoG, BurtonA, BannisterAJ, et al., 2022. Histone post-translational modifications‒cause and consequence of genome function. Nat Rev Genet, 23(9):563-580. ![]() [58]MohrAM, MottJL, 2015. Overview of microRNA biology. Semin Liver Dis, 35(1):3-11. ![]() [59]NibaliL, GkraniasN, MainasG, et al., 2022. Periodontitis and implant complications in diabetes. Periodontol 2000, 90(1):88-105. ![]() [60]OhJM, KimY, SonH, et al., 2024. Comparative transcriptome analysis of periodontitis and peri-implantitis in human subjects. J Periodontol, 95(4):337-349. ![]() [61]Oton-GonzalezL, MazziottaC, IaquintaMR, et al., 2022. Genetics and epigenetics of bone remodeling and metabolic bone diseases. Int J Mol Sci, 23(3):1500. ![]() [62]PanKQ, HuY, WangYF, et al., 2020. RANKL blockade alleviates peri-implant bone loss and is enhanced by anti-inflammatory microRNA-146a through TLR2/4 signaling. Int J Implant Dent, 6:15. ![]() [63]SchwarzF, DerksJ, MonjeA, et al., 2018. Peri-implantitis. J Clin Periodontol, 45(S20):S246-S266. ![]() [64]SczepanikFSC, GrossiML, CasatiM, et al., 2020. Periodontitis is an inflammatory disease of oxidative stress: we should treat it that way. Periodontol 2000, 84(1):45-68. ![]() [65]SelbachM, SchwanhäusserB, ThierfelderN, et al., 2008. Widespread changes in protein synthesis induced by microRNAs. Nature, 455(7209):58-63. ![]() [66]ShangRF, LeeS, SenavirathneG, et al., 2023. microRNAs in action: biogenesis, function and regulation. Nat Rev Genet, 24(12):816-833. ![]() [67]ShaoD, WangCF, SunYP, et al., 2018. Effects of oral implants with miR-122-modified cell sheets on rat bone marrow mesenchymal stem cells. Mol Med Rep, 17(1):1537-1544. ![]() [68]ShenGY, RenH, ShangQ, et al., 2020. miR-128 plays a critical role in murine osteoclastogenesis and estrogen deficiency-induced bone loss. Theranostics, 10(10):4334-4348. ![]() [69]StraussFJ, StähliA, KobatakeR, et al., 2020. miRNA-21 deficiency impairs alveolar socket healing in mice. J Periodontol, 91(12):1664-1672. ![]() [70]SubramaniamR, VijakumaranU, ShanmugananthaL, et al., 2023. The role and mechanism of microRNA 21 in osteogenesis: an update. Int J Mol Sci, 24(14):11330. ![]() [71]SunL, GirnaryM, WangLF, et al., 2020. IL-10 dampens an IL-17-mediated periodontitis-associated inflammatory network. J Immunol, 204(8):2177-2191. ![]() [72]TanakaU, KajiokaS, FinotiLS, et al., 2021. Decitabine inhibits bone resorption in periodontitis by upregulating anti-inflammatory cytokines and suppressing osteoclastogenesis. Biomedicines, 9(2):199. ![]() [73]UrvasizogluG, KilicA, BarlakN, et al., 2021. MiR-4484 acts as a potential saliva biomarker for early detection of peri-implantitis. Int J Oral Maxillofac Implants, 36(1):115-121. ![]() [74]UrvasizogluG, KilicA, CapikO, et al., 2024. CXCL14 and miR-4484 serves as potential salivary biomarkers for early detection of peri-implantitis. Odontology, 112(3):864-871. ![]() [75]VojinovicJ, DamjanovN, D'UrzoC, et al., 2011. Safety and efficacy of an oral histone deacetylase inhibitor in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum, 63(5):1452-1458. ![]() [76]WachiT, ShutoT, ShinoharaY, et al., 2015. Release of titanium ions from an implant surface and their effect on cytokine production related to alveolar bone resorption. Toxicology, 327:1-9. ![]() [77]WaddingtonCH, 2012. The epigenotype. Int J Epidemiol, 41(1):10-13. ![]() [78]WangQ, WangXY, ValverdeP, et al., 