Review Article

MicroRNA in Implant Dentistry: From Basic Science to Clinical Application

Author(s): Maria Menini*, Elena Dellepiane, Francesco Pera, Alberto Izzotti, Domenico Baldi, Francesca Delucchi, Francesco Bagnasco and Paolo Pesce

Volume 10 , Issue 1 , 2021

Published on: 13 July, 2021

Page: [14 - 28] Pages: 15

DOI: 10.2174/2211536610666210506123240

Price: $65

Abstract

Specific microRNA (miRNA) expression profiles have been reported to be predictive of specific clinical outcomes of dental implants and might be used as biomarkers in implant dentistry with diagnostic and prognostic purposes. The aim of the present narrative review was to summarize current knowledge regarding the use of miRNAs in implant dentistry. The authors attempted to identify all available evidence on the topic and critically appraise it in order to lay the foundation for the development of further research oriented towards the clinical application of miRNAs in implant dentistry.

Keywords: miRNA, implant dentistry, osseointegration, peri-implantitis, dental implants, osteogenesis.

Graphical Abstract
[1]
Ali Z, Baker SR, Shahrbaf S, Martin N, Vettore MV. Oral health-related quality of life after prosthodontic treatment for patients with partial edentulism: A systematic review and meta-analysis. J Prosthet Dent 2019; 121(1): 59-68.e3.
[http://dx.doi.org/10.1016/j.prosdent.2018.03.003] [PMID: 30006220]
[2]
Guglielmotti MB, Olmedo DG, Cabrini RL. Research on implants and osseointegration. Periodontol 2000 2019; 79(1): 178-89.
[http://dx.doi.org/10.1111/prd.12254] [PMID: 30892769]
[3]
Berglundh T, Armitage G, Araujo MG, et al. 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 2018; 45(20)(Suppl. 20): S286-91.
[http://dx.doi.org/10.1111/jcpe.12957] [PMID: 29926491]
[4]
Pesce P, Menini M, Tealdo T, Bevilacqua M, Pera F, Pera P. Peri-implantitis: A systematic review of recently published papers. Int J Prosthodont 2014; 27(1): 15-25.
[http://dx.doi.org/10.11607/ijp.3785] [PMID: 24392473]
[5]
Pesce P, Canullo L, Grusovin MG, de Bruyn H, Cosyn J, Pera P. Systematic review of some prosthetic risk factors for periimplantitis. J Prosthet Dent 2015; 114(3): 346-50.
[http://dx.doi.org/10.1016/j.prosdent.2015.04.002] [PMID: 26050027]
[6]
Menini M, Setti P, Pera P, Pera F, Pesce P. Peri-implant tissue health and bone resorption in patients with immediately loaded, implant-supported, full-arch prostheses. Int J Prosthodont 2018; 31(4): 327-33.
[http://dx.doi.org/10.11607/ijp.5567] [PMID: 29953561]
[7]
Williams SD, Hughes TE, Adler CJ, Brook AH, Townsend GC. Epigenetics: A new frontier in dentistry. Aust Dent J 2014; 59(Suppl. 1): 23-33.
[http://dx.doi.org/10.1111/adj.12155] [PMID: 24611746]
[8]
Barros SP, Offenbacher S. Epigenetics: Connecting environment and genotype to phenotype and disease. J Dent Res 2009; 88(5): 400-8.
[http://dx.doi.org/10.1177/0022034509335868] [PMID: 19493882]
[9]
Sartori EM, das Neves AM, Magro-Filho O, et al. The role of microRNAs in the osseointegration process. Int J Oral Maxillofac Implants 2019; 34(2): 397-410.
[http://dx.doi.org/10.11607/jomi.6581] [PMID: 30883619]
[10]
