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Investigation of salivary miRNA-199a-5p levels in plaque-induced gingivitis

Yıl 2025, Cilt: 7 Sayı: 3, 369 - 374, 30.05.2025

Fatma Tuba Akdeniz , Ahmet Mert Nalbantoğlu , Zerrin Barut , Şule Bulut , Orçun Avşar , Hilal Korkmaz Karadeniz , Turgay İsbir

Öz

Aims: Epigenetic mechanisms play a crucial role in regulating the response to chronic inflammation in periodontal diseases and serve as reliable biomarkers. While these biomarkers are traditionally assessed through invasive techniques, analyzing miRNA expression in saliva offers a non-invasive and convenient alternative. Our study aims to investigate salivary miRNA-199a-5p levels in both healthy and diseased conditions and to evaluate its potential role as an early diagnostic indicator of periodontal diseases such as gingivitis.
Methods: Saliva samples from 50 individuals, either diagnosed with gingivitis or exhibiting a healthy periodontal condition, were analyzed using miRNeasy serum/plasma kit (Qiagen). SPSS software was used for statistical analysis. MiRNA-199a-5p expression levels were compared using the Mann-Whitney U test.
Results: In saliva samples collected from 50 individuals, the expression levels of miRNA-199a-5p were significantly elevated in the gingivitis group compared to the healthy control group. Aditionally, the bleeding on probing (BOP %) values were significantly higher in group G compared to the healthy group.
Conclusion: miRNA-199a-5p can be considered an important regulator with potential as both an early diagnostic biomarker and a therapeutic target for periodontal diseases. Although its role in autophagy and inflammation shows promise, further studies are needed to clarify its specific functions and clinical relevance.

Anahtar Kelimeler

miRNA-199a-5p gingivitis periodontal disease

Etik Beyan

Ethics Committee Approval This research was carried out in compliance with the principles outlined in the Declaration of Helsinki. Ethical approval for this study was obtained from the Non-Interventional Clinical Research Ethics Committee of Hitit University (Date: 05.12.2024, Decision No: 323/2024-25).

