MiR-506 targets polypyrimidine tract-binding protein 1 to inhibit airway inflammatory response and remodeling via mediating Wnt/β-catenin signaling pathway
Main Article Content
Keywords
airway smooth -muscle cells, childhood asthma, miR-506, PTBP1, Wnt/β-catenin
Abstract
Background: Airway remodeling, which contributes to the clinical course of childhood asthma, occurs due to airway inflammation and is featured by anomalous biological behaviors of airway smooth muscle cells (ASMCs). microRNA (miRNA) plays an essential role in the etiopathogenesis of asthma.
Objective: This research was aimed to characterize miR-506 in asthma and uncover potential regulatory machinery.
Material and methods: The asthmatic cell model was established by treating ASMCs with transforming growth factor-beta1 (TGF-β1) and assessed by the levels of interleukin (IL)-1β and interferon gamma (IFN-γ). Using real-time quantitative polymerase chain reaction, mRNA expression of miR-506 and polypyrimidine tract-binding protein 1 (PTBP1) was measured. Cell counting kit-8 and Transwell migration tests were used for estimating the capacity of ASMCs to proliferate and migrate. Luciferase reporter assay was used to corroborate whether miR-506 was directly bound to PTBP1. Expression of PTBP1, collagen I and III, and essential proteins of the wingless-related integration (Wnt)/β-catenin pathway (β-catenin, c-MYC and cyclin D1) was accomplished by Western blot analysis. The involvement of Wnt/β-catenin signaling in asthma was confirmed by Wnt signaling pathway inhibitor (IWR-1).
Results: miR-506 was poorly expressed in asthmatic tissues and cell model. Functionally, overexpression of miR-506 reduced aberrant proliferation, migration, inflammation and collagen deposition of ASMCs triggered by TGF-β1. Mechanically, miR-506 directly targeted the 3’ untranslated region (3-UTR) of PTBP1 and had a negative regulation on PTBP1 expression. Moreover, overexpression of miR-506 suppressed the induction of Wnt/β-catenin pathway. The administration of IWR-1 further validated negative correlation between miR-506 and the Wnt/β-catenin pathway in asthma.
Conclusion: Our data indicated that targeting miR-506/PTBP1/Wnt/β-catenin axis might point in a helpful direction for treating asthma in children.
References
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43. Ding Y, Gao S, Zheng J, Chen X. Blocking lncRNA-SNHG16 sensitizes gastric cancer cells to 5-Fu through targeting the miR-506-3p-PTBP1-mediated glucose metabolism. Cancer Metab. 2022 Nov;10(1):20. 10.1186/s40170-022-00293-w.
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2. Barnes PJ. Endogenous inhibitory mechanisms in asthma. Am J Respir Crit Care Med. 2000 Mar;161(2):S176–81. 10.1164/ajrccm.161.supplement_2.a1q4-6
3. Liu Y, Miao Y, Gao X, Wang YY, Wang H, Zheng YW, et al. MicroRNA-200a affects the proliferation of airway smooth muscle cells and airway remodeling by targeting FOXC1 via the PI3K/AKT signaling pathway in ovalbumin-induced asthmatic mice. Cell Physiol Biochem. 2018 Nov;50(6):2365–89. 10.1159/000495097
4. Chen YF, Huang G, Wang YM, Cheng M, Zhu FF, Zhong JN, et al. Exchange protein directly activated by cAMP (Epac) protects against airway inflammation and airway remodeling in asthmatic mice. Respir Res. 2019 Dec;20(1):285. 10.1186/s12931-019-1260-2
5. Munitz A, Karo-Atar D, Foster PS. Asthma diagnosis: MicroRNAs to the rescue. JJ Allergy Clin Immunol. 2016 May;137(5):1447–48. 10.1016/j.jaci.2016.02.013