Asa’ad F, Monje A, Larsson L. Role of epigenetics in alveolar bone resorption and regeneration around periodontal and peri-implant tissues. Eur J Oral Sci 2019; 127(6): 477-93.
[http://dx.doi.org/10.1111/eos.12657] [PMID: 31701573]
[11]
Shookhoff JM, Gallicano GI. The emerging role of microRNAs in adult stem cells. Stem Cell Biology and Regenerative Medicine. Humana Press: New York, NY, USA; Springer: Berlin, Germany 2011; 1: pp. 57-94.
[http://dx.doi.org/10.1007/978-1-61779-002-7_3]
[12]
Pasquinelli AE, Reinhart BJ, Slack F, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000; 408(6808): 86-9.
[http://dx.doi.org/10.1038/35040556] [PMID: 11081512]
[13]
Osada H, Takahashi T. MicroRNAs in biological processes and carcinogenesis. Carcinogenesis 2007; 28(1): 2-12.
[http://dx.doi.org/10.1093/carcin/bgl185] [PMID: 17028302]
[14]
Izzotti A. Molecular medicine and the development of cancer chemopreventive agents. Ann N Y Acad Sci 2012; 1259: 26-32.
[http://dx.doi.org/10.1111/j.1749-6632.2012.06646.x] [PMID: 22758633]
[15]
Di Gianfilippo R. The use of MiRNAs as activators of dental implant surfaces, a review. Int J of Bone Mineral Metabolism 2018; 1(1): 2-9.
[16]
Weber JA, Baxter DH, Zhang S, et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010; 56(11): 1733-41.
[http://dx.doi.org/10.1373/clinchem.2010.147405] [PMID: 20847327]
[17]
Katchy A, Williams C. Expression profiles of estrogen-regulated microRNAs in breast cancer cells. Methods Mol Biol 2016; 1366: 373-93.
[http://dx.doi.org/10.1007/978-1-4939-3127-9_30] [PMID: 26585151]
[18]
Gulyaeva LF, Kushlinskiy NE. Regulatory mechanisms of microRNA expression. J Transl Med 2016; 14(1): 143.
[http://dx.doi.org/10.1186/s12967-016-0893-x] [PMID: 27197967]
[19]
Lu TX, Rothenberg ME. MicroRNA. J Allergy Clin Immunol 2018; 141(4): 1202-7.
[http://dx.doi.org/10.1016/j.jaci.2017.08.034] [PMID: 29074454]
[20]
Kebschull M, Papapanou PN. Mini but mighty: MicroRNAs in the pathobiology of periodontal disease. Periodontol 2000 2015; 69(1): 201-20.
[http://dx.doi.org/10.1111/prd.12095] [PMID: 26252410]
[21]
Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: Approaches and considerations. Nat Rev Genet 2012; 13(5): 358-69.
[http://dx.doi.org/10.1038/nrg3198] [PMID: 22510765]
[22]
Kim SH, Lee SY, Lee YM, Lee YK. MicroRNAs as biomarkers for dental diseases. Singapore Dent J 2015; 36: 18-22.
[http://dx.doi.org/10.1016/j.sdj.2015.09.001] [PMID: 26684491]
[23]
Liu C, Tong Z, Tan J, Xin Z, Wang Z, Tian L. MicroRNA-21-5p targeting PDCD4 suppresses apoptosis via regulating the PI3K/AKT/FOXO1 signaling pathway in tongue squamous cell carcinoma. Exp Ther Med 2019; 18(5): 3543-51.
[http://dx.doi.org/10.3892/etm.2019.7970] [PMID: 31602231]
[24]
Menini M, De Giovanni E, Bagnasco F, et al. Salivary micro-RNA and oral squamous cell carcinoma: A systematic review. J Pers Med 2021; 11(2): 101.
[http://dx.doi.org/10.3390/jpm11020101] [PMID: 33557138]
[25]
Gombos K, Horváth R, Szele E, et al. miRNA expression profiles of oral squamous cell carcinomas. Anticancer Res 2013; 33(4): 1511-7.
[PMID: 23564792]
[26]
Roy R, De Sarkar N, Ghose S, et al. Association between risk of oral precancer and genetic variations in microRNA and related processing genes. J Biomed Sci 2014; 21: 48.
