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Published in: Cancer Cell International 1/2022

Open Access 01-12-2022 | Review

Emerging role of non-coding RNAs in the regulation of Sonic Hedgehog signaling pathway

Authors: Soudeh Ghafouri-Fard, Tayyebeh Khoshbakht, Bashdar Mahmud Hussen, Mohammad Taheri, Majid Samsami

Published in: Cancer Cell International | Issue 1/2022

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Abstract

Sonic Hedgehog (Shh) signaling cascade is one of the complex signaling pathways that control the accurately organized developmental processes in multicellular organisms. This pathway has fundamental roles in the tumor formation and induction of resistance to conventional therapies. Numerous non-coding RNAs (ncRNAs) have been found to interact with Shh pathway to induce several pathogenic processes, including malignant and non-malignant disorders. Many of the Shh-interacting ncRNAs are oncogenes whose expressions have been increased in diverse malignancies. A number of Shh-targeting miRNAs such as miR-26a, miR-1471, miR-129-5p, miR-361-3p, miR-26b-5p and miR-361-3p have been found to be down-regulated in tumor tissues. In addition to malignant conditions, Shh-interacting ncRNAs can affect tissue regeneration and development of neurodegenerative disorders. XIST, LOC101930370, lncRNA-Hh, circBCBM1, SNHG6, LINC‐PINT, TUG1 and LINC01426 are among long non-coding RNAs/circular RNAs that interact with Shh pathway. Moreover, miR-424, miR-26a, miR-1471, miR-125a, miR-210, miR-130a-5p, miR-199b, miR-155, let-7, miR-30c, miR-326, miR-26b-5p, miR-9, miR-132, miR-146a and miR-425-5p are among Shh-interacting miRNAs. The current review summarizes the interactions between ncRNAs and Shh in these contexts.
Literature
1.
go back to reference Skoda AM, Simovic D, Karin V, Kardum V, Vranic S, Serman L. The role of the Hedgehog signaling pathway in cancer: a comprehensive review. Bosn J Basic Med Sci. 2018;18(1):8.PubMedPubMedCentralCrossRef Skoda AM, Simovic D, Karin V, Kardum V, Vranic S, Serman L. The role of the Hedgehog signaling pathway in cancer: a comprehensive review. Bosn J Basic Med Sci. 2018;18(1):8.PubMedPubMedCentralCrossRef
2.
go back to reference Nüsslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980;287(5785):795–801.PubMedCrossRef Nüsslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980;287(5785):795–801.PubMedCrossRef
3.
go back to reference Choudhry Z, Rikani AA, Choudhry AM, Tariq S, Zakaria F, Asghar MW, et al. Sonic hedgehog signalling pathway: a complex network. Ann Neurosci. 2014;21(1):28–31.PubMedPubMedCentralCrossRef Choudhry Z, Rikani AA, Choudhry AM, Tariq S, Zakaria F, Asghar MW, et al. Sonic hedgehog signalling pathway: a complex network. Ann Neurosci. 2014;21(1):28–31.PubMedPubMedCentralCrossRef
4.
go back to reference Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature. 2004;432(7015):324–31.PubMedCrossRef Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature. 2004;432(7015):324–31.PubMedCrossRef
5.
6.
go back to reference Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996;383(6599):407–13.PubMedCrossRef Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996;383(6599):407–13.PubMedCrossRef
7.
go back to reference Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Altaba AR, et al. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell. 1994;76(4):761–75.PubMedCrossRef Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Altaba AR, et al. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell. 1994;76(4):761–75.PubMedCrossRef
8.
go back to reference Campbell V, Copland M. Hedgehog signaling in cancer stem cells: a focus on hematological cancers. Stem Cells Cloning Adv Appl. 2015;8:27. Campbell V, Copland M. Hedgehog signaling in cancer stem cells: a focus on hematological cancers. Stem Cells Cloning Adv Appl. 2015;8:27.
9.
go back to reference Onodera S, Nakamura Y, Azuma T. Gorlin syndrome: recent advances in genetic testing and molecular and cellular biological research. Int J Mol Sci. 2020;21(20):7559.PubMedCentralCrossRef Onodera S, Nakamura Y, Azuma T. Gorlin syndrome: recent advances in genetic testing and molecular and cellular biological research. Int J Mol Sci. 2020;21(20):7559.PubMedCentralCrossRef
10.
go back to reference Fattahi S, Nikbakhsh N, Ranaei M, Sabour D, Akhavan-Niaki H. Association of sonic hedgehog signaling pathway genes IHH, BOC, RAB23a and MIR195-5p, MIR509-3-5p, MIR6738-3p with gastric cancer stage. Sci Rep. 2021;11(1):1–12. Fattahi S, Nikbakhsh N, Ranaei M, Sabour D, Akhavan-Niaki H. Association of sonic hedgehog signaling pathway genes IHH, BOC, RAB23a and MIR195-5p, MIR509-3-5p, MIR6738-3p with gastric cancer stage. Sci Rep. 2021;11(1):1–12.