6. Perry MM, Baker JE, Gibeon DS, Adcock IM, Chung KF. Airway smooth muscle hyperproliferation is regulated by microRNA-221 in severe asthma. Am J Respir Cell Mol Biol. 2014 Jan;50(1):7–17. 10.1165/rcmb.2013-0067OC
7. Gao Y, Wang B, Luo H, Zhang Q, Xu M. miR-217 represses TGF-β1-induced airway smooth muscle cell proliferation and migration through targeting ZEB1. Biomed Pharmacother. 2018 Dec;108:27–35. 10.1016/j.biopha.2018.09.030
8. Peng T, Zhou L, Zuo L, Luan Y. MiR-506 functions as a tumor suppressor in glioma by targeting STAT3. Oncol Rep. 2016 Feb;35(2):1057–64. 10.3892/or.2015.4406
9. Guo S, Yang P, Jiang X, Li X, Wang Y, Zhang X, et al. Genetic and epigenetic silencing of mircoRNA-506-3p enhances COTL1 oncogene expression to foster non-small lung cancer progression. Oncotarget. 2017 Jan;8(1):644–57. 10.18632/oncotarget.13501
10. Hossian A, Sajib MS, Tullar PE, Mikelis CM, Mattheolabakis G. Multipronged activity of combinatorial miR-143 and miR-506 inhibits lung cancer cell cycle progression and angiogenesis in vitro. Sci Rep. 2018 Jul;8(1):10495. 10.1038/s41598-018-28872-2
11. Li L, Wei H, Zhang H, Xu F, Che G. Circ_100565 promotes proliferation, migration and invasion in non-small cell lung cancer through upregulating HMGA2 via sponging miR-506-3p. Cancer Cell Int. 2020 May;20:160. 10.1186/s12935-020-01241-8
12. Li ZH, Zhou JH, Chen SN, Pan L, Feng Y, Luo MQ, et al. MicroRNA-506 has a suppressive effect on the tumorigenesis of nonsmall-cell lung cancer by regulating tubby-like protein 3. Bioengineered. 2021 Dec;12(2):10176–86. 10.1080/21655979.2021.2001216
13. Zhu M, An Y, Zhang X, Wang Z, Duan H. Experimental pulmonary fibrosis was suppressed by microRNA-506 through NF-kappa-mediated apoptosis and inflammation. Cell Tissue Res. 2019 Nov;378(2):255–65. 10.1007/s00441-019-03054-2
14. Spellman R, Rideau A, Matlin A, Gooding C, Robinson F, McGlincy N, et al. Regulation of alternative splicing by PTB and associated factors. Biochem Soc Trans. 2005 Jun;33(3): 457–60. 10.1042/BST0330457
15. Sawicka K, Bushell M, Spriggs KA, Willis AE. Polypyrimidine-tract-binding protein: A multifunctional RNA-binding protein. Biochem Soc Trans. 2008 Aug;36(4):641–47. 10.1042/BST0360641
16. Wollerton MC, Gooding C, Wagner EJ, Garcia-Blanco MA, Smith CW. Autoregulation of polypyr0imidine tract binding protein by alternative splicing leading to nonsense--mediated decay. Mol Cell. 2004 Jan;13(1):91–100. 10.1016/S1097-2765(03)00502-1
17. Llorian M, Schwartz S, Clark TA, Hollander D, Tan L-Y, Spellman R, et al. Position-dependent alternative splicing activity revealed by global profiling of alternative-splicing events regulated by PTB. Nat Struct Mol Biol. 2010 Sep;17(9):1114. 10.1038/nsmb.1881
18. Cho CY, Chung SY, Lin S, Huang JS, Chen YL, Jiang SS, et al. PTBP1-mediated regulation of AXL mRNA stability plays a role in lung tumorigenesis. Sci Rep. 2019 Nov;9(1):1–12. 10.1038/s41598-019-53097-2
19. Caruso P, Dunmore BJ, Schlosser K, Schoors S, Dos Santos C, Perez-Iratxeta C, et al. Identification of microRNA-124 as a major regulator of enhanced endothelial cell glycolysis in pulmonary arterial hypertension via PTBP1 (polypyrimidine tract binding protein) and pyruvate kinase M2. Circulation. 2017 Dec;136(25):2451–67. 10.1161/CIRCULATIONAHA.117.028034
20. Xu T, Yan W, Wu Q, Xu Q, Yuan J, Li Y, et al. MiR-326 inhibits inflammation and promotes autophagy in silica-induced pulmonary fibrosis through targeting TNFSF14 and PTBP1. Chem Res Toxicol. 2019 Nov;32(11):2192–203. 10.1021/acs.chemrestox.9b00194
21. Wang Z, Gan X, Qiu C, Yang D, Sun X, Zeng Z. Role of polypyrimidine tract-binding protein 1/yin yang 2 signaling in regulating vascular smooth muscle cell proliferation and neointima hyperplasia. Toxicol Appl Pharmacol. 2019 Nov;383:114747. 10.1016/j.taap.2019.114747
22. Yick CY, Zwinderman AH, Kunst PW, Grünberg K, Mauad T, Chowdhury S, et al. Gene expression profiling of laser-microdissected airway smooth muscle tissue in asthma and atopy. Allergy. 2014 Sep;69(9):1233–40. 10.1111/all.12452
23. Tang X, Nian H, Li X, Yang Y, Wang X, Xu L, et al. Effects of the combined extracts of Herba Epimedii and Fructus Ligustrilucidi on airway remodeling in the asthmatic rats with the treatment of budesonide. BMC Complement Altern Med. 2017 Aug;17(1):380. 10.1186/s12906-017-1891-0
24. Cheng Y, Wang N, Zhao L, Liu C, Wang J, Ma C, et al. Knockdown of NOVA1 inhibits inflammation and migration of asthmatic airway smooth muscle cells to regulate PTEN/Akt pathway by targeting PTBP1. Mol Immunol. 2021 Oct;138: 31–37. 10.1016/j.molimm.2021.07.016
25. Koopmans T, Gosens R. Revisiting asthma therapeutics: Focus on WNT signal transduction. Drug Discov Today. 2018 Jan;23(1):49–62. 10.1016/j.drudis.2017.09.001
26. Porcaro F, Ullmann N, Allegorico A, Di Marco A, Cutrera R. Difficult and severe asthma in children. Children. 2020 Dec;7(12):286. 10.3390/children7120286
27. Yu Y, Men S, Zhang Y. miR-20a-5p ameliorates ovalbumin (OVA)-induced mouse model of allergic asthma through targeting ATG7-regulated cell death, fibrosis and inflammation. Int Immunopharmacol. 2021 Jun;95:107342. 10.1016/j.intimp.2020.107342
28. Wang J, Dong X, Yu Z, Ge L, Lu L, Ding L, et al. Borneol inhibits CD4+T cells proliferation by down-regulating miR-26a and miR-142-3p to attenuate asthma. Int Immunopharmacol. 2021 Jan;90:107223. 10.1016/j.intimp.2020.107223
29. Fan Q, Jian Y. MiR-203a-3p regulates TGF-β1-induced epithelial-mesenchymal transition (EMT) in asthma by regulating Smad3 pathway through SIX1. Biosci Rep. 2020 Feb;40(2):BSR20192645. 10.1042/BSR20192645
30. Shi J, Chen M, Ouyang L, Wang Q, Guo Y, Huang L, et al. miR-142-5p and miR-130a-3p regulate pulmonary macrophage polarization and asthma airway remodeling. Immunol Cell Biol. 2020 Oct;98(9):715–25. 10.1111/imcb.12369
31. Li BB, Chen YL, Pang F. MicroRNA-30a targets ATG5 and attenuates airway fibrosis in asthma by suppressing autophagy. Inflammation. 2020 Feb;43(1):44–53. 10.1007/s10753-019-01076-0
32. Zhang Y, Han Y, Dong L, Yu H, Cheng L, Zhao X, et al. Genetic variation of ITGB3 is associated with asthma in Chinese Han children. PLoS ONE. 2013 Feb;8(2):e56914. 10.1371/journal.pone.0056914
33. Wang ML, Qiao H. Effect of miR-506-3p on proliferation and apoptosis of airway smooth muscle cells in asthmatic mice by regulating CCL2 gene expression and mediating TLR4/NF-κB signaling pathway activation. Mol Biotechnol. 2021 May;63(5):410–23. 10.1007/s12033-021-00309-8
34. Jin SS, Lin XF, Zheng JZ, Wang Q, Guan HQ. lncRNA NEAT1 regulates fibrosis and inflammatory response induced by nonalcoholic fatty liver by regulating miR-506/GLI3. Eur Cytokine Netw. 2019 Sep 1;30(3):98–106. 10.1684/ecn.2019.0432
35. Huang S, Wu S, Ding J, Lin J, Wei L, Gu J, et al. MicroRNA-181a modulates gene expression of zinc finger family members by directly targeting their coding regions. Nucleic Acids Res. 2010 Nov;38(20):7211–18. 10.1093/nar/gkq564
36. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009 Jan;136(2):215. 10.1016/j.cell.2009.01.002
37. Panda AC, Itishri S, Kulkarni SD, Martindale JL, Kotb A, Arya V, et al. miR-196b-mediated translation regulation of mouse insulin2 via the 5'UTR. PLoS ONE. 2014 Jul;9(7):e101084. 10.1371/journal.pone.0101084
38. Shao Y, Chong L, Lin P, Li H, Zhu L, Wu Q, et al. MicroRNA-133a alleviates airway remodeling in asthtama through PI3K/AKT/mTOR signaling pathway by targeting IGF1R. J Cell Physiol. 2019 Apr;234(4):4068–80. 10.1002/jcp.27201
39. Sun M, Huang Y, Li F, Li H, Zhang B, Jin L. MicroRNA-874 inhibits TNF-α-induced remodeling in human fetal airway smooth muscle cells by targeting STAT3. Respir Physiol Neurobiol. 2018 May;251:34–40. 10.1016/j.resp.2018.02.008
40. Chen M, Shi J, Zhang W, Huang L, Lin X, Lv Z, et al. MiR-23b controls TGF-β1-induced airway smooth muscle cell proliferation via direct targeting of Smad3. Pulm Pharmacol Ther. 2017 Feb;42:33–42. 10.1016/j.pupt.2017.01.001
41. Kang H, Heo S, Shin JJ, Ji E, Tak H, Ahn S, et al. A miR-194/PTBP1/CCND3 axis regulates tumor growth in human hepatocellular carcinoma. J Pathol. 2019 Nov;249(3):395–408. 10.1002/path.5325
42. Cui J, Placzek WJ. PTBP1 enhances miR-101-guided AGO2 targeting to MCL1 and promotes miR-101-induced apoptosis. Cell Death Dis. 2018 May;9(5):552. 10.1038/s41419-018-0551-8
43. Ding Y, Gao S, Zheng J, Chen X. Blocking lncRNA-SNHG16 sensitizes gastric cancer cells to 5-Fu through targeting the miR-506-3p-PTBP1-mediated glucose metabolism. Cancer Metab. 2022 Nov;10(1):20. 10.1186/s40170-022-00293-w.
44. Shan L, Liu S, Zhang Q, Zhou Q, Shang Y. Human bone marrow--mesenchymal stem cell-derived exosomal microRNA-188 reduces bronchial smooth muscle cell proliferation in asthma through suppressing the JARID2/Wnt/β-catenin axis. Cell Cycle. 2022 Feb;21(4):352–67. 10.1080/15384101.2021.2020432
45. Zou Y, Zhou Q, Zhang Y. MicroRNA-21 released from mast cells-derived extracellular vesicles drives asthma in mice by potentiating airway inflammation and oxidative stress. Am J Transl Res. 2021 Jul;13(7):7475–91.
46. He X, Sheng J, Yu W, Wang K, Zhu S, Liu Q. LncRNA MIR155HG promotes temozolomide resistance by activating the Wnt/ β-catenin pathway via binding to PTBP1 in glioma. Cell Mol Neurobiol. 2021 Aug;41(6):1271–84. 10.1007/s10571-020-00898-z
47. Yao J, Qin L, Miao S, Wang X, Wu X. Overexpression of miR-506 suppresses proliferation and promotes apoptosis of osteosarcoma cells by targeting astrocyte elevated gene-1. Oncol Lett. 2016 Sep;12(3):1840–48. 10.3892/ol.2016.4827
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May 1, 2023
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Cai, Y., Tian, J., Su, Y., & Shi, X. (2023). MiR-506 targets polypyrimidine tract-binding protein 1 to inhibit airway inflammatory response and remodeling via mediating Wnt/β-catenin signaling pathway. Allergologia Et Immunopathologia, 51(3), 15-24. https://doi.org/10.15586/aei.v51i3.676
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How to Cite
Cai, Y., Tian, J., Su, Y., & Shi, X. (2023). MiR-506 targets polypyrimidine tract-binding protein 1 to inhibit airway inflammatory response and remodeling via mediating Wnt/β-catenin signaling pathway. Allergologia Et Immunopathologia, 51(3), 15-24. https://doi.org/10.15586/aei.v51i3.676