DOI QR코드

DOI QR Code

MicroRNAs and periodontal disease: a qualitative systematic review of human studies

  • Mico-Martinez, Pablo (Department of Stomatology, Faculty of Medicine and Dentistry, University of Valencia) ;
  • Alminana-Pastor, Pedro J. (Department of Stomatology, Faculty of Medicine and Dentistry, University of Valencia) ;
  • Alpiste-Illueca, Francisco (Department of Stomatology, Faculty of Medicine and Dentistry, University of Valencia) ;
  • Lopez-Roldan, Andres (Department of Stomatology, Faculty of Medicine and Dentistry, University of Valencia)
  • Received : 2020.12.14
  • Accepted : 2021.05.28
  • Published : 2021.12.31

Abstract

Purpose: MicroRNAs (miRNAs) are epigenetic post-transcriptional regulators that modulate gene expression and have been identified as biomarkers for several diseases, including cancer. This study aimed to systematically review the relationship between miRNAs and periodontal disease in humans, and to evaluate the potential of miRNAs as diagnostic and prognostic biomarkers of disease. Methods: The review was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines (reference number CRD42020180683). The MEDLINE, Scopus, Cochrane Library, Embase, Web of Science, and SciELO databases were searched for clinical studies conducted in humans investigating periodontal diseases and miRNAs. Expression levels of miRNAs across the different groups were analysed using the collected data. Results: A total of 1,299 references were identified in the initial literature search, and 23 articles were finally included in the review. The study designs were heterogeneous, which prevented a meta-analysis of the data. Most of the studies compared miRNA expression levels between patients with periodontitis and healthy controls. The most widely researched miRNA in periodontal diseases was miR-146a. Most studies reported higher expression levels of miR-146a in patients with periodontitis than in healthy controls. In addition, many studies also focused on identifying target genes of the differentially expressed miRNAs that were significantly related to periodontal inflammation. Conclusions: The results of the studies that we analysed are promising, but diagnostic tests are needed to confirm the use of miRNAs as biomarkers to monitor and aid in the early diagnosis of periodontitis in clinical practice.