Kaynakça

  • Belibasakis GN, Charalampakis G, Bostanci N, Stadlinger B. Peri-implant infections of oral biofilm etiology. Adv Exp Med Biol. 2015;830: 69-84. doi:10.1007/978-3-319-11038-7_4
  • Weidlich P, Lopes De Souza MA, Oppermann RV. Evaluation of the dentogingival area during early plaque formation. J Periodontol. 2001; 72(7):901-910. doi:10.1902/jop.2001.72.7.901
  • Löe H, Theilade E, Jensen SB. Experimental gingivitis in man. J Periodontol. 1965;36(3):177-187. doi: 10.1902/jop.1965.36.3.177
  • Yamamoto SL. Periodontal disease: symptoms, treatment, and prevention. Hauppauge, NY: Nova Science Publishers. 2010.
  • Maqbool R, Hussain MU. MicroRNAs and human diseases: diagnostic and therapeutic potential. Cell Tissue Res. 2014;358(1):1-15. doi:10.1007/s00441-013-1787-3
  • Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014; 42(Database issue):D68-D73. doi:10.1093/nar/gkt1181
  • García-Giménez JL, Seco-Cervera M, Tollefsbol TO, et al. Epigenetic biomarkers: current strategies and future challenges for their use in the clinical laboratory. Crit Res Clin Lab Sci. 2017;54(7-8):529-550. doi:10.1080/10408363.2017.1410520
  • O'Brien J, Hayder H, Zayed Y, et al. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402. doi:10.3389/fendo.2018.00402
  • Meyle J, Chapple I. Molecular aspects of the pathogenesis of periodontitis. Periodontol 2000. 2015;69(1):7-17. doi:10.1111/prd.12104
  • Park MG, Kim JS, Park SY, et al. microRNA-27 promotes the differentiation of odontoblastic cell by targeting APC and activating Wnt/β-catenin signaling. Gene. 2014;538(2):266-272. doi:10.1016/j.gene. 2014.01.045
  • Nahid MA, Rivera M, Lucas A, et al. Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE−/− mice during experimental periodontal disease. Infect Immun. 2011;79(4):1597-1605. doi:10.1128/IAI.01062-10
  • Zhu L, Xu H, Lv W, et al. miR-199b-5p regulates immune-mediated allograft rejection after lung transplantation through the GSK3β and NF-κB pathways. Inflammation. 2018;41(4):1524-1535. doi:10.1007/s10753-018-0799-2
  • Motedayyen, H, Ghotloo S, Saffari M, et al. Evaluation of MicroRNA-146a and its targets in gingival tissues of patients with chronic periodontitis. J Periodontol. 2015;86(12):1380-1385. doi:10.1902/jop. 2015.150319
  • Wang Q, Ye B, Wang P, et al. Overview of microRNA-199a regulation in cancer. Cancer Manag Res. 2019;10;11:10327-10335. doi:10.2147/CMAR.S231971
  • Jiang Q, Huang Yu W, Huang R, et al. mTOR signaling in the regulation of CD4+ T cell subsets in periodontal diseases. Front Immunol. 2022;13: 827461. doi:10.3389/fimmu.2022.827461
  • Kim YC, Guan K L. mTOR: a pharmacologic target for autophagy regulation. J Clin Iinvest. 2015;125(1):25-32. doi:10.1172/JCI73939
  • Deleyto-Seldas N, Efeyan A. The mTOR-autophagy axis and the control of metabolism. Front Cell Dev Biol. 2020;9:655731. doi:10.3389/fcell. 2021.655731
  • Chen R, Alvero AB, Silasi DA, et al. Regulation of IKKbeta by miR-199a affects NF-kappaB activity in ovarian cancer cells. Oncogene. 2008; 27(34):4712-4723. doi:10.1038/onc.2008.112
  • Lu H, Yang Y, Ou S, et al. The silencing of miR-199a-5p protects the articular cartilage through MAPK4 in osteoarthritis. Ann Transl Med. 2022;10(10):601. doi:10.21037/atm-22-2057
  • Garabet L, Rangber A, Eriksson AM, et al. MicroRNA-199a-5p may be a diagnostic biomarker of primary ITP. Br J Haematol. 2025;206(5):1443-1449. doi:10.1111/bjh.19987
  • Zhao DY, Zho L, Yin TF, et al. Circulating miR-627-5p and miR-199a-5p are promising diagnostic biomarkers of colorectal neoplasia. World J Clin Cases. 2022;10(16):5165-5184. doi:10.12998/wjcc.v10.i16.5165
  • Almiñana-Pastor PJ, Boronat-Catalá M, Micó-Martinez P, et al. Epigenetics and periodontics: a systematic review. Med Oral Patol Oral Cir Bucal. 2019;24(5):e659-e672. doi:10.4317/medoral.23008