11.
go back to reference Zhang J, Fan J, Zeng X, Nie M, Luan J, Wang Y, et al. Hedgehog signaling in gastrointestinal carcinogenesis and the gastrointestinal tumor microenvironment. Acta Pharmaceutica Sinica B. 2021;11(3):609–20.PubMedCrossRef Zhang J, Fan J, Zeng X, Nie M, Luan J, Wang Y, et al. Hedgehog signaling in gastrointestinal carcinogenesis and the gastrointestinal tumor microenvironment. Acta Pharmaceutica Sinica B. 2021;11(3):609–20.PubMedCrossRef
12.
go back to reference Carballo GB, Honorato JR, de Lopes GPF. A highlight on Sonic hedgehog pathway. Cell Commun Signal. 2018;16(1):1–15.CrossRef Carballo GB, Honorato JR, de Lopes GPF. A highlight on Sonic hedgehog pathway. Cell Commun Signal. 2018;16(1):1–15.CrossRef
13.
go back to reference Statello L, Guo C-J, Chen L-L, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 2021;22(2):96–118.PubMedCrossRef Statello L, Guo C-J, Chen L-L, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 2021;22(2):96–118.PubMedCrossRef
15.
16.
go back to reference Lin B-J, Zhu J-Y, Ye J, Lu S-D, Liao M-D, Meng X-C, et al. LncRNA-XIST promotes dermal papilla induced hair follicle regeneration by targeting miR-424 to activate hedgehog signaling. Cell Signal. 2020;72: 109623.PubMedCrossRef Lin B-J, Zhu J-Y, Ye J, Lu S-D, Liao M-D, Meng X-C, et al. LncRNA-XIST promotes dermal papilla induced hair follicle regeneration by targeting miR-424 to activate hedgehog signaling. Cell Signal. 2020;72: 109623.PubMedCrossRef
17.
go back to reference Zheng G, Tao Y, Yu W, Schwartz RJ. Brief report: SRF-dependent MiR-210 silences the sonic hedgehog signaling during cardiopoesis. Stem Cells. 2013;31(10):2279–85.PubMedCrossRef Zheng G, Tao Y, Yu W, Schwartz RJ. Brief report: SRF-dependent MiR-210 silences the sonic hedgehog signaling during cardiopoesis. Stem Cells. 2013;31(10):2279–85.PubMedCrossRef
18.
go back to reference Li X, Liu H, Lv Y, Yu W, Liu X, Liu C. MiR-130a-5p/Foxa2 axis modulates fetal lung development in congenital diaphragmatic hernia by activating the Shh/Gli1 signaling pathway. Life Sci. 2020;241: 117166.PubMedCrossRef Li X, Liu H, Lv Y, Yu W, Liu X, Liu C. MiR-130a-5p/Foxa2 axis modulates fetal lung development in congenital diaphragmatic hernia by activating the Shh/Gli1 signaling pathway. Life Sci. 2020;241: 117166.PubMedCrossRef
19.
go back to reference Richbourg HA, Hu DP, Xu Y, Barczak AJ, Marcucio RS. miR-199 family contributes to regulation of sonic hedgehog expression during craniofacial development. Dev Dyn. 2020;249(9):1062–76.PubMedPubMedCentralCrossRef Richbourg HA, Hu DP, Xu Y, Barczak AJ, Marcucio RS. miR-199 family contributes to regulation of sonic hedgehog expression during craniofacial development. Dev Dyn. 2020;249(9):1062–76.PubMedPubMedCentralCrossRef
20.
go back to reference Liu T, Wang Z, Dong M, Wei J, Pan Y. MicroRNA-26a inhibits cell proliferation and invasion by targeting FAM98A in breast cancer. Oncol Lett. 2021;21(5):1–9.CrossRef Liu T, Wang Z, Dong M, Wei J, Pan Y. MicroRNA-26a inhibits cell proliferation and invasion by targeting FAM98A in breast cancer. Oncol Lett. 2021;21(5):1–9.CrossRef
21.
go back to reference Liu X, Zhao T, Bai X, Li M, Ren J, Wang M, et al. LOC101930370/MiR-1471 axis modulates the hedgehog signaling pathway in breast cancer. Cell Physiol Biochem. 2018;48(3):1139–50.PubMedCrossRef Liu X, Zhao T, Bai X, Li M, Ren J, Wang M, et al. LOC101930370/MiR-1471 axis modulates the hedgehog signaling pathway in breast cancer. Cell Physiol Biochem. 2018;48(3):1139–50.PubMedCrossRef
22.
go back to reference Zhou M, Hou Y, Yang G, Zhang H, Tu G, Du Y-e, et al. LncRNA-Hh strengthen cancer stem cells generation in twist-positive breast cancer via activation of hedgehog signaling pathway. Stem Cells. 2016;34(1):55–66.PubMedCrossRef Zhou M, Hou Y, Yang G, Zhang H, Tu G, Du Y-e, et al. LncRNA-Hh strengthen cancer stem cells generation in twist-positive breast cancer via activation of hedgehog signaling pathway. Stem Cells. 2016;34(1):55–66.PubMedCrossRef
23.