Keywords

References

  1. Chapple ILC, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007;43:160-232. https://doi.org/10.1111/j.1600-0757.2006.00178.x
  2. Preshaw PM, Seymour RA, Heasman PA. Current concepts in periodontal pathogenesis. Dent Update 2004;31:570-2, 574-8. https://doi.org/10.12968/denu.2004.31.10.570
  3. Van Dyke TE. Commentary: periodontitis is characterized by an immuno-inflammatory host-mediated destruction of bone and connective tissues that support the teeth. J Periodontol 2014;85:509-11. https://doi.org/10.1902/jop.2014.130701
  4. Huang W, He BY, Shao J, Jia XW, Yuan YD. Interleukin-1β rs1143627 polymorphism with susceptibility to periodontal disease. Oncotarget 2017;8:31406-14. https://doi.org/10.18632/oncotarget.15612
  5. Rodenhiser D, Mann M. Epigenetics and human disease: translating basic biology into clinical applications. CMAJ 2006;174:341-8. https://doi.org/10.1503/cmaj.050774
  6. Behm-Ansmant I, Rehwinkel J, Izaurralde E. MicroRNAs silence gene expression by repressing protein expression and/or by promoting mRNA decay. Cold Spring Harb Symp Quant Biol 2006;71:523-30. https://doi.org/10.1101/sqb.2006.71.013
  7. Alminana-Pastor PJ, Boronat-Catala M, Mico-Martinez P, Bellot-Arcis C, Lopez-Roldan A, Alpiste-Illueca FM. Epigenetics and periodontics: a systematic review. Med Oral Patol Oral Cir Bucal 2019;24:e659-72.
  8. Dai R, Ahmed SA. MicroRNA, a new paradigm for understanding immunoregulation, inflammation, and autoimmune diseases. Transl Res 2011;157:163-79. https://doi.org/10.1016/j.trsl.2011.01.007
  9. Hammond SM. An overview of microRNAs. Adv Drug Deliv Rev 2015;87:3-14. https://doi.org/10.1016/j.addr.2015.05.001
  10. Palanisamy V, Jakymiw A, Van Tubergen EA, D'Silva NJ, Kirkwood KL. Control of cytokine mRNA expression by RNA-binding proteins and microRNAs. J Dent Res 2012;91:651-8. https://doi.org/10.1177/0022034512437372
  11. Peng Y, Croce CM. The role of MicroRNAs in human cancer. Signal Transduct Target Ther 2016;1:15004. https://doi.org/10.1038/sigtrans.2015.4
  12. Melak T, Baynes HW. Circulating microRNAs as possible biomarkers for coronary artery disease: a narrative review. EJIFCC 2019;30:179-94.
  13. Poy MN, Spranger M, Stoffel M. microRNAs and the regulation of glucose and lipid metabolism. Diabetes Obes Metab 2007;9 Suppl 2:67-73. https://doi.org/10.1111/j.1463-1326.2007.00775.x
  14. Keller A, Leidinger P, Bauer A, Elsharawy A, Haas J, Backes C, et al. Toward the blood-borne miRNome of human diseases. Nat Methods 2011;8:841-3. https://doi.org/10.1038/nmeth.1682
  15. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6. https://doi.org/10.1902/annals.1999.4.1.1
  16. 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;56:253-60. https://doi.org/10.2334/josnusd.56.253
  17. Venugopal P, Lavu V, Rao SR, Venkatesan V. Association of microRNA-125a and microRNA-499a polymorphisms in chronic periodontitis in a sample south Indian population: a hospital-based genetic association study. Gene 2017;631:10-5. https://doi.org/10.1016/j.gene.2017.07.053
  18. Kalea AZ, Hoteit R, Suvan J, Lovering RC, Palmen J, Cooper JA, et al. Upregulation of gingival tissue miR-200b in obese periodontitis subjects. J Dent Res 2015;94:59S-69S. https://doi.org/10.1177/0022034514568197
  19. Naqvi AR, Brambila MF, Martinez G, Chapa G, Nares S. Dysregulation of human miRNAs and increased prevalence of HHV miRNAs in obese periodontitis subjects. J Clin Periodontol 2019;46:51-61. https://doi.org/10.1111/jcpe.13040
  20. Perri R, Nares S, Zhang S, Barros SP, Offenbacher S. MicroRNA modulation in obesity and periodontitis. J Dent Res 2012;91:33-8. https://doi.org/10.1177/0022034511425045
  21. Radovic N, Nikolic Jakoba N, Petrovic N, Milosavljevic A, Brkovic B, Roganovic J. MicroRNA-146a and microRNA-155 as novel crevicular fluid biomarkers for periodontitis in non-diabetic and type 2 diabetic patients. J Clin Periodontol 2018;45:663-71. https://doi.org/10.1111/jcpe.12888
  22. Bagavad Gita J, George AV, Pavithra N, Chandrasekaran SC, Latchumanadhas K, Gnanamani A. Dysregulation of miR-146a by periodontal pathogens: A risk for acute coronary syndrome. J Periodontol 2019;90:756-65. https://doi.org/10.1002/JPER.18-0466