  • De Souza AP, Planello AC, Marques MR, et al. High-throughput DNA analysis shows the importance of methylation in the control of immune inflammatory gene transcription in chronic periodontitis. Clin Epigenetics. 2014;6(1):15. doi:10.1186/1868-7083-6-15
  • Li H, Deng Y, Sun K, et al. Structural basis of kindlin-mediated integrin recognition and activation. Proc Natl Acad Sci USA. 2017;114(35): 93499354. doi:10.1073/pnas.1703064114
  • Chapple ILC, Mealey BL, Van Dyke TE, et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: consensus report of workgroup 1 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(Suppl 1):S74-S84. doi:10.1002/JPER.17-0719
  • Silness J, Löe H. Periodontal disease in pregnancy. II. correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22(1):121-135. doi:10.3109/00016356408993968
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408. doi:10.1006/meth.2001.1262
  • Kim SH, Lee SY, Lee YM, et al. MicroRNAs as biomarkers for dental diseases. Singapore Dent J. 2015;36:18-22. doi:10.1016/j.sdj.2015.09.001
  • García-Giménez J, Sanchis-Gomar F, Lippi G, et al. Epigenetic biomarkers: a new perspective in laboratory diagnostics. Clin Chim Acta. 2012;413(19-20):1576-1582. doi:10.1016/j.cca.2012.05.0
  • Irwandi RA, Vacharaksa A. The role of microRNA in periodontal tissue: a review of the literature. Arch Oral Biol. 2016;72:66-74. doi:10.1016/j.archoralbio.2016.08.014
  • Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 2009;1(6):a001651. doi:10.1101/cshperspect.a001651
  • Barut Z, Akdeniz FT, Avsar O, Cabbar AT. Investigation of miRNA-199a-5p expression and its clinical association with LDL cholesterol levels in atherosclerosis. In Vivo. 2024;38(6):2656-2664. doi:10.21873/invivo.13742
  • Dolz S, Górriz D, Tembl JI, et al. Circulating microRNAs as novel biomarkers of stenosis progression in asymptomatic carotid stenosis. Storke. 2017;48(1):10-16. doi:10.1161/STROKEAHA.116.013650
  • Almiñana-Pastor PJ, Alpiste-Illueca FM, Micó-Martinez P, et al. MicroRNAs in gingival crevicular fluid: an observational case-control study of differential expressionin periodontitis. Noncoding RNA. 2023; 9(6):73. doi:10.3390/ncrna9060073
  • Cinpolat O, Unal ZN, Ismi O, et al. Comparison of microRNA profiles between benign and malignant salivary gland tumors in tissue, blood and saliva samples: a prospective, case-control study. Braz J Otorhinolaryngo. 2017;83(3):276-284. doi:10.1016/j.bjorl.2016.03.013
  • Yuan Y, Li N, Zeng L, et al. Pathogenesis investigation of miR-199-5p in oral submucous fibrosis based on bioinformatics analysis. Oral Dis. 2019;25(2):456-465. doi:10.1111/odi.13008
  • Quadri MFA, Kamel AM, Nayeem M, et al. Smokeless tobacco and periodontitis: a systematic review with meta-analysis. J Periodontal Res. 2024;59(6):1062-1070. doi:10.1111/jre.13274
  • Al-Rawi NH, Rizvi Z, Mkadmi S, et al. Differential expression profile of salivary oncomiRNAs among smokeless tobacco users. Eur J Dent. 2023;17(04):1215-1220. doi:10.1055/s-0043-1761191
  • Li Y, He Y, Xiang J, et al. The functional mechanism of microRNA in oral lichen planus. J Inflamm Res. 2022;4261-4274. doi:10.2147/JIR.S369304
  • Wang L, Wu W, Chen J, et al. miR 122 and miR 199 synergistically promote autophagy in oral lichen planus by targeting the Akt/mTOR pathway. Int J Mol Med. 2019;43(3):1373-1381. doi:10.3892/ijmm.2019. 4068
  • Rovas A, Puriene A, Snipaitiene K, et al. Analysis of periodontitis-associated miRNAs in gingival tissue, gingival crevicular fluid, saliva and blood plasma. Arch Oral Biol. 2021;126:105125. doi:10.1016/j.archoralbio.2021.105125
  • Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(Suppl 1):173-S182. doi:10.1002/JPER.17-0721

Yıl 2025, Cilt: 7 Sayı: 3, 369 - 374, 30.05.2025

Fatma Tuba Akdeniz , Ahmet Mert Nalbantoğlu , Zerrin Barut , Şule Bulut , Orçun Avşar , Hilal Korkmaz Karadeniz , Turgay İsbir

Öz

Kaynakça

  • Belibasakis GN, Charalampakis G, Bostanci N, Stadlinger B. Peri-implant infections of oral biofilm etiology. Adv Exp Med Biol. 2015;830: 69-84. doi:10.1007/978-3-319-11038-7_4
  • Weidlich P, Lopes De Souza MA, Oppermann RV. Evaluation of the dentogingival area during early plaque formation. J Periodontol. 2001; 72(7):901-910. doi:10.1902/jop.2001.72.7.901
  • Löe H, Theilade E, Jensen SB. Experimental gingivitis in man. J Periodontol. 1965;36(3):177-187. doi: 10.1902/jop.1965.36.3.177
  • Yamamoto SL. Periodontal disease: symptoms, treatment, and prevention. Hauppauge, NY: Nova Science Publishers. 2010.
  • Maqbool R, Hussain MU. MicroRNAs and human diseases: diagnostic and therapeutic potential. Cell Tissue Res. 2014;358(1):1-15. doi:10.1007/s00441-013-1787-3
  • Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014; 42(Database issue):D68-D73. doi:10.1093/nar/gkt1181
  • García-Giménez JL, Seco-Cervera M, Tollefsbol TO, et al. Epigenetic biomarkers: current strategies and future challenges for their use in the clinical laboratory. Crit Res Clin Lab Sci. 2017;54(7-8):529-550. doi:10.1080/10408363.2017.1410520
  • O'Brien J, Hayder H, Zayed Y, et al. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402. doi:10.3389/fendo.2018.00402
  • Meyle J, Chapple I. Molecular aspects of the pathogenesis of periodontitis. Periodontol 2000. 2015;69(1):7-17. doi:10.1111/prd.12104
  • Park MG, Kim JS, Park SY, et al. microRNA-27 promotes the differentiation of odontoblastic cell by targeting APC and activating Wnt/β-catenin signaling. Gene. 2014;538(2):266-272. doi:10.1016/j.gene. 2014.01.045
  • Nahid MA, Rivera M, Lucas A, et al. Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE−/− mice during experimental periodontal disease. Infect Immun. 2011;79(4):1597-1605. doi:10.1128/IAI.01062-10
  • Zhu L, Xu H, Lv W, et al. miR-199b-5p regulates immune-mediated allograft rejection after lung transplantation through the GSK3β and NF-κB pathways. Inflammation. 2018;41(4):1524-1535. doi:10.1007/s10753-018-0799-2
  • Motedayyen, H, Ghotloo S, Saffari M, et al. Evaluation of MicroRNA-146a and its targets in gingival tissues of patients with chronic periodontitis. J Periodontol. 2015;86(12):1380-1385. doi:10.1902/jop. 2015.150319
  • Wang Q, Ye B, Wang P, et al. Overview of microRNA-199a regulation in cancer. Cancer Manag Res. 2019;10;11:10327-10335. doi:10.2147/CMAR.S231971
  • Jiang Q, Huang Yu W, Huang R, et al. mTOR signaling in the regulation of CD4+ T cell subsets in periodontal diseases. Front Immunol. 2022;13: 827461. doi:10.3389/fimmu.2022.827461
  • Kim YC, Guan K L. mTOR: a pharmacologic target for autophagy regulation. J Clin Iinvest. 2015;125(1):25-32. doi:10.1172/JCI73939
  • Deleyto-Seldas N, Efeyan A. The mTOR-autophagy axis and the control of metabolism. Front Cell Dev Biol. 2020;9:655731. doi:10.3389/fcell. 2021.655731
  • Chen R, Alvero AB, Silasi DA, et al. Regulation of IKKbeta by miR-199a affects NF-kappaB activity in ovarian cancer cells. Oncogene. 2008; 27(34):4712-4723. doi:10.1038/onc.2008.112
  • Lu H, Yang Y, Ou S, et al. The silencing of miR-199a-5p protects the articular cartilage through MAPK4 in osteoarthritis. Ann Transl Med. 2022;10(10):601. doi:10.21037/atm-22-2057
  • Garabet L, Rangber A, Eriksson AM, et al. MicroRNA-199a-5p may be a diagnostic biomarker of primary ITP. Br J Haematol. 2025;206(5):1443-1449. doi:10.1111/bjh.19987
  • Zhao DY, Zho L, Yin TF, et al. Circulating miR-627-5p and miR-199a-5p are promising diagnostic biomarkers of colorectal neoplasia. World J Clin Cases. 2022;10(16):5165-5184. doi:10.12998/wjcc.v10.i16.5165
  • Almiñana-Pastor PJ, Boronat-Catalá M, Micó-Martinez P, et al. Epigenetics and periodontics: a systematic review. Med Oral Patol Oral Cir Bucal. 2019;24(5):e659-e672. doi:10.4317/medoral.23008
  • De Souza AP, Planello AC, Marques MR, et al. High-throughput DNA analysis shows the importance of methylation in the control of immune inflammatory gene transcription in chronic periodontitis. Clin Epigenetics. 2014;6(1):15. doi:10.1186/1868-7083-6-15
  • Li H, Deng Y, Sun K, et al. Structural basis of kindlin-mediated integrin recognition and activation. Proc Natl Acad Sci USA. 2017;114(35): 93499354. doi:10.1073/pnas.1703064114
  • Chapple ILC, Mealey BL, Van Dyke TE, et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: consensus report of workgroup 1 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(Suppl 1):S74-S84. doi:10.1002/JPER.17-0719
  • Silness J, Löe H. Periodontal disease in pregnancy. II. correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22(1):121-135. doi:10.3109/00016356408993968
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408. doi:10.1006/meth.2001.1262
  • Kim SH, Lee SY, Lee YM, et al. MicroRNAs as biomarkers for dental diseases. Singapore Dent J. 2015;36:18-22. doi:10.1016/j.sdj.2015.09.001
  • García-Giménez J, Sanchis-Gomar F, Lippi G, et al. Epigenetic biomarkers: a new perspective in laboratory diagnostics. Clin Chim Acta. 2012;413(19-20):1576-1582. doi:10.1016/j.cca.2012.05.0
  • Irwandi RA, Vacharaksa A. The role of microRNA in periodontal tissue: a review of the literature. Arch Oral Biol. 2016;72:66-74. doi:10.1016/j.archoralbio.2016.08.014
  • Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 2009;1(6):a001651. doi:10.1101/cshperspect.a001651
  • Barut Z, Akdeniz FT, Avsar O, Cabbar AT. Investigation of miRNA-199a-5p expression and its clinical association with LDL cholesterol levels in atherosclerosis. In Vivo. 2024;38(6):2656-2664. doi:10.21873/invivo.13742
  • Dolz S, Górriz D, Tembl JI, et al. Circulating microRNAs as novel biomarkers of stenosis progression in asymptomatic carotid stenosis. Storke. 2017;48(1):10-16. doi:10.1161/STROKEAHA.116.013650
  • Almiñana-Pastor PJ, Alpiste-Illueca FM, Micó-Martinez P, et al. MicroRNAs in gingival crevicular fluid: an observational case-control study of differential expressionin periodontitis. Noncoding RNA. 2023; 9(6):73. doi:10.3390/ncrna9060073
  • Cinpolat O, Unal ZN, Ismi O, et al. Comparison of microRNA profiles between benign and malignant salivary gland tumors in tissue, blood and saliva samples: a prospective, case-control study. Braz J Otorhinolaryngo. 2017;83(3):276-284. doi:10.1016/j.bjorl.2016.03.013
  • Yuan Y, Li N, Zeng L, et al. Pathogenesis investigation of miR-199-5p in oral submucous fibrosis based on bioinformatics analysis. Oral Dis. 2019;25(2):456-465. doi:10.1111/odi.13008
  • Quadri MFA, Kamel AM, Nayeem M, et al. Smokeless tobacco and periodontitis: a systematic review with meta-analysis. J Periodontal Res. 2024;59(6):1062-1070. doi:10.1111/jre.13274
  • Al-Rawi NH, Rizvi Z, Mkadmi S, et al. Differential expression profile of salivary oncomiRNAs among smokeless tobacco users. Eur J Dent. 2023;17(04):1215-1220. doi:10.1055/s-0043-1761191
  • Li Y, He Y, Xiang J, et al. The functional mechanism of microRNA in oral lichen planus. J Inflamm Res. 2022;4261-4274. doi:10.2147/JIR.S369304
  • Wang L, Wu W, Chen J, et al. miR 122 and miR 199 synergistically promote autophagy in oral lichen planus by targeting the Akt/mTOR pathway. Int J Mol Med. 2019;43(3):1373-1381. doi:10.3892/ijmm.2019. 4068
  • Rovas A, Puriene A, Snipaitiene K, et al. Analysis of periodontitis-associated miRNAs in gingival tissue, gingival crevicular fluid, saliva and blood plasma. Arch Oral Biol. 2021;126:105125. doi:10.1016/j.archoralbio.2021.105125
  • Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(Suppl 1):173-S182. doi:10.1002/JPER.17-0721
Toplam 42 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Dental Materyaller
Bölüm Research Articles
Yazarlar

Fatma Tuba Akdeniz 0000-0002-6076-0509

Ahmet Mert Nalbantoğlu 0000-0002-0505-867X

Zerrin Barut 0000-0002-6289-5562

Şule Bulut 0000-0002-8808-0185

Orçun Avşar 0000-0003-3556-6218

Hilal Korkmaz Karadeniz 0000-0001-9886-5843

Turgay İsbir 0000-0002-7350-6032

Yayımlanma Tarihi 30 Mayıs 2025
Gönderilme Tarihi 15 Nisan 2025
Kabul Tarihi 29 Mayıs 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 7 Sayı: 3

Kaynak Göster

AMA Akdeniz FT, Nalbantoğlu AM, Barut Z, Bulut Ş, Avşar O, Korkmaz Karadeniz H, İsbir T. Investigation of salivary miRNA-199a-5p levels in plaque-induced gingivitis. Anatolian Curr Med J / ACMJ / acmj. Mayıs 2025;7(3):369-374.
 Kapak Resmi İndir

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