Circulating miR-135b as a Biomarker of Obesity-Related Insulin Resistance and Dyslipidemia in Children and Adolescents
-
Pegah Golpour
,
Saeedeh Moradgholi
,
Zahra Arab Sadeghabadi
,
Mona Nourbakhsh
,
Mitra Nourbakhsh
,
Zeynab Yousefi
,
Maryam Razzaghy-Azar
Abstract
Objective: Childhood obesity is a global health concern associated with long-term metabolic complications. MicroRNA-135b (miR-135b) has been implicated in regulating adipogenesis, glucose metabolism, and insulin signaling, partly by directly targeting SIRT1, a key metabolic regulator that plays a crucial role in energy homeostasis and inflammation. However, the role of miR-135b in pediatric obesity remains unclear. This study aimed to investigate circulating miR-135b level and its relationship with SIRT1 expression, lipid profile, and glycemic parameters in children and adolescents with obesity.
Methods: A total of 67 participants (36 obese and 31 normal-weight controls) aged 8–16 years were enrolled. Anthropometric measurements and biochemical analyses were performed. miR-135b and SIRT1 expression levels were measured using quantitative real-time PCR. Insulin resistance was assessed using HOMA-IR, and metabolic syndrome was diagnosed based on International Diabetes Federation criteria.
Results: miR-135b expression was significantly elevated in the obesity group compared to controls and was highest among participants with insulin resistance and metabolic syndrome. Elevated miR-135b correlated positively with BMI z-score, insulin levels, HOMA-IR, total cholesterol, triglycerides, and LDL-C, while showing no significant correlation with HDL-C. In contrast, SIRT1 expression was significantly decreased in obese individuals (p = 0.0026) and inversely correlated with miR-135b levels.
Conclusion: Elevated miR-135b and reduced SIRT1 expression are associated with obesity-related metabolic disturbances in children and adolescents. These findings suggest that the miR-135b/SIRT1 axis may play a pivotal role in the development of insulin resistance and dyslipidemia, highlighting miR-135b as a potential biomarker and therapeutic target for early intervention in pediatric obesity.
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9. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature. 2004;429(6993):771-6. https://doi.org/10.1038/nature02583.
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14. Lu L, He Y. Dysregulation of miR-335-5p in People with Obesity and its Predictive Value for Metabolic Syndrome. Horm Metab Res. 2024;56(10):749-55. https://doi.org/10.1055/a-2261-8115.
15. Vonhögen IGC, Mohseni Z, Winkens B, Xiao K, Thum T, Calore M, et al. Circulating miR-216a as a biomarker of metabolic alterations and obesity in women. Non-coding RNA Res. 2020;5(3):144-52. https://doi.org/https://doi.org/10.1016/j.ncrna.2020.08.001.
16. Abu-Farha M, Cherian P, Al-Khairi I, Nizam R, Alkandari A, Arefanian H, et al. Reduced miR-181d level in obesity and its role in lipid metabolism via regulation of ANGPTL3. Sci Rep. 2019;9(1):11866. https://doi.org/10.1038/s41598-019-48371-2.
17. Ojeda-Rodríguez A, Assmann TS, Alonso-Pedrero L, Azcona-Sanjulian MC, Milagro FI, Marti A. Circulating miRNAs in girls with abdominal obesity: miR-221-3p as a biomarker of response to weight loss interventions. Pediatr Obes. 2022;17(8):e12910. https://doi.org/https://doi.org/10.1111/ijpo.12910.
18. Zhuang G, Meng C, Guo X, Cheruku PS, Shi L, Xu H, et al. A Novel Regulator of Macrophage Activation. Circulation. 2012;125(23):2892-903. https://doi.org/10.1161/CIRCULATIONAHA.111.087817.
19. Price NL, Holtrup B, Kwei SL, Wabitsch M, Rodeheffer M, Bianchini L, et al. SREBP-1c/MicroRNA 33b Genomic Loci Control Adipocyte Differentiation. Mol Cell Biol. 2016;36(7):1180-93. https://doi.org/10.1128/MCB.00745-15.
20. Lin Y-Y, Chou C-F, Giovarelli M, Briata P, Gherzi R, Chen C-Y. KSRP and MicroRNA 145 Are Negative Regulators of Lipolysis in White Adipose Tissue. Mol Cell Biol. 2014;34(12):2339-49. https://doi.org/10.1128/MCB.00042-14.