  23. Yagnik K, Mahendra J, Kurian VM. The periodontal-cardiovascular alliance: evaluation of miRNA-146a in subgingival plaque samples of chronic periodontitis patients with and without coronary heart disease. J Investig Clin Dent 2019;10:e12442.
  24. Chen H, Lan Z, Li Q, Li Y. Abnormal expression of long noncoding RNA FGD5-AS1 affects the development of periodontitis through regulating miR-142-3p/SOCS6/NF-κB pathway. Artif Cells Nanomed Biotechnol 2019;47:2098-106. https://doi.org/10.1080/21691401.2019.1620256
  25. Ghotloo S, Motedayyen H, Amani D, Saffari M, Sattari M. Assessment of microRNA-146a in generalized aggressive periodontitis and its association with disease severity. J Periodontal Res 2019;54:27-32. https://doi.org/10.1111/jre.12538
  26. Kadkhodazadeh M, Jafari AR, Amid R, Ebadian AR, Alipour MM, Mollaverdi F, et al. MiR146a and MiR499 gene polymorphisms in Iranian periodontitis and peri-implantitis patients. J Long Term Eff Med Implants 2013;23:9-16. https://doi.org/10.1615/JLongTermEffMedImplants.2013007073
  27. Lee YH, Na HS, Jeong SY, Jeong SH, Park HR, Chung J. Comparison of inflammatory microRNA expression in healthy and periodontitis tissues. Biocell 2011;35:43-9. https://doi.org/10.32604/biocell.2011.35.043
  28. Li J, Wang R, Ge Y, Chen D, Wu B, Fang F. Assessment of microRNA-144-5p and its putative targets in inflamed gingiva from chronic periodontitis patients. J Periodontal Res 2019;54:266-77. https://doi.org/10.1111/jre.12627
  29. Mico-Martinez P, Garcia-Gimenez JL, Seco-Cervera M, Lopez-Roldan A, Alminana-Pastor PJ, AlpisteIllueca F, et al. miR-1226 detection in GCF as potential biomarker of chronic periodontitis: a pilot study. Med Oral Patol Oral Cir Bucal 2018;23:e308-14.
  30. Motedayyen H, Ghotloo S, Saffari M, Sattari M, Amid R. Evaluation of microRNA-146a and its targets in gingival tissues of patients with chronic periodontitis. J Periodontol 2015;86:1380-5. https://doi.org/10.1902/jop.2015.150319
  31. Na HS, Park MH, Song YR, Kim S, Kim HJ, Lee JY, et al. Elevated microrna-128 in periodontitis mitigates tumor necrosis factor-α response via p38 signaling pathway in macrophages. J Periodontol 2016;87:e173-82. https://doi.org/10.1902/jop.2016.160033
  32. Nisha KJ, Janam P, Harshakumar K. Identification of a novel salivary biomarker miR-143-3p for periodontal diagnosis: a proof of concept study. J Periodontol 2019;90:1149-59. https://doi.org/10.1002/JPER.18-0729
  33. Saito A, Horie M, Ejiri K, Aoki A, Katagiri S, Maekawa S, et al. MicroRNA profiling in gingival crevicular fluid of periodontitis-a pilot study. FEBS Open Bio 2017;7:981-94. https://doi.org/10.1002/2211-5463.12238
  34. Stoecklin-Wasmer C, Guarnieri P, Celenti R, Demmer RT, Kebschull M, Papapanou PN. MicroRNAs and their target genes in gingival tissues. J Dent Res 2012;91:934-40. https://doi.org/10.1177/0022034512456551
  35. Venugopal P, Koshy T, Lavu V, Ranga Rao S, Ramasamy S, Hariharan S, et al. Differential expression of microRNAs let-7a, miR-125b, miR-100, and miR-21 and interaction with NF-kB pathway genes in periodontitis pathogenesis. J Cell Physiol 2018;233:5877-84. https://doi.org/10.1002/jcp.26391
  36. Xie YF, Shu R, Jiang SY, Liu DL, Zhang XL. Comparison of microRNA profiles of human periodontal diseased and healthy gingival tissues. Int J Oral Sci 2011;3:125-34. https://doi.org/10.4248/IJOS11046
  37. Yoneda T, Tomofuji T, Ekuni D, Azuma T, Maruyama T, Fujimori K, et al. Serum microRNAs and chronic periodontitis: a case-control study. Arch Oral Biol 2019;101:57-63. https://doi.org/10.1016/j.archoralbio.2019.03.009
  38. Venugopal P, Lavu V, RangaRao S, Venkatesan V. Evaluation of a panel of single-nucleotide polymorphisms in miR-146a and miR-196a2 genomic regions in patients with chronic periodontitis. Genet Test Mol Biomarkers 2017;21:228-35. https://doi.org/10.1089/gtmb.2016.0358
  39. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006;103:12481-6. https://doi.org/10.1073/pnas.0605298103
  40. Asa'ad F, Garaicoa-Pazmino C, Dahlin C, Larsson L. Expression of microRNAs in periodontal and peri-implant diseases: a systematic review and meta-analysis. Int J Mol Sci 2020;21:4147. https://doi.org/10.3390/ijms21114147