go back to reference Fu B, Liu W, Zhu C, Li P, Wang L, Pan L, et al. Circular RNA circBCBM1 promotes breast cancer brain metastasis by modulating miR-125a/BRD4 axis. Int J Biol Sci. 2021;17(12):3104.PubMedPubMedCentralCrossRef Fu B, Liu W, Zhu C, Li P, Wang L, Pan L, et al. Circular RNA circBCBM1 promotes breast cancer brain metastasis by modulating miR-125a/BRD4 axis. Int J Biol Sci. 2021;17(12):3104.PubMedPubMedCentralCrossRef
24.
go back to reference Zhao D, Hou Y, Sun F, Han B, Li S. Effects of miR-132 on proliferation and apoptosis of pancreatic cancer cells via Hedgehog signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(5):1978–85.PubMed Zhao D, Hou Y, Sun F, Han B, Li S. Effects of miR-132 on proliferation and apoptosis of pancreatic cancer cells via Hedgehog signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(5):1978–85.PubMed
25.
go back to reference Yin S, Du W, Wang F, Han B, Cui Y, Yang D, et al. MicroRNA-326 sensitizes human glioblastoma cells to curcumin via the SHH/GLI1 signaling pathway. Cancer Biol Ther. 2018;19(4):260–70.PubMedPubMedCentralCrossRef Yin S, Du W, Wang F, Han B, Cui Y, Yang D, et al. MicroRNA-326 sensitizes human glioblastoma cells to curcumin via the SHH/GLI1 signaling pathway. Cancer Biol Ther. 2018;19(4):260–70.PubMedPubMedCentralCrossRef
26.
go back to reference Munoz JL, Rodriguez-Cruz V, Ramkissoon SH, Ligon KL, Greco SJ, Rameshwar P. Temozolomide resistance in glioblastoma occurs by miRNA-9-targeted PTCH1, independent of sonic hedgehog level. Oncotarget. 2015;6(2):1190.PubMedPubMedCentralCrossRef Munoz JL, Rodriguez-Cruz V, Ramkissoon SH, Ligon KL, Greco SJ, Rameshwar P. Temozolomide resistance in glioblastoma occurs by miRNA-9-targeted PTCH1, independent of sonic hedgehog level. Oncotarget. 2015;6(2):1190.PubMedPubMedCentralCrossRef
27.
go back to reference Zhou H, Han L, Wang H, Wei J, Guo Z, Li Z. Chidamide inhibits glioma cells by increasing oxidative stress via the miRNA-338–5p regulation of Hedgehog signaling. Oxidative Med Cell Longevity. 2020;2020:1.CrossRef Zhou H, Han L, Wang H, Wei J, Guo Z, Li Z. Chidamide inhibits glioma cells by increasing oxidative stress via the miRNA-338–5p regulation of Hedgehog signaling. Oxidative Med Cell Longevity. 2020;2020:1.CrossRef
28.
go back to reference Wang Y-F, Yang H-Y, Shi X-Q, Wang Y. Upregulation of microRNA-129-5p inhibits cell invasion, migration and tumor angiogenesis by inhibiting ZIC2 via downregulation of the Hedgehog signaling pathway in cervical cancer. Cancer Biol Ther. 2018;19(12):1162–73.PubMedPubMedCentralCrossRef Wang Y-F, Yang H-Y, Shi X-Q, Wang Y. Upregulation of microRNA-129-5p inhibits cell invasion, migration and tumor angiogenesis by inhibiting ZIC2 via downregulation of the Hedgehog signaling pathway in cervical cancer. Cancer Biol Ther. 2018;19(12):1162–73.PubMedPubMedCentralCrossRef
29.
go back to reference Gao J, Zhao G, Li W, Zhang J, Che Y, Song M, et al. MiR-155 targets PTCH1 to mediate endothelial progenitor cell dysfunction caused by high glucose. Exp Cell Res. 2018;366(1):55–62.PubMedCrossRef Gao J, Zhao G, Li W, Zhang J, Che Y, Song M, et al. MiR-155 targets PTCH1 to mediate endothelial progenitor cell dysfunction caused by high glucose. Exp Cell Res. 2018;366(1):55–62.PubMedCrossRef
30.
go back to reference Neumann JE, Wefers AK, Lambo S, Bianchi E, Bockstaller M, Dorostkar MM, et al. A mouse model for embryonal tumors with multilayered rosettes uncovers the therapeutic potential of Sonic-hedgehog inhibitors. Nat Med. 2017;23(10):1191–202.PubMedCrossRef Neumann JE, Wefers AK, Lambo S, Bianchi E, Bockstaller M, Dorostkar MM, et al. A mouse model for embryonal tumors with multilayered rosettes uncovers the therapeutic potential of Sonic-hedgehog inhibitors. Nat Med. 2017;23(10):1191–202.PubMedCrossRef
31.