21. Yang W-M, Jeong H-J, Park S-W, Lee W. Obesity-induced miR-15b is linked causally to the development of insulin resistance through the repression of the insulin receptor in hepatocytes. Mol Nutr Food Res. 2015;59(11):2303-14. https://doi.org/https://doi.org/10.1002/mnfr.201500107.
22. Yousefi Z, Nourbakhsh M, Abdolvahabi Z, Ghorbanhosseini S-S, Hesari Z, Yarahmadi S, et al. microRNA-141 is associated with hepatic steatosis by downregulating the sirtuin1/AMP-activated protein kinase pathway in hepatocytes. J Cell Physiol. 2020;235(2):880-90. https://doi.org/10.1002/jcp.29002.
23. Borji M, Nourbakhsh M, Shafiee SM, Owji AA, Abdolvahabi Z, Hesari Z, et al. Down-Regulation of SIRT1 Expression by mir-23b Contributes to Lipid Accumulation in HepG2 Cells. Biochem Genet. 2019;57(4):507-21. https://doi.org/10.1007/s10528-019-09905-5.
24. Abdolvahabi Z, Nourbakhsh M, Hosseinkhani S, Hesari Z, Alipour M, Jafarzadeh M, et al. MicroRNA‐590‐3P suppresses cell survival and triggers breast cancer cell apoptosis via targeting sirtuin‐1 and deacetylation of p53. J Cell Biochem. 2018;120(6):9356-68. https://doi.org/10.1002/jcb.28211
25. Zhang Q, Ye X, Xu X, Yan J. Placenta-derived exosomal miR-135a-5p promotes gestational diabetes mellitus pathogenesis by activating PI3K/AKT signalling pathway via SIRT1. J Cell Mol Med. 2023;27(23):3729-43. https://doi.org/10.1111/jcmm.17941.
26. Zhang J, Zhang L, Zha D, Wu X. Inhibition of miRNA‑135a‑5p ameliorates TGF‑β1‑induced human renal fibrosis by targeting SIRT1 in diabetic nephropathy. Int J Mol Med. 2020;46(3):1063-73. https://doi.org/10.3892/ijmm.2020.4647.
27. Chen ACH, Peng Q, Fong SW, Yeung WSB, Lee YL. Sirt1 is regulated by miR-135a and involved in DNA damage repair during mouse cellular reprogramming. Aging (Albany NY). 2020;12(8):7431-47. https://doi.org/10.18632/aging.103090.
28. Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C. Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics. 2005;115(4):e500-e3. https://doi.org/10.1542/peds.2004-1921
29. Gao S, Yang D, Huang W, Wang T, Li W. miR-135a-5p affects adipogenic differentiation of human adipose-derived mesenchymal stem cellsby promoting the Hippo signaling pathway. Int J Clin Exp Pathol. 2018;11(3):1347-55.
30. Chen C, Peng Y, Peng Y, Peng J, Jiang S. miR-135a-5p inhibits 3T3-L1 adipogenesis through activation of canonical Wnt/β-catenin signaling. J Mol Endocrinol. 2014;52(3):311-20. https://doi.org/10.1530/jme-14-0013.
31. Beilerli A, Kudriashov V, Sufianov A, Kostin A, Begliarzade S, Ilyasova T, et al. Regulation and mechanism of action of miRNAs on insulin resistance in skeletal muscles. Non-coding RNA Res. 2023;8(2):218-23. https://doi.org/https://doi.org/10.1016/j.ncrna.2023.02.005.
32. Agarwal P, Srivastava R, Srivastava AK, Ali S, Datta M. miR-135a targets IRS2 and regulates insulin signaling and glucose uptake in the diabetic gastrocnemius skeletal muscle. Biochim Biophys Acta. 2013;1832(8):1294-303. https://doi.org/10.1016/j.bbadis.2013.03.021.
33. Honardoost M, Arefian E, Soleimani M, Soudi S, Sarookhani MR. Development of Insulin Resistance through Induction of miRNA-135 in C2C12 Cells. Cell J. 2016;18(3):353-61. https://doi.org/10.22074/cellj.2016.4563.