[http://dx.doi.org/10.1186/1423-0127-21-48] [PMID: 24885463]
[27]
Babu JM, Prathibha R, Jijith VS, Hariharan R, Pillai MR. A miR- centric view of head and neck cancers. Biochim Biophys Acta (BBA)- Rev Can 2011; 1816(1): 67-72.
[28]
Heah KG, Shobri NRBT, Suhaimi SNB, et al. A review of microRNA associated with oral cancer. J Int Dental and Medical Res 2019; 12: 738-43.
[29]
Li Y, Zhou X, St John MA, Wong DT. RNA profiling of cell-free saliva using microarray technology. J Dent Res 2004; 83(3): 199-203.
[http://dx.doi.org/10.1177/154405910408300303] [PMID: 14981119]
[30]
Park NJ, Zhou H, Elashoff D, et al. Salivary microRNA: Discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res 2009; 15(17): 5473-7.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-0736] [PMID: 19706812]
[31]
Patel RS, Jakymiw A, Yao B, et al. High resolution of microRNA signatures in human whole saliva. Arch Oral Biol 2011; 56(12): 1506-13.
[http://dx.doi.org/10.1016/j.archoralbio.2011.05.015] [PMID: 21704302]
[32]
Liu CJ, Lin SC, Yang CC, Cheng HW, Chang KW. Exploiting salivary miR-31 as a clinical biomarker of oral squamous cell carcinoma. Head Neck 2012; 34(2): 219-24.
[http://dx.doi.org/10.1002/hed.21713] [PMID: 22083872]
[33]
Yoshizawa JM, Wong DT. Salivary microRNAs and oral cancer detection. Methods Mol Biol 2013; 936: 313-24.
[http://dx.doi.org/10.1007/978-1-62703-083-0_24] [PMID: 23007518]
[34]
Drury RE, O’Connor D, Pollard AJ. The clinical application of microRNAs in infectious disease. Front Immunol 2017; 8: 1182.
[http://dx.doi.org/10.3389/fimmu.2017.01182] [PMID: 28993774]
[35]
Ogata Y, Matsui S, Kato A, Zhou L, Nakayama Y, Takai H. MicroRNA expression in inflamed and noninflamed gingival tissues from Japanese patients. J Oral Sci 2014; 56(4): 253-60.
[http://dx.doi.org/10.2334/josnusd.56.253] [PMID: 25500922]
[36]
Asa’ad F, Garaicoa-Pazmiño C, Dahlin C, et al. Expression of MicroRNAs in periodontal and peri-implant diseases: A systematic review and meta-analysis. Int J Mol Sci 2020; 21(11): 4147.
[http://dx.doi.org/10.3390/ijms21114147] [PMID: 32532036]
[37]
Nahid MA, Rivera M, Lucas A, Chan EKL, Kesavalu L. Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease. Infect Immun 2011; 79(4): 1597-605.
[http://dx.doi.org/10.1128/IAI.01062-10] [PMID: 21263019]
[38]
Honda T, Takahashi N, Miyauchi S, Yamazaki K. Porphyromonas gingivalis lipopolysaccharide induces miR-146a without altering the production of inflammatory cytokines. Biochem Biophys Res Commun 2012; 420(4): 918-25.
[http://dx.doi.org/10.1016/j.bbrc.2012.03.102] [PMID: 22480686]
[39]
Sun M, Ma Y, Cai Z, Yang Z. MiR-218 promotes osteogenic differentiation of periodontal ligament stem cell through activation of Wnt signaling by targeting SFRP2. Int J Clin Exp Pathol 2016; 9: 10188-96.
[40]
Liu F, Wang ZF, Liu FF, Xu JZ, Liu Q, Lan J. MicroRNA-29a-3p regulates osteoblast differentiation and peri-implant osseointegration in a rat model of hyperlipidemia by modulating Frizzled 4 expression. Hua Xi Kou Qiang Yi Xue Za Zhi 2019; 37(2): 200-7.
[PMID: 31168988]
[41]