go back to reference Liu X, Li M, Peng Y, Hu X, Xu J, Zhu S, et al. miR-30c regulates proliferation, apoptosis and differentiation via the Shh signaling pathway in P19 cells. Exp Mol Med. 2016;48(7):e248-e.CrossRef Liu X, Li M, Peng Y, Hu X, Xu J, Zhu S, et al. miR-30c regulates proliferation, apoptosis and differentiation via the Shh signaling pathway in P19 cells. Exp Mol Med. 2016;48(7):e248-e.CrossRef
32.
go back to reference Jiang Z, Cushing L, Ai X, Lü J. miR-326 is downstream of Sonic hedgehog signaling and regulates the expression of Gli2 and smoothened. Am J Respir Cell Mol Biol. 2014;51(2):273–83.PubMedPubMedCentralCrossRef Jiang Z, Cushing L, Ai X, Lü J. miR-326 is downstream of Sonic hedgehog signaling and regulates the expression of Gli2 and smoothened. Am J Respir Cell Mol Biol. 2014;51(2):273–83.PubMedPubMedCentralCrossRef
33.
go back to reference Liu X, Wang K, Du H. LncRNA SNHG6 regulating Hedgehog signaling pathway and affecting the biological function of gallbladder carcinoma cells through targeting miR-26b-5p. Eur Rev Med Pharmacol Sci. 2020;24:7598–611.PubMed Liu X, Wang K, Du H. LncRNA SNHG6 regulating Hedgehog signaling pathway and affecting the biological function of gallbladder carcinoma cells through targeting miR-26b-5p. Eur Rev Med Pharmacol Sci. 2020;24:7598–611.PubMed
34.
go back to reference Bier A, Giladi N, Kronfeld N, Lee HK, Cazacu S, Finniss S, et al. MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1. Oncotarget. 2013;4(5):665.PubMedPubMedCentralCrossRef Bier A, Giladi N, Kronfeld N, Lee HK, Cazacu S, Finniss S, et al. MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1. Oncotarget. 2013;4(5):665.PubMedPubMedCentralCrossRef
35.
go back to reference Li J, Zhang Q, Fan X, Mo W, Dai W, Feng J, et al. The long noncoding RNA TUG1 acts as a competing endogenous RNA to regulate the Hedgehog pathway by targeting miR-132 in hepatocellular carcinoma. Oncotarget. 2017;8(39):65932.PubMedPubMedCentralCrossRef Li J, Zhang Q, Fan X, Mo W, Dai W, Feng J, et al. The long noncoding RNA TUG1 acts as a competing endogenous RNA to regulate the Hedgehog pathway by targeting miR-132 in hepatocellular carcinoma. Oncotarget. 2017;8(39):65932.PubMedPubMedCentralCrossRef
36.
go back to reference Ghorpade DS, Sinha AY, Holla S, Singh V, Balaji KN. NOD2-nitric oxide-responsive microRNA-146a activates Sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease. J Biol Chem. 2013;288(46):33037–48.PubMedPubMedCentralCrossRef Ghorpade DS, Sinha AY, Holla S, Singh V, Balaji KN. NOD2-nitric oxide-responsive microRNA-146a activates Sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease. J Biol Chem. 2013;288(46):33037–48.PubMedPubMedCentralCrossRef
37.
go back to reference Yuan Z, Xiu C, Liu D, Zhou G, Yang H, Pei R, et al. Long noncoding RNA LINC-PINT regulates laryngeal carcinoma cell stemness and chemoresistance through miR-425-5p/PTCH1/SHH axis. J Cell Physiol. 2019;234(12):23111–22.PubMedCrossRef Yuan Z, Xiu C, Liu D, Zhou G, Yang H, Pei R, et al. Long noncoding RNA LINC-PINT regulates laryngeal carcinoma cell stemness and chemoresistance through miR-425-5p/PTCH1/SHH axis. J Cell Physiol. 2019;234(12):23111–22.PubMedCrossRef
38.
go back to reference Yu F, Zheng Y, Hong W, Chen B, Dong P, Zheng J. MicroRNA-200a suppresses epithelial-to-mesenchymal transition in rat hepatic stellate cells via GLI family zinc finger 2. Mol Med Rep. 2015;12(6):8121–8.PubMedCrossRef Yu F, Zheng Y, Hong W, Chen B, Dong P, Zheng J. MicroRNA-200a suppresses epithelial-to-mesenchymal transition in rat hepatic stellate cells via GLI family zinc finger 2. Mol Med Rep. 2015;12(6):8121–8.PubMedCrossRef
39.
go back to reference Haque I, Kawsar HI, Motes H, Sharma M, Banerjee S, Banerjee SK, et al. Downregulation of miR-506-3p facilitates EGFR-TKI resistance through induction of sonic hedgehog signaling in non-small-cell lung cancer cell lines. Int J Mol Sci. 2020;21(23):9307.PubMedCentralCrossRef Haque I, Kawsar HI, Motes H, Sharma M, Banerjee S, Banerjee SK, et al. Downregulation of miR-506-3p facilitates EGFR-TKI resistance through induction of sonic hedgehog signaling in non-small-cell lung cancer cell lines. Int J Mol Sci. 2020;21(23):9307.PubMedCentralCrossRef
40.