2021. Osteogenic effects of microRNA-335-5p/lipidoid nanoparticles coated on titanium surface. Arch Oral Biol, 129:105207. ![]() [79]WangQN, YanYZ, ZhangXZ, et al., 2022. Rescuing effects of periostin in advanced glycation end-products (AGEs) caused osteogenic and oxidative damage through AGE receptor mediation and DNA methylation of the CALCA promoter. Chem Biol Interact, 354:109835. ![]() [80]WangSM, WuWY, 2018. DNA methylation alterations in human cancers. In: Tollefsbol TO (Ed.), Epigenetics in Human Disease, 2nd Ed. Academic Press, SanDiego, p.109-139. ![]() [81]WangYF, LiuHM, WuJM, et al., 2020. 5-Aza-2-deoxycytidine inhibits osteolysis induced by titanium particles by regulating RANKL/OPG ratio. Biochem Biophys Res Commun, 529(3):629-634. ![]() [82]WangZL, WuXF, HouXW, et al., 2020. miR-548b-3p functions as a tumor suppressor in lung cancer. Lasers Med Sci, 35(4):833-839. ![]() [83]WangZS, WuGS, FengZH, et al., 2015. Microarc-oxidized titanium surfaces functionalized with microRNA-21-loaded chitosan/hyaluronic acid nanoparticles promote the osteogenic differentiation of human bone marrow mesenchymal stem cells. Int J Nanomedicine, 10:6675-6687. ![]() [84]WangZS, WuGS, YangZJ, et al., 2022. Chitosan/hyaluronic acid/microRNA-21 nanoparticle-coated smooth titanium surfaces promote the functionality of human gingival fibroblasts. Int J Nanomedicine, 17:3793-3807. ![]() [85]WuXL, ChenXP, MiWX, et al., 2017. MicroRNA sequence analysis identifies microRNAs associated with peri-implantitis in dogs. Biosci Rep, 37(5):BSR20170768. ![]() [86]WuXL, GuQH, ChenXP, et al., 2019. MiR-27a targets DKK2 and SFRP1 to promote reosseointegration in the regenerative treatment of peri-implantitis. J Bone Miner Res, 34(1):123-134. ![]() [87]XieN, CuiHC, BanerjeeS, et al., 2014. miR-27a regulates inflammatory response of macrophages by targeting IL-10. J Immunol, 193(1):327-334. ![]() [88]XuC, WangZD, LiuYJ, et al., 2023. Extracellular vesicles derived from bone marrow mesenchymal stem cells loaded on magnetic nanoparticles delay the progression of diabetic osteoporosis via delivery of miR-150-5p. Cell Biol Toxicol, 39(4):1257-1274. ![]() [89]YadalamPK, ThiyagarajA, 2020. An immune interaction network driven approach for identifying biomarkers for peri‐implantitis. Clin Oral Implants Res, 31(S20):70. ![]() [90]YanJ, ChangB, HuXX, et al., 2018. Titanium implant functionalized with antimiR-138 delivered cell sheet for enhanced peri-implant bone formation and vascularization. Mater Sci Eng C Mater Biol Appl, 89:52-64. ![]() [91]ZhangHM, YuanY, XueHX, et al., 2022. MicroRNA sequence and function analysis in peri-implantitis and periodontitis: an animal study. J Periodontal Res, 57(5):1043-1055. ![]() [92]ZhangHM, YuanY, XueHX, et al., 2023. Reprogramming mitochondrial metabolism of macrophages by miRNA-released microporous coatings to prevent peri-implantitis. J Nanobiotechnol, 21:485. ![]() [93]ZhouHL, ChenDH, XieGF, et al., 2020. LncRNA-mediated ceRNA network was identified as a crucial determinant of differential effects in periodontitis and periimplantitis by high-throughput sequencing. Clin Implant Dent Relat Res, 22(3):424-450. ![]() [94]ZhouW, SuL, DuanXY, et al., 2018. MicroRNA-21 down-regulates inflammation and inhibits periodontitis. Mol Immunol, 101:608-614. ![]() Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou
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