Issue
Resveratrol inhibits skin squamous cell carcinoma proliferation, migration and invasion through up-regulating miR-126
Corresponding Author(s) : Bo Zhang
Cellular and Molecular Biology,
Vol. 66 No. 5: Issue 5
Abstract
The current experiment was performed to explore the effect and possible mechanism of resveratrol on the proliferation, migration and invasion of skin squamous cell carcinoma cells (HSC-5). Tetramethyl azozo blue (MTT) method, Transwell experiment and real-time fluorescence quantitative PCR (RT-qPCR) were used to detect the effects of resveratrol intervention on the proliferation, migration and invasion of HSC-5 cells and the expression of miR-126. The miR-126 mimics and inhibitors were transfected into HSC-5 cells, and the effects of up-regulation or down-regulation of HSC-5 expression on the proliferation, migration and invasion of HSC-5 cells were detected. The miR-126 inhibitor was transfected into HSC-5 cells, and the effects of resveratrol intervention on HSC-5 cell proliferation, migration and invasion, and β-catenin protein expression were detected. After resveratrol intervention, the growth rate, migration and invasion of HSC-5 cells were significantly reduced, miR-126 expression was significantly increased, and β-catenin protein expression was significantly reduced (p<0.05). After up-regulating the expression of miR-126, the growth rate, migration and invasion of HSC-5 cells were significantly reduced (p<0.05). After down-regulating the expression of miR-126, the growth rate, migration and invasion of HSC-5 cells were significantly increased (p<0.05). Down-regulation of miR-126 expression could reverse the effects of resveratrol intervention on HSC-5 cell proliferation, migration and invasion, and β-catenin protein expression (p<0.05). Resveratrol could inhibit the proliferation, migration and invasion of skin squamous cell carcinoma cells, which may be related to the up-regulation of miR-126 to inhibit the Wnt / β-catenin signaling pathway.
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- Berretta M, Bignucolo A, Di Francia R, Comello F, Facchini G, Ceccarelli M, Iaffaioli RV, Quagliariello V, Maurea N. Resveratrol in Cancer Patients: From Bench to Bedside. Int J Mol Sci 2020; 21(8):2945.
- Peiyi L, Jinping Ch, Haiping L. Proteomic study on apoptosis induced by resveratrol in human cutaneous squamous cell carcinoma. China Foreign Med Treat 2011; 30(34): 29-30.
- Hao Y, Huang W, Liao M, Zhu Y, Liu H, Hao C, Liu G, Zhang G, Feng H, Ning X, Li H. The inhibition of resveratrol to human skin squamous cell carcinoma A431 xenografts in nude mice. Fitoterapia 2013; 86:84-91.
- Hao YQ, Huang WX, Feng HX, Zhang GH, Ning XH, Li HG, Hao CG, Li ZH. Study of apoptosis related factors regulatory mechanism of resveratrol to human skin squamous cell carcinoma A431 xenograft in nude mice. Zhonghua Yi Xue Za Zhi 2013; 93(6):464-8.
- Alhasan L. MiR-126 Modulates Angiogenesis in Breast Cancer by Targeting VEGF-A -mRNA. Asian Pac J Cancer Prev 2019; 20(1): 193-197.
- Yujie X, Ting W, Lizhong H, et al. Mechanism of Baicalin on the Apoptosis of Breast Cancer Cells by Up-Regulating miR-126. J Tradit Chin Med University of Hunan 2017; 37(5): 481-484.
- Xuguang MI, Shouqing LI, Liu D, Wei H, Jiang X, Fang Y. MiR-126 expression relationship with VEGF in breast cancer and its anti-tumor effect. Chin J Immunol 2016; 32(7):1000-3.
- Gong Jin, Zhou Yu, Tu Yating. Expression and role of micro RNA -126 and vascular endothelial growth factor mRNA in cutaneous squamous cell carcinoma. J Clin Dermatol 2016; 45(4): 256-258.