go back to reference Sun J, Jia J, Yuan W, Liu S, Wang W, Ge L, et al. LncRNA BLACAT1 accelerates non-small cell lung cancer through up-regulating the activation of Sonic Hedgehog Pathway. Front Oncol. 2021;11:708. Sun J, Jia J, Yuan W, Liu S, Wang W, Ge L, et al. LncRNA BLACAT1 accelerates non-small cell lung cancer through up-regulating the activation of Sonic Hedgehog Pathway. Front Oncol. 2021;11:708.
41.
go back to reference Liu X, Yin Z, Xu L, Liu H, Jiang L, Liu S, et al. Upregulation of LINC01426 promotes the progression and stemness in lung adenocarcinoma by enhancing the level of SHH protein to activate the hedgehog pathway. Cell Death Dis. 2021;12(2):1–13.CrossRef Liu X, Yin Z, Xu L, Liu H, Jiang L, Liu S, et al. Upregulation of LINC01426 promotes the progression and stemness in lung adenocarcinoma by enhancing the level of SHH protein to activate the hedgehog pathway. Cell Death Dis. 2021;12(2):1–13.CrossRef
42.
go back to reference Liu M-w, Su M-x, Tang D-y, Hao L, Xun X-H, Huang Y-q. Ligustrazin increases lung cell autophagy and ameliorates paraquat-induced pulmonary fibrosis by inhibiting PI3K/Akt/mTOR and hedgehog signalling via increasing miR-193a expression. BMC Pulmonary Med. 2019;19(1):1–16.CrossRef Liu M-w, Su M-x, Tang D-y, Hao L, Xun X-H, Huang Y-q. Ligustrazin increases lung cell autophagy and ameliorates paraquat-induced pulmonary fibrosis by inhibiting PI3K/Akt/mTOR and hedgehog signalling via increasing miR-193a expression. BMC Pulmonary Med. 2019;19(1):1–16.CrossRef
43.
go back to reference Holla S, Stephen-Victor E, Prakhar P, Sharma M, Saha C, Udupa V, et al. Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1-and prostaglandin E2-induced regulatory T cell expansion. Sci Rep. 2016;6(1):1–14.CrossRef Holla S, Stephen-Victor E, Prakhar P, Sharma M, Saha C, Udupa V, et al. Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1-and prostaglandin E2-induced regulatory T cell expansion. Sci Rep. 2016;6(1):1–14.CrossRef
44.
go back to reference Miele E, Po A, Begalli F, Antonucci L, Mastronuzzi A, Marras CE, et al. β-arrestin1-mediated acetylation of Gli1 regulates Hedgehog/Gli signaling and modulates self-renewal of SHH medulloblastoma cancer stem cells. BMC Cancer. 2017;17(1):1–12.CrossRef Miele E, Po A, Begalli F, Antonucci L, Mastronuzzi A, Marras CE, et al. β-arrestin1-mediated acetylation of Gli1 regulates Hedgehog/Gli signaling and modulates self-renewal of SHH medulloblastoma cancer stem cells. BMC Cancer. 2017;17(1):1–12.CrossRef
45.
go back to reference Zhang Y, Wang T, Wang S, Xiong Y, Zhang R, Zhang X, et al. Nkx2-2as suppression contributes to the pathogenesis of sonic hedgehog medulloblastoma. Can Res. 2018;78(4):962–73.CrossRef Zhang Y, Wang T, Wang S, Xiong Y, Zhang R, Zhang X, et al. Nkx2-2as suppression contributes to the pathogenesis of sonic hedgehog medulloblastoma. Can Res. 2018;78(4):962–73.CrossRef
46.
go back to reference Lang Z, Fan X, Lin H, Qiu L, Zhang J, Gao C. Silencing of SNHG6 alleviates hypoxia/reoxygenation-induced cardiomyocyte apoptosis by modulating miR-135a-5p/HIF1AN to activate Shh/Gli1 signalling pathway. J Pharm Pharmacol. 2021;73(1):22–31.PubMedCrossRef Lang Z, Fan X, Lin H, Qiu L, Zhang J, Gao C. Silencing of SNHG6 alleviates hypoxia/reoxygenation-induced cardiomyocyte apoptosis by modulating miR-135a-5p/HIF1AN to activate Shh/Gli1 signalling pathway. J Pharm Pharmacol. 2021;73(1):22–31.PubMedCrossRef
48.
go back to reference Akhtar N, Makki MS, Haqqi TM. MicroRNA-602 and microRNA-608 regulate sonic hedgehog expression via target sites in the coding region in human chondrocytes. Arthritis Rheumatol. 2015;67(2):423–34.PubMedPubMedCentralCrossRef Akhtar N, Makki MS, Haqqi TM. MicroRNA-602 and microRNA-608 regulate sonic hedgehog expression via target sites in the coding region in human chondrocytes. Arthritis Rheumatol. 2015;67(2):423–34.PubMedPubMedCentralCrossRef
49.