34. Lu Q, Shen Q, Su J, Li X, Xia B, Tang A. Inhibition of mir-155-5p alleviates cardiomyocyte pyroptosis induced by hypoxia/reoxygenation via targeting SIRT1-mediated activation of the NLRP3 inflammasome. J Cardiothorac Surg. 2025;20(1):135. https://doi.org/10.1186/s13019-025-03366-1.
35. Martinez-Arroyo O, Flores-Chova A, Mendez-Debaets M, Garcia-Ferran L, Escrivá L, Forner MJ, et al. Inhibiting miR-200a-3p Increases Sirtuin 1 and Mitigates Kidney Injury in a Tubular Cell Model of Diabetes and Hypertension-Related Renal Damage. Biomolecules. 2025;15(7). https://doi.org/10.3390/biom15070995.
36. Lee YH, Lee J, Jeong J, Park K, Baik B, Kwon Y, et al. Hepatic miR-93 promotes the pathogenesis of metabolic dysfunction-associated steatotic liver disease by suppressing SIRT1. Metabolism. 2025;169:156266. https://doi.org/10.1016/j.metabol.2025.156266.
37. Du J, Cao L, Zhou J, Liao Z, Hu B, Zhou K, et al. The emerging role of miR-22 in inflammation. Biomed Pharmacother. 2025;191:118482. https://doi.org/10.1016/j.biopha.2025.118482.
38. Ding T, Zeng L, Xia Y, Zhang B, Cui D. miR-135a Mediates Mitochondrial Oxidative Respiratory Function through SIRT1 to Regulate Atrial Fibrosis. Cardiology. 2024;149(3):286-96. https://doi.org/10.1159/000536059.
2. Mendis S, Graham I, Branca F, Collins T, Tukuitonga C, Gunawardane A, Narula J. Alarming Rise of Obesity: The 4(th) United Nations High-Level Meeting on Noncommunicable Diseases and Mental Health Should Advance Action to Tackle Obesity. Glob Heart. 2025;20(1):70. https://doi.org/10.5334/gh.1459.
3. Münte E, Zhang X, Khurana A, Hartmann P. Prevalence of Extremely Severe Obesity and Metabolic Dysfunction Among US Children and Adolescents. JAMA Netw Open. 2025;8(7):e2521170. https://doi.org/10.1001/jamanetworkopen.2025.21170.
4. Zhang B, Shi H, Cai W, Yang B, Xiu W. Metabolic syndrome in children and adolescents: definitions, epidemiology, pathophysiology, interventions, and challenges. Front Endocrinol (Lausanne). 2025;16:1512642. https://doi.org/10.3389/fendo.2025.1512642.
5. Pfluger PT, Herranz D, Velasco-Miguel S, Serrano M, Tschöp MH. Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci U S A. 2008;105(28):9793-8. https://doi.org/10.1073/pnas.0802917105.
6. Purushotham A, Schug TT, Xu Q, Surapureddi S, Guo X, Li X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 2009;9(4):327-38. https://doi.org/10.1016/j.cmet.2009.02.006.
7. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006;444(7117):337-42. https://doi.org/10.1038/nature05354.
8. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127(6):1109-22. https://doi.org/10.1016/j.cell.2006.11.013.
9. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature. 2004;429(6993):771-6. https://doi.org/10.1038/nature02583.
10. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell. 2007;6(6):759-67. https://doi.org/10.1111/j.1474-9726.2007.00335.x.
11. Banks AS, Kon N, Knight C, Matsumoto M, Gutiérrez-Juárez R, Rossetti L, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8(4):333-41. https://doi.org/10.1016/j.cmet.2008.08.014.
12. Sandoval-Bórquez A, Carrión P, Hernández MP, Pérez JA, Tapia-Castillo A, Vecchiola A, et al. Adipose Tissue Dysfunction and the Role of Adipocyte-Derived Extracellular Vesicles in Obesity and Metabolic Syndrome. J Endocr Soc. 2024;8(8):bvae126. https://doi.org/10.1210/jendso/bvae126.
13. Engin AB, Engin A. MicroRNAs as Epigenetic Regulators of Obesity. Adv Exp Med Biol. 2024;1460:595-627. https://doi.org/10.1007/978-3-031-63657-8_20.