- Wu H, Chen L, Zhu F, Han X, Sun L, Chen K. The Cytotoxicity Effect of Resveratrol: Cell Cycle Arrest and Induced Apoptosis of Breast Cancer 4T1 Cells. Toxins 2019; 11(12):731.
- Kim YN, Choe SR, Cho KH, Kang J, Park CG, Lee HY. Resveratrol suppresses breast cancer cell invasion by inactivating a RhoA/YAP signaling axis. Exp Mol Med 2017; 49(2):e296-.
- Yuan L, Zhou M, Huang D, Wasan HS, Zhang K, Sun L, Huang H, Ma S, Shen M, Ruan S. Resveratrol inhibits the invasion and metastasis of colon cancer through reversal of epithelial mesenchymal transition via the AKT/GSK 3β/Snail signaling pathway. Mol Med Rep 2019; 20(3):2783-95.
- Li Guoyuan, Guo Yu, Guo Zhengliang. Resveratrol suppressed invasion of osteosarcoma cells. Int J Orthop 2019; 40(3): 171-177.
- Bao J, Yu Y, Chen J, He Y, Chen X, Ren Z, Xue C, Liu L, Hu Q, Li J, Cui G. MiR-126 negatively regulates PLK-4 to impact the development of hepatocellular carcinoma via ATR/CHEK1 pathway. Cell Death Dis 2018; 9(10):1-5.
- Han J, Wang L, Wang X, Li K. Downregulation of microRNA-126 contributes to tumorigenesis of squamous tongue cell carcinoma via targeting KRAS. Med Sci Monit 2016; 22:522.
- Wei L, Chen Z, Cheng N, Li X, Chen J, Wu D, Dong M, Wu X. MicroRNA-126 Inhibit Viability of Colorectal Cancer Cell by Repressing mTOR Induced Apoptosis and Autophagy. Onco Targets Ther 2020; 13:2459.
- Hua Y, Liang C, Miao C, Wang S, Su S, Shao P, Liu B, Bao M, Zhu J, Xu A, Zhang J. MicroRNA 126 inhibits proliferation and metastasis in prostate cancer via regulation of ADAM9. Oncol Lett 2018; 15(6):9051-60.
- Jiang R, Zhang C, Liu G, Gu R, Wu H. MicroRNA"126 Inhibits Proliferation, Migration, Invasion, and EMT in Osteosarcoma by Targeting ZEB1. J Cell Biochem 2017; 118(11):3765-74.
- Gao D, Chen HQ. Specific knockdown of HOXB7 inhibits cutaneous squamous cell carcinoma cell migration and invasion while inducing apoptosis via the Wnt/β-catenin signaling pathway. Am J Physiol Cell Physiol 2018; 315(5): C675-86.
- Jingyu W, Lingkun H, Jianming W. Inhibition of resveratrol on the growth of colon cancer cells by Wnt/β-catenin signaling pathway. Central South Pharm 2015; 13(5): 499-501.
- Luo W, Yan D, Song Z, Zhu X, Liu X, Li X, Zhao S. miR-126-3p sensitizes glioblastoma cells to temozolomide by inactivating Wnt/β-catenin signaling via targeting SOX2. Life Sci 2019; 226:98-106.
- Bordbar M, Darvishzadeh R, Pazhouhandeh M, Kahrizi D. An overview of genome editing methods based on endonucleases. Mod Genet J 2020; 15(2): 75-92.
- Ghaheri M, Kahrizi D, Bahrami G, Mohammadi-Motlagh HR. Study of gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni under various mannitol concentrations. Mol Biol Rep 2019; 46(1): 7-16.
- Eruygur N, Ucar E, Akpulat HA, Shahsavari K, Safavi SM, Kahrizi D. In vitro antioxidant assessment, screening of enzyme inhibitory activities of methanol and water extracts and gene expression in Hypericum lydium. Mol Biol Rep 2019; 46(2): 2121-9.