go back to reference Qing Y, Huang M, Cao Y, Du T, Song K. Effects of miRNA-342-3p in modulating Hedgehog signaling pathway of human umbilical cord mesenchymal stem cells by down-regulating Sufu. Oral Dis. 2019;25(4):1147–57.PubMedCrossRef Qing Y, Huang M, Cao Y, Du T, Song K. Effects of miRNA-342-3p in modulating Hedgehog signaling pathway of human umbilical cord mesenchymal stem cells by down-regulating Sufu. Oral Dis. 2019;25(4):1147–57.PubMedCrossRef
50.
go back to reference Huang M, Qing Y, Shi Q, Cao Y, Song K. miR-342-3p elevates osteogenic differentiation of umbilical cord mesenchymal stem cells via inhibiting Sufu in vitro. Biochem Biophys Res Commun. 2017;491(3):571–7.PubMedCrossRef Huang M, Qing Y, Shi Q, Cao Y, Song K. miR-342-3p elevates osteogenic differentiation of umbilical cord mesenchymal stem cells via inhibiting Sufu in vitro. Biochem Biophys Res Commun. 2017;491(3):571–7.PubMedCrossRef
51.
go back to reference Nan K, Zhang Y, Zhang X, Li D, Zhao Y, Jing Z, et al. Exosomes from miRNA-378-modified adipose-derived stem cells prevent glucocorticoid-induced osteonecrosis of the femoral head by enhancing angiogenesis and osteogenesis via targeting miR-378 negatively regulated suppressor of fused (Sufu). Stem Cell Res Ther. 2021;12(1):1–13.CrossRef Nan K, Zhang Y, Zhang X, Li D, Zhao Y, Jing Z, et al. Exosomes from miRNA-378-modified adipose-derived stem cells prevent glucocorticoid-induced osteonecrosis of the femoral head by enhancing angiogenesis and osteogenesis via targeting miR-378 negatively regulated suppressor of fused (Sufu). Stem Cell Res Ther. 2021;12(1):1–13.CrossRef
52.
go back to reference Kaur S, Gupta S, Chaudhary M, Khursheed MA, Mitra S, Kurup AJ, et al. let-7 MicroRNA-mediated regulation of Shh signaling and the gene regulatory network is essential for retina regeneration. Cell Rep. 2018;23(5):1409–23.PubMedPubMedCentralCrossRef Kaur S, Gupta S, Chaudhary M, Khursheed MA, Mitra S, Kurup AJ, et al. let-7 MicroRNA-mediated regulation of Shh signaling and the gene regulatory network is essential for retina regeneration. Cell Rep. 2018;23(5):1409–23.PubMedPubMedCentralCrossRef
53.
go back to reference Zhao D, Cui Z. MicroRNA-361-3p regulates retinoblastoma cell proliferation and stemness by targeting hedgehog signaling. Exp Ther Med. 2019;17(2):1154–62.PubMed Zhao D, Cui Z. MicroRNA-361-3p regulates retinoblastoma cell proliferation and stemness by targeting hedgehog signaling. Exp Ther Med. 2019;17(2):1154–62.PubMed
54.
go back to reference Suh HN, Han HJ. Sonic hedgehog increases the skin wound-healing ability of mouse embryonic stem cells through the micro RNA 200 family. Br J Pharmacol. 2015;172(3):815–28.PubMedCrossRef Suh HN, Han HJ. Sonic hedgehog increases the skin wound-healing ability of mouse embryonic stem cells through the micro RNA 200 family. Br J Pharmacol. 2015;172(3):815–28.PubMedCrossRef
55.
go back to reference Liu XS, Chopp M, Wang XL, Zhang L, Hozeska-Solgot A, Tang T, et al. MicroRNA-17-92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem. 2013;288(18):12478–88.PubMedPubMedCentralCrossRef Liu XS, Chopp M, Wang XL, Zhang L, Hozeska-Solgot A, Tang T, et al. MicroRNA-17-92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem. 2013;288(18):12478–88.PubMedPubMedCentralCrossRef
56.
go back to reference Zhang H, Tan M, Zhang J, Han X, Ma Y. Propofol inhibits thyroid cancer cell proliferation, migration, and invasion by suppressing SHH and PI3K/AKT signaling pathways via the miR-141–3p/BRD4 Axis. J Healthcare Eng. 2021;2021:1. Zhang H, Tan M, Zhang J, Han X, Ma Y. Propofol inhibits thyroid cancer cell proliferation, migration, and invasion by suppressing SHH and PI3K/AKT signaling pathways via the miR-141–3p/BRD4 Axis. J Healthcare Eng. 2021;2021:1.
57.
go back to reference Li S, Zhang Y, Sun Y, Zhao H, Wang Y. Inhibition of microRNA-802-5p inhibits myocardial apoptosis after myocardial infarction via Sonic Hedgehog signaling pathway by targeting PTCH1. Eur Rev Med Pharmacol Sci. 2021;25(1):326–34.PubMed Li S, Zhang Y, Sun Y, Zhao H, Wang Y. Inhibition of microRNA-802-5p inhibits myocardial apoptosis after myocardial infarction via Sonic Hedgehog signaling pathway by targeting PTCH1. Eur Rev Med Pharmacol Sci. 2021;25(1):326–34.PubMed
58.
go back to reference Wang B, Xu J, Hu J, Hu M, Huang J, Zhu X. Effects of miR-153 on angiogenesis in MCAO rats through Shh signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(2):732–9.PubMed Wang B, Xu J, Hu J, Hu M, Huang J, Zhu X. Effects of miR-153 on angiogenesis in MCAO rats through Shh signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(2):732–9.PubMed
59.
go back to reference Sun Q, Zeng J, Liu Y, Chen J, Zeng Q-C, Chen Y-Q, et al. microRNA-9 and-29a regulate the progression of diabetic peripheral neuropathy via ISL1-mediated sonic hedgehog signaling pathway. Aging (Albany NY). 2020;12(12):11446.CrossRef Sun Q, Zeng J, Liu Y, Chen J, Zeng Q-C, Chen Y-Q, et al. microRNA-9 and-29a regulate the progression of diabetic peripheral neuropathy via ISL1-mediated sonic hedgehog signaling pathway. Aging (Albany NY). 2020;12(12):11446.CrossRef
60.
go back to reference Hyun J, Wang S, Kim J, Kim GJ, Jung Y. MicroRNA125b-mediated Hedgehog signaling influences liver regeneration by chorionic plate-derived mesenchymal stem cells. Sci Rep. 2015;5(1):1–15.CrossRef Hyun J, Wang S, Kim J, Kim GJ, Jung Y. MicroRNA125b-mediated Hedgehog signaling influences liver regeneration by chorionic plate-derived mesenchymal stem cells. Sci Rep. 2015;5(1):1–15.CrossRef
61.
go back to reference Zhang Z, Li S, Cheng SY. The miR-183∼ 96∼ 182 cluster promotes tumorigenesis in a mouse model of medulloblastoma. J Biomed Res. 2013;27(6):486.PubMedPubMedCentral Zhang Z, Li S, Cheng SY. The miR-183∼ 96∼ 182 cluster promotes tumorigenesis in a mouse model of medulloblastoma. J Biomed Res. 2013;27(6):486.PubMedPubMedCentral
62.
go back to reference Lin J-C, Liu Z-G, Yu B, Zhang X-R. MicroRNA-874 targeting SUFU involves in osteoblast proliferation and differentiation in osteoporosis rats through the Hedgehog signaling pathway. Biochem Biophys Res Commun. 2018;506(1):194–203.PubMedCrossRef Lin J-C, Liu Z-G, Yu B, Zhang X-R. MicroRNA-874 targeting SUFU involves in osteoblast proliferation and differentiation in osteoporosis rats through the Hedgehog signaling pathway. Biochem Biophys Res Commun. 2018;506(1):194–203.PubMedCrossRef
63.
go back to reference Wang J, Wang W, Zhai H. MicroRNA-124 enhances dopamine receptor expression and neuronal proliferation in mouse models of Parkinson’s disease via the hedgehog signaling pathway by targeting EDN2. NeuroImmunoModulation. 2019;26(4):174–87.PubMedCrossRef Wang J, Wang W, Zhai H. MicroRNA-124 enhances dopamine receptor expression and neuronal proliferation in mouse models of Parkinson’s disease via the hedgehog signaling pathway by targeting EDN2. NeuroImmunoModulation. 2019;26(4):174–87.PubMedCrossRef
64.
go back to reference Hudish LI, Galati DF, Ravanelli AM, Pearson CG, Huang P, Appel B. miR-219 regulates neural progenitors by dampening apical Par protein-dependent Hedgehog signaling. Development. 2016;143(13):2292–304.PubMedPubMedCentral Hudish LI, Galati DF, Ravanelli AM, Pearson CG, Huang P, Appel B. miR-219 regulates neural progenitors by dampening apical Par protein-dependent Hedgehog signaling. Development. 2016;143(13):2292–304.PubMedPubMedCentral
65.
go back to reference Wang X, Wang H, Zhang T, He M, Liang H, Wang H, et al. Inhibition of MicroRNA-195 alleviates neuropathic pain by targeting Patched1 and inhibiting SHH signaling pathway activation. Neurochem Res. 2019;44(7):1690–702.PubMedCrossRef Wang X, Wang H, Zhang T, He M, Liang H, Wang H, et al. Inhibition of MicroRNA-195 alleviates neuropathic pain by targeting Patched1 and inhibiting SHH signaling pathway activation. Neurochem Res. 2019;44(7):1690–702.PubMedCrossRef
66.