14. Lu L, He Y. Dysregulation of miR-335-5p in People with Obesity and its Predictive Value for Metabolic Syndrome. Horm Metab Res. 2024;56(10):749-55. https://doi.org/10.1055/a-2261-8115.
15. Vonhögen IGC, Mohseni Z, Winkens B, Xiao K, Thum T, Calore M, et al. Circulating miR-216a as a biomarker of metabolic alterations and obesity in women. Non-coding RNA Res. 2020;5(3):144-52. https://doi.org/https://doi.org/10.1016/j.ncrna.2020.08.001.
16. Abu-Farha M, Cherian P, Al-Khairi I, Nizam R, Alkandari A, Arefanian H, et al. Reduced miR-181d level in obesity and its role in lipid metabolism via regulation of ANGPTL3. Sci Rep. 2019;9(1):11866. https://doi.org/10.1038/s41598-019-48371-2.
17. Ojeda-Rodríguez A, Assmann TS, Alonso-Pedrero L, Azcona-Sanjulian MC, Milagro FI, Marti A. Circulating miRNAs in girls with abdominal obesity: miR-221-3p as a biomarker of response to weight loss interventions. Pediatr Obes. 2022;17(8):e12910. https://doi.org/https://doi.org/10.1111/ijpo.12910.
18. Zhuang G, Meng C, Guo X, Cheruku PS, Shi L, Xu H, et al. A Novel Regulator of Macrophage Activation. Circulation. 2012;125(23):2892-903. https://doi.org/10.1161/CIRCULATIONAHA.111.087817.
19. Price NL, Holtrup B, Kwei SL, Wabitsch M, Rodeheffer M, Bianchini L, et al. SREBP-1c/MicroRNA 33b Genomic Loci Control Adipocyte Differentiation. Mol Cell Biol. 2016;36(7):1180-93. https://doi.org/10.1128/MCB.00745-15.
20. Lin Y-Y, Chou C-F, Giovarelli M, Briata P, Gherzi R, Chen C-Y. KSRP and MicroRNA 145 Are Negative Regulators of Lipolysis in White Adipose Tissue. Mol Cell Biol. 2014;34(12):2339-49. https://doi.org/10.1128/MCB.00042-14.
21. Yang W-M, Jeong H-J, Park S-W, Lee W. Obesity-induced miR-15b is linked causally to the development of insulin resistance through the repression of the insulin receptor in hepatocytes. Mol Nutr Food Res. 2015;59(11):2303-14. https://doi.org/https://doi.org/10.1002/mnfr.201500107.
22. Yousefi Z, Nourbakhsh M, Abdolvahabi Z, Ghorbanhosseini S-S, Hesari Z, Yarahmadi S, et al. microRNA-141 is associated with hepatic steatosis by downregulating the sirtuin1/AMP-activated protein kinase pathway in hepatocytes. J Cell Physiol. 2020;235(2):880-90. https://doi.org/10.1002/jcp.29002.
23. Borji M, Nourbakhsh M, Shafiee SM, Owji AA, Abdolvahabi Z, Hesari Z, et al. Down-Regulation of SIRT1 Expression by mir-23b Contributes to Lipid Accumulation in HepG2 Cells. Biochem Genet. 2019;57(4):507-21. https://doi.org/10.1007/s10528-019-09905-5.
24. Abdolvahabi Z, Nourbakhsh M, Hosseinkhani S, Hesari Z, Alipour M, Jafarzadeh M, et al. MicroRNA‐590‐3P suppresses cell survival and triggers breast cancer cell apoptosis via targeting sirtuin‐1 and deacetylation of p53. J Cell Biochem. 2018;120(6):9356-68. https://doi.org/10.1002/jcb.28211
25. Zhang Q, Ye X, Xu X, Yan J. Placenta-derived exosomal miR-135a-5p promotes gestational diabetes mellitus pathogenesis by activating PI3K/AKT signalling pathway via SIRT1. J Cell Mol Med. 2023;27(23):3729-43. https://doi.org/10.1111/jcmm.17941.
26. Zhang J, Zhang L, Zha D, Wu X. Inhibition of miRNA‑135a‑5p ameliorates TGF‑β1‑induced human renal fibrosis by targeting SIRT1 in diabetic nephropathy. Int J Mol Med. 2020;46(3):1063-73. https://doi.org/10.3892/ijmm.2020.4647.