- Esmaeili F, Ghaheri M, Kahrizi D, Mansouri M, Safavi SM, Ghorbani T, Muhammadi S, Rahmanian E, Vaziri S. Effects of various glutamine concentrations on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 1-5.
- Akbari F, Arminian A, Kahrizi D, Fazeli A, Ghaheri M. Effect of nitrogen sources on gene expression of Stevia rebaudiana (Bertoni) under in vitro conditions. Cell Mol Biol, 64(2): 11-16.
- Ghaheri M, Adibrad E, Safavi SM, Kahrizi D, Soroush A, Muhammadi S, Ghorbani T, Sabzevari A, Ansarypour Z, Rahmanian E. Effects of life cycle and leaves location on gene expression and glycoside biosynthesis pathway in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 17-22.
- Kahrizi D, Ghaheri M, Yari Z, Yari K, Bahraminejad S. Investigation of different concentrations of MS media effects on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 23-27.
- Hashempoor S, Ghaheri M, Kahrizi D, Kazemi N, Muhammadi S, Safavi SM, Ghorbani T, Rahmanian E, Heshmatpanaah M. Effects of different concentrations of mannitol on gene expression in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 28-31.
- Akbarabadi A, Ismaili A, Kahrizi D, Firouzabadi FN. Validation of expression stability of reference genes in response to herbicide stress in wild oat (Avena ludoviciana). Cell Mol Biol 2018; 64(4). 113-118.
- Ghorbani T, Kahrizi D, Saeidi M, Arji I. Effect of sucrose concentrations on Stevia rebaudiana Bertoni tissue culture and gene expression. Cell Mol Biol, 63(11): 32-36.
- Kahrizi D, Ghari SM, Ghaheri M, Fallah F, Ghorbani T, Beheshti AA, Kazemi E, Ansarypour Z. Effect of KH2PO4 on gene expression, morphological and biochemical characteristics of stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol, 63(7): 107-111.
- Fallah F, Nokhasi F, Ghaheri M, Kahrizi D, Beheshti Ale AA, Ghorbani T, Kazemi E, Ansarypour Z. Effect of salinity on gene expression, morphological and biochemical characteristics of Stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol 2017; 63(7): 102-106.
- Fatemi SS, Yari K, Tavallaei M, Kahrizi D. Expression of recombinant Hc domain of Clostridium botulinum neurotoxin A in E. coli and its purification as a vaccine candidate against botulism. Sci J Kurdistan Univ Med Sci 2011 Aug 10;16(2):36-44.
- Taheri Z, Asadzadeh Aghdaei H, Irani S, Modarressi MH, Noormohammadi Z. Clinical Correlation of miR-200c/141 Cluster DNA Methylation and miR-141 Expression with the Clinicopathological Features of Colorectal Primary Lesions/Tumors. Rep Biochem Mol Biol, 2019; 8(3):208-215.
- Esfandi F, Fallah H, Arsang-Jang S, Taheri M, Ghafouri-Fard S. The Expression of CCAT2, UCA1, PANDA and GHET1 Long Non-coding RNAs in Lung Cancer. Rep Biochem Mol Biol, 2019; 8(1):36-41.
- Azari I, Ghafouri-Fard S, Omrani MD, Arsang-Jang S, Kordi Tamandani DM, Saroone Rigi M, Rafiee S, Pouresmaeili F, Taheri M. Expression of Long Non-Coding RNAs in Placentas of Intrauterine Growth Restriction (IUGR) Pregnancies. Rep Biochem Mol Biol 2019; 8(1):25-31.
References
Berretta M, Bignucolo A, Di Francia R, Comello F, Facchini G, Ceccarelli M, Iaffaioli RV, Quagliariello V, Maurea N. Resveratrol in Cancer Patients: From Bench to Bedside. Int J Mol Sci 2020; 21(8):2945.
Peiyi L, Jinping Ch, Haiping L. Proteomic study on apoptosis induced by resveratrol in human cutaneous squamous cell carcinoma. China Foreign Med Treat 2011; 30(34): 29-30.