Menini M, Dellepiane E, Chvartszaid D, Baldi D, Schiavetti I, Pera P. Influence of different surface characteristics on peri-implant tissue behavior: A six-year prospective report. Int J Prosthodont 2015; 28(4): 389-95.
[http://dx.doi.org/10.11607/ijp.4066] [PMID: 26218023]
[42]
Baldi D, Longobardi M, Cartiglia C, et al. Dental implants osteogenic properties evaluated by cDNA microarrays. Implant Dent 2011; 20(4): 299-305.
[http://dx.doi.org/10.1097/ID.0b013e318225f22b] [PMID: 21778890]
[43]
Iaculli F, Di Filippo ES, Piattelli A, Mancinelli R, Fulle S. Dental pulp stem cells grown on dental implant titanium surfaces: An in vitro evaluation of differentiation and microRNAs expression. J Biomed Mater Res B Appl Biomater 2017; 105(5): 953-65.
[http://dx.doi.org/10.1002/jbm.b.33628] [PMID: 26856387]
[44]
Gardin C, Ferroni L, Piattelli A, et al. Non-Washed Resorbable Blasting Media (NWRBM) on titanium surfaces could enhance osteogenic properties of MSCs through increase of miRNA-196a and VCAM1. Stem Cell Rev Rep 2016; 12(5): 543-52.
[http://dx.doi.org/10.1007/s12015-016-9669-1] [PMID: 27318850]
[45]
Chakravorty N, Ivanovski S, Prasadam I, Crawford R, Oloyede A, Xiao Y. The microRNA expression signature on modified titanium implant surfaces influences genetic mechanisms leading to osteogenic differentiation. Acta Biomater 2012; 8(9): 3516-23.
[http://dx.doi.org/10.1016/j.actbio.2012.05.008] [PMID: 22588073]
[46]
Wimmers Ferreira MR, Rodrigo Fernandes R, Freire Assis A, et al. Oxidative nanopatterning of titanium surface influences mRNA and microRNA expression in human alveolar bone osteoblastic cells. Int J Biomater 2016; 2016: 9169371.
[http://dx.doi.org/10.1155/2016/9169371] [PMID: 27200092]
[47]
Sartori EM, Magro-Filho O, Silveira Mendonça DB, et al. Modulation of Micro RNA expression and osteoblast differentiation by nanotopography. Int J Oral Maxillofac Implants 2018; 33(2): 269-80.
[http://dx.doi.org/10.11607/jomi.5372] [PMID: 29534118]
[48]
Kato RB, Roy B, De Oliveira FS, et al. Nanotopography directs mesenchymal stem cells to osteoblast lineage through regulation of microRNA-SMAD-BMP-2 circuit. J Cell Physiol 2014; 229(11): 1690-6.
[http://dx.doi.org/10.1002/jcp.24614] [PMID: 24619927]
[49]
Kato RB, Roy B, De Oliveira FS, et al. Erratum: Nanotopography directs mesenchymal stem cells to osteoblast lineage through regulation of microRNA-SMAD-BMP-2 circuit. J Cell Physiol 2016; 231(11): 2548.
[http://dx.doi.org/10.1002/jcp.25474] [PMID: 27420802]
[50]
Yang J, McNamara LE, Gadegaard N, et al. Nanotopographical induction of osteogenesis through adhesion, bone morphogenic protein cosignaling, and regulation of microRNAs. ACS Nano 2014; 8(10): 9941-53.
[http://dx.doi.org/10.1021/nn504767g] [PMID: 25227207]
[51]
Palmieri A, Pezzetti F, Brunelli G, et al. Short-period effects of zirconia and titanium on osteoblast microRNAs. Clin Implant Dent Relat Res 2008; 10(3): 200-5.
[http://dx.doi.org/10.1111/j.1708-8208.2007.00078.x] [PMID: 18241218]
[52]
Palmieri A, Pezzetti F, Brunelli G, et al. Zirconium oxide regulates RNA interfering of osteoblast-like cells. J Mater Sci Mater Med 2008; 19(6): 2471-6.
[http://dx.doi.org/10.1007/s10856-008-3386-5] [PMID: 18253813]
[53]
Cossellu G, Motta V, Dioni L, et al. Titanium and zirconium levels are associated with changes in microRNAs expression: Results from a human cross-sectional study on obese population. PLoS One 2016; 11(9): e0161916.
[http://dx.doi.org/10.1371/journal.pone.0161916] [PMID: 27611787]
[54]
Du W, Su L, Zhang N, Wang H. Exosomes derived from preadipocytes improve osteogenic differentiation, potentially via reduced miR-223 expression. Mol Med Rep 2019; 19(2): 951-8.
[PMID: 30569151]
[55]
Ghassib I, Chen Z, Zhu J, Wang HL. Use of IL-1 β, IL-6, TNF-α, and MMP-8 biomarkers to distinguish peri-implant diseases: A systematic review and meta-analysis. Clin Implant Dent Relat Res 2019; 21(1): 190-207.
[http://dx.doi.org/10.1111/cid.12694] [PMID: 30508312]
[56]
Menini M, Dellepiane E, Baldi D, Longobardi MG, Pera P, Izzotti A. Microarray expression in peri-implant tissue next to different titanium implant surfaces predicts clinical outcomes: A split-mouth study. Clin Oral Implants Res 2017; 28(9): e121-34.
[http://dx.doi.org/10.1111/clr.12943] [PMID: 27492799]
[57]
Menini M, Pesce P, Baldi D, et al. Prediction of titanium implant success by analysis of microrna expression in peri-implant tissue. A 5-year follow-up study. J Clin Med 2019; 8(6): 888.
[http://dx.doi.org/10.3390/jcm8060888] [PMID: 31234311]
[58]
Wu X, Chen X, Mi W, Wu T, Gu Q, Huang H. MicroRNA sequence analysis identifies microRNAs associated with peri-implantitis in dogs. Biosci Rep 2017; 37(5): 1-12.
[http://dx.doi.org/10.1042/BSR20170768] [PMID: 28864780]
[59]
Wu X, Gu Q, Chen X, Mi W, Wu T, Huang H. MiR-27a targets DKK2 and SFRP1 to promote reosseointegration in the regenerative treatment of peri-implantitis. J Bone Miner Res 2019; 34(1): 123-34.
[http://dx.doi.org/10.1002/jbmr.3575] [PMID: 30151888]
[60]
Kadkhodazadeh M, Jafari AR, Amid R, et al. MiR146a and MiR499 gene polymorphisms in Iranian periodontitis and peri-implantitis patients. J Long Term Eff Med Implants 2013; 23(1): 9-16.
[http://dx.doi.org/10.1615/JLongTermEffMedImplants.2013007073] [PMID: 24266439]
[61]
Izzotti A, Carozzo S, Pulliero A, Zhabayeva D, Ravetti JL, Bersimbaev R. Extracellular MicroRNA in liquid biopsy: Applicability in cancer diagnosis and prevention. Am J Cancer Res 2016; 6(7): 1461-93.
[PMID: 27508091]
[62]
Heitzer E, Haque IS, Roberts CES, Speicher MR. Current and future perspectives of liquid biopsies in genomics-driven oncology. Nat Rev Genet 2019; 20(2): 71-88.
[http://dx.doi.org/10.1038/s41576-018-0071-5] [PMID: 30410101]
[63]
Chen M, Zhao H. Next-generation sequencing in liquid biopsy: Cancer screening and early detection. Hum Genomics 2019; 13(1): 34.
[http://dx.doi.org/10.1186/s40246-019-0220-8] [PMID: 31370908]
[64]
Mendioroz M, Martínez-Merino L, Blanco-Luquin I, Urdánoz A, Roldán M, Jericó I. Liquid biopsy: A new source of candidate biomarkers in amyotrophic lateral sclerosis. Ann Clin Transl Neurol 2018; 5(6): 763-8.
[http://dx.doi.org/10.1002/acn3.565] [PMID: 29928659]
[65]
Duarte PM, Serrão CR, Miranda TS, et al. Could cytokine levels in the peri-implant crevicular fluid be used to distinguish between healthy implants and implants with peri-implantitis? A systematic review. J Periodontal Res 2016; 51(6): 689-98.