27. Chen ACH, Peng Q, Fong SW, Yeung WSB, Lee YL. Sirt1 is regulated by miR-135a and involved in DNA damage repair during mouse cellular reprogramming. Aging (Albany NY). 2020;12(8):7431-47. https://doi.org/10.18632/aging.103090.
28. Keskin M, Kurtoglu S, Kendirci M, Atabek ME, Yazici C. Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents. Pediatrics. 2005;115(4):e500-e3. https://doi.org/10.1542/peds.2004-1921
29. Gao S, Yang D, Huang W, Wang T, Li W. miR-135a-5p affects adipogenic differentiation of human adipose-derived mesenchymal stem cellsby promoting the Hippo signaling pathway. Int J Clin Exp Pathol. 2018;11(3):1347-55.
30. Chen C, Peng Y, Peng Y, Peng J, Jiang S. miR-135a-5p inhibits 3T3-L1 adipogenesis through activation of canonical Wnt/β-catenin signaling. J Mol Endocrinol. 2014;52(3):311-20. https://doi.org/10.1530/jme-14-0013.
31. Beilerli A, Kudriashov V, Sufianov A, Kostin A, Begliarzade S, Ilyasova T, et al. Regulation and mechanism of action of miRNAs on insulin resistance in skeletal muscles. Non-coding RNA Res. 2023;8(2):218-23. https://doi.org/https://doi.org/10.1016/j.ncrna.2023.02.005.
32. Agarwal P, Srivastava R, Srivastava AK, Ali S, Datta M. miR-135a targets IRS2 and regulates insulin signaling and glucose uptake in the diabetic gastrocnemius skeletal muscle. Biochim Biophys Acta. 2013;1832(8):1294-303. https://doi.org/10.1016/j.bbadis.2013.03.021.
33. Honardoost M, Arefian E, Soleimani M, Soudi S, Sarookhani MR. Development of Insulin Resistance through Induction of miRNA-135 in C2C12 Cells. Cell J. 2016;18(3):353-61. https://doi.org/10.22074/cellj.2016.4563.
34. Lu Q, Shen Q, Su J, Li X, Xia B, Tang A. Inhibition of mir-155-5p alleviates cardiomyocyte pyroptosis induced by hypoxia/reoxygenation via targeting SIRT1-mediated activation of the NLRP3 inflammasome. J Cardiothorac Surg. 2025;20(1):135. https://doi.org/10.1186/s13019-025-03366-1.
35. Martinez-Arroyo O, Flores-Chova A, Mendez-Debaets M, Garcia-Ferran L, Escrivá L, Forner MJ, et al. Inhibiting miR-200a-3p Increases Sirtuin 1 and Mitigates Kidney Injury in a Tubular Cell Model of Diabetes and Hypertension-Related Renal Damage. Biomolecules. 2025;15(7). https://doi.org/10.3390/biom15070995.
36. Lee YH, Lee J, Jeong J, Park K, Baik B, Kwon Y, et al. Hepatic miR-93 promotes the pathogenesis of metabolic dysfunction-associated steatotic liver disease by suppressing SIRT1. Metabolism. 2025;169:156266. https://doi.org/10.1016/j.metabol.2025.156266.
37. Du J, Cao L, Zhou J, Liao Z, Hu B, Zhou K, et al. The emerging role of miR-22 in inflammation. Biomed Pharmacother. 2025;191:118482. https://doi.org/10.1016/j.biopha.2025.118482.
38. Ding T, Zeng L, Xia Y, Zhang B, Cui D. miR-135a Mediates Mitochondrial Oxidative Respiratory Function through SIRT1 to Regulate Atrial Fibrosis. Cardiology. 2024;149(3):286-96. https://doi.org/10.1159/000536059.
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| Issue | Vol 3 No 4 (2025) | |
| Section | Original Articles | |
| Keywords | ||
| miR-135b Obesity Sirtuin 1 Metabolic syndrome Insulin resistance | ||
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How to Cite
1.
Golpour P, Moradgholi S, Arab Sadeghabadi Z, Nourbakhsh M, Nourbakhsh M, Yousefi Z, Razzaghy-Azar M. Circulating miR-135b as a Biomarker of Obesity-Related Insulin Resistance and Dyslipidemia in Children and Adolescents. ABI. 2025;3(4):226-234.