Hao Y, Huang W, Liao M, Zhu Y, Liu H, Hao C, Liu G, Zhang G, Feng H, Ning X, Li H. The inhibition of resveratrol to human skin squamous cell carcinoma A431 xenografts in nude mice. Fitoterapia 2013; 86:84-91.
Hao YQ, Huang WX, Feng HX, Zhang GH, Ning XH, Li HG, Hao CG, Li ZH. Study of apoptosis related factors regulatory mechanism of resveratrol to human skin squamous cell carcinoma A431 xenograft in nude mice. Zhonghua Yi Xue Za Zhi 2013; 93(6):464-8.
Alhasan L. MiR-126 Modulates Angiogenesis in Breast Cancer by Targeting VEGF-A -mRNA. Asian Pac J Cancer Prev 2019; 20(1): 193-197.
Yujie X, Ting W, Lizhong H, et al. Mechanism of Baicalin on the Apoptosis of Breast Cancer Cells by Up-Regulating miR-126. J Tradit Chin Med University of Hunan 2017; 37(5): 481-484.
Xuguang MI, Shouqing LI, Liu D, Wei H, Jiang X, Fang Y. MiR-126 expression relationship with VEGF in breast cancer and its anti-tumor effect. Chin J Immunol 2016; 32(7):1000-3.
Gong Jin, Zhou Yu, Tu Yating. Expression and role of micro RNA -126 and vascular endothelial growth factor mRNA in cutaneous squamous cell carcinoma. J Clin Dermatol 2016; 45(4): 256-258.
Wu H, Chen L, Zhu F, Han X, Sun L, Chen K. The Cytotoxicity Effect of Resveratrol: Cell Cycle Arrest and Induced Apoptosis of Breast Cancer 4T1 Cells. Toxins 2019; 11(12):731.
Kim YN, Choe SR, Cho KH, Kang J, Park CG, Lee HY. Resveratrol suppresses breast cancer cell invasion by inactivating a RhoA/YAP signaling axis. Exp Mol Med 2017; 49(2):e296-.
Yuan L, Zhou M, Huang D, Wasan HS, Zhang K, Sun L, Huang H, Ma S, Shen M, Ruan S. Resveratrol inhibits the invasion and metastasis of colon cancer through reversal of epithelial mesenchymal transition via the AKT/GSK 3β/Snail signaling pathway. Mol Med Rep 2019; 20(3):2783-95.
Li Guoyuan, Guo Yu, Guo Zhengliang. Resveratrol suppressed invasion of osteosarcoma cells. Int J Orthop 2019; 40(3): 171-177.
Bao J, Yu Y, Chen J, He Y, Chen X, Ren Z, Xue C, Liu L, Hu Q, Li J, Cui G. MiR-126 negatively regulates PLK-4 to impact the development of hepatocellular carcinoma via ATR/CHEK1 pathway. Cell Death Dis 2018; 9(10):1-5.
Han J, Wang L, Wang X, Li K. Downregulation of microRNA-126 contributes to tumorigenesis of squamous tongue cell carcinoma via targeting KRAS. Med Sci Monit 2016; 22:522.
Wei L, Chen Z, Cheng N, Li X, Chen J, Wu D, Dong M, Wu X. MicroRNA-126 Inhibit Viability of Colorectal Cancer Cell by Repressing mTOR Induced Apoptosis and Autophagy. Onco Targets Ther 2020; 13:2459.
Hua Y, Liang C, Miao C, Wang S, Su S, Shao P, Liu B, Bao M, Zhu J, Xu A, Zhang J. MicroRNA 126 inhibits proliferation and metastasis in prostate cancer via regulation of ADAM9. Oncol Lett 2018; 15(6):9051-60.
Jiang R, Zhang C, Liu G, Gu R, Wu H. MicroRNA"126 Inhibits Proliferation, Migration, Invasion, and EMT in Osteosarcoma by Targeting ZEB1. J Cell Biochem 2017; 118(11):3765-74.