go back to reference Huang H, Fu S, Liu D. Detection and analysis of the hedgehog signaling pathway-related long non-coding RNA (lncRNA) expression profiles in keloid. Med Sci Monitor: Int Med J Exp Clin Res. 2018;24:9032–44.CrossRef Huang H, Fu S, Liu D. Detection and analysis of the hedgehog signaling pathway-related long non-coding RNA (lncRNA) expression profiles in keloid. Med Sci Monitor: Int Med J Exp Clin Res. 2018;24:9032–44.CrossRef
67.
go back to reference Yoo YA, Kang MH, Lee HJ, Kim B-h, Park JK, Kim HK, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res. 2011;71(22):7061–70.PubMedCrossRef Yoo YA, Kang MH, Lee HJ, Kim B-h, Park JK, Kim HK, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res. 2011;71(22):7061–70.PubMedCrossRef
69.
go back to reference Islam S, Mokhtari R, Noman A, Uddin M, Rahman M, Azadi M, et al. Sonic hedgehog (Shh) signaling promotes tumorigenicity and stemness via activation of epithelial-to-mesenchymal transition (EMT) in bladder cancer. Mol Carcinog. 2016;55(5):537–51.PubMedCrossRef Islam S, Mokhtari R, Noman A, Uddin M, Rahman M, Azadi M, et al. Sonic hedgehog (Shh) signaling promotes tumorigenicity and stemness via activation of epithelial-to-mesenchymal transition (EMT) in bladder cancer. Mol Carcinog. 2016;55(5):537–51.PubMedCrossRef
70.
go back to reference Song J, Ge Y, Sun X, Guan Q, Gong S, Wei M, et al. Noncoding RNAs related to the hedgehog pathway in cancer: clinical implications and future perspectives. Mol Cancer. 2022;21(1):115.PubMedPubMedCentralCrossRef Song J, Ge Y, Sun X, Guan Q, Gong S, Wei M, et al. Noncoding RNAs related to the hedgehog pathway in cancer: clinical implications and future perspectives. Mol Cancer. 2022;21(1):115.PubMedPubMedCentralCrossRef
71.
go back to reference Wang YZ. The limited role of most circRNAs as sponges for microRNAs. Cell Mol Life Sci: CMLS. 2022;79(6):299.PubMedCrossRef Wang YZ. The limited role of most circRNAs as sponges for microRNAs. Cell Mol Life Sci: CMLS. 2022;79(6):299.PubMedCrossRef
72.
go back to reference Wang Y. Comment on "Circular RNAs and their emerging roles as diagnostic and prognostic biomarkers in ovarian cancer. Cancer Lett. 2020;2020(473):139–47. Wang Y. Comment on "Circular RNAs and their emerging roles as diagnostic and prognostic biomarkers in ovarian cancer. Cancer Lett. 2020;2020(473):139–47.
73.
go back to reference Wang YZ. Letter to the Editor: the limited functions and mechanisms of CircASAP1 as a Sponge of Onco-microRNAs. Hepatology (Baltimore, Md). 2021;73(6):2610.CrossRef Wang YZ. Letter to the Editor: the limited functions and mechanisms of CircASAP1 as a Sponge of Onco-microRNAs. Hepatology (Baltimore, Md). 2021;73(6):2610.CrossRef
75.
go back to reference Wang YZ. Comment on "Regulation of nuclear Factor-KappaB (NF-κB) signaling pathway by non-coding RNAs in cancer: Inhibiting or promoting carcinogenesis? [Cancer Lett. 509 (2021 May 2) 63-80]. Cancer Lett. 2021;516:99–100.PubMedCrossRef Wang YZ. Comment on "Regulation of nuclear Factor-KappaB (NF-κB) signaling pathway by non-coding RNAs in cancer: Inhibiting or promoting carcinogenesis? [Cancer Lett. 509 (2021 May 2) 63-80]. Cancer Lett. 2021;516:99–100.PubMedCrossRef
76.
go back to reference Wang Y. Letter to the editor: issues of circular RNAs as MicroRNA Sponges. Hepatology (Baltimore, Md). 2020;72(1):365.CrossRef Wang Y. Letter to the editor: issues of circular RNAs as MicroRNA Sponges. Hepatology (Baltimore, Md). 2020;72(1):365.CrossRef
77.
go back to reference Sari IN, Phi LTH, Jun N, Wijaya YT, Lee S, Kwon HY. Hedgehog signaling in cancer: a prospective therapeutic target for eradicating cancer stem cells. Cells. 2018;7(11):208.PubMedCentralCrossRef Sari IN, Phi LTH, Jun N, Wijaya YT, Lee S, Kwon HY. Hedgehog signaling in cancer: a prospective therapeutic target for eradicating cancer stem cells. Cells. 2018;7(11):208.PubMedCentralCrossRef
Metadata
Title
Emerging role of non-coding RNAs in the regulation of Sonic Hedgehog signaling pathway
Authors
Soudeh Ghafouri-Fard
Tayyebeh Khoshbakht
Bashdar Mahmud Hussen
Mohammad Taheri
Majid Samsami
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2022
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-022-02702-y

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