[http://dx.doi.org/10.1111/jre.12354] [PMID: 26774043]
[66]
Menini M, Pesce P, Pera F, et al. 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 2020.
[67]
Wu K, Song W, Zhao L, et al. MicroRNA functionalized microporous titanium oxide surface by lyophilization with enhanced osteogenic activity. ACS Appl Mater Interfaces 2013; 5(7): 2733-44.
[http://dx.doi.org/10.1021/am400374c] [PMID: 23459382]
[68]
Wu K, Liu M, Li N, et al. Chitosan-miRNA functionalized microporous titanium oxide surfaces via a layer-by-layer approach with a sustained release profile for enhanced osteogenic activity. J Nanobiotechnology 2020; 18(1): 127.
[http://dx.doi.org/10.1186/s12951-020-00674-7] [PMID: 32907598]
[69]
Yan J, Chang B, Hu X, Cao C, Zhao L, Zhang Y. Titanium implant functionalized with antimiR-138 delivered cell sheet for enhanced peri-implant bone formation and vascularization. Mater Sci Eng C 2018; 89: 52-64.
[http://dx.doi.org/10.1016/j.msec.2018.03.011] [PMID: 29752119]
[70]
Liu X, Tan N, Zhou Y, et al. Delivery of antagomiR204-conjugated gold nanoparticles from PLGA sheets and its implication in promoting osseointegration of titanium implant in type 2 diabetes mellitus. Int J Nanomedicine 2017; 12: 7089-101.
[http://dx.doi.org/10.2147/IJN.S124584] [PMID: 29026303]
[71]
Shao D, Wang C, Sun Y, Cui L. Effects of oral implants with miR-122-modified cell sheets on rat bone marrow mesenchymal stem cells. Mol Med Rep 2018; 17(1): 1537-44.
[PMID: 29257226]
[72]
Eskildsen T, Taipaleenmäki H, Stenvang J, et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci USA 2011; 108(15): 6139-44.
[http://dx.doi.org/10.1073/pnas.1016758108] [PMID: 21444814]
[73]
Wang Z, Wu G, Feng Z, et al. 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 2015; 10(10): 6675-87.
[PMID: 26604744]
[74]
Si YJ, Ren QH, Bi L. miR-135b-5p regulates human mesenchymal stem cell osteogenic differentiation by facilitating the Hippo signaling pathway. Int J Clin Exp Pathol 2017; 10(7): 7767-75.
[PMID: 31966624]
[75]
Ren H, Huo F, Wang Z, et al. Sdccag3 promotes implant osseointegration during experimental hyperlipidemia. J Dent Res 2020; 99(8): 938-48.
[http://dx.doi.org/10.1177/0022034520916400] [PMID: 32339468]
[76]
Ma X, Bian Y, Yuan H, et al. Human amnion-derived mesenchymal stem cells promote osteogenic differentiation of human bone marrow mesenchymal stem cells via H19/miR-675/APC axis. Aging (Albany NY) 2020; 12(11): 10527-43.
[http://dx.doi.org/10.18632/aging.103277] [PMID: 32434960]
[77]
Razzouk S, Sarkis R. Smoking and diabetes. Epigenetics involvement in osseointegration. N Y State Dent J 2013; 79(2): 27-30.
[PMID: 23691725]
[78]
Monje A, Asa’ad F, Larsson L, Giannobile WV, Wang HL. Epigenetics: A missing link between periodontitis and peri-implantitis? Int J Periodont Restor Dent 2018; 38(4): 476-7.
[http://dx.doi.org/10.11607/prd.2018.4.e] [PMID: 29999503]
[79]
Izzotti A, Longobardi M, La Maestra S, et al. Release of microRNAs into body fluids from ten organs of mice exposed to cigarette smoke. Theranostics 2018; 8(8): 2147-60.
[http://dx.doi.org/10.7150/thno.22726] [PMID: 29721069]

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