Gao D, Chen HQ. Specific knockdown of HOXB7 inhibits cutaneous squamous cell carcinoma cell migration and invasion while inducing apoptosis via the Wnt/β-catenin signaling pathway. Am J Physiol Cell Physiol 2018; 315(5): C675-86.
Jingyu W, Lingkun H, Jianming W. Inhibition of resveratrol on the growth of colon cancer cells by Wnt/β-catenin signaling pathway. Central South Pharm 2015; 13(5): 499-501.
Luo W, Yan D, Song Z, Zhu X, Liu X, Li X, Zhao S. miR-126-3p sensitizes glioblastoma cells to temozolomide by inactivating Wnt/β-catenin signaling via targeting SOX2. Life Sci 2019; 226:98-106.
Bordbar M, Darvishzadeh R, Pazhouhandeh M, Kahrizi D. An overview of genome editing methods based on endonucleases. Mod Genet J 2020; 15(2): 75-92.
Ghaheri M, Kahrizi D, Bahrami G, Mohammadi-Motlagh HR. Study of gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni under various mannitol concentrations. Mol Biol Rep 2019; 46(1): 7-16.
Eruygur N, Ucar E, Akpulat HA, Shahsavari K, Safavi SM, Kahrizi D. In vitro antioxidant assessment, screening of enzyme inhibitory activities of methanol and water extracts and gene expression in Hypericum lydium. Mol Biol Rep 2019; 46(2): 2121-9.
Esmaeili F, Ghaheri M, Kahrizi D, Mansouri M, Safavi SM, Ghorbani T, Muhammadi S, Rahmanian E, Vaziri S. Effects of various glutamine concentrations on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 1-5.
Akbari F, Arminian A, Kahrizi D, Fazeli A, Ghaheri M. Effect of nitrogen sources on gene expression of Stevia rebaudiana (Bertoni) under in vitro conditions. Cell Mol Biol, 64(2): 11-16.
Ghaheri M, Adibrad E, Safavi SM, Kahrizi D, Soroush A, Muhammadi S, Ghorbani T, Sabzevari A, Ansarypour Z, Rahmanian E. Effects of life cycle and leaves location on gene expression and glycoside biosynthesis pathway in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 17-22.
Kahrizi D, Ghaheri M, Yari Z, Yari K, Bahraminejad S. Investigation of different concentrations of MS media effects on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 23-27.
Hashempoor S, Ghaheri M, Kahrizi D, Kazemi N, Muhammadi S, Safavi SM, Ghorbani T, Rahmanian E, Heshmatpanaah M. Effects of different concentrations of mannitol on gene expression in Stevia rebaudiana Bertoni. Cell Mol Biol, 64(2): 28-31.
Akbarabadi A, Ismaili A, Kahrizi D, Firouzabadi FN. Validation of expression stability of reference genes in response to herbicide stress in wild oat (Avena ludoviciana). Cell Mol Biol 2018; 64(4). 113-118.
Ghorbani T, Kahrizi D, Saeidi M, Arji I. Effect of sucrose concentrations on Stevia rebaudiana Bertoni tissue culture and gene expression. Cell Mol Biol, 63(11): 32-36.
Kahrizi D, Ghari SM, Ghaheri M, Fallah F, Ghorbani T, Beheshti AA, Kazemi E, Ansarypour Z. Effect of KH2PO4 on gene expression, morphological and biochemical characteristics of stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol, 63(7): 107-111.
Fallah F, Nokhasi F, Ghaheri M, Kahrizi D, Beheshti Ale AA, Ghorbani T, Kazemi E, Ansarypour Z. Effect of salinity on gene expression, morphological and biochemical characteristics of Stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol 2017; 63(7): 102-106.
Fatemi SS, Yari K, Tavallaei M, Kahrizi D. Expression of recombinant Hc domain of Clostridium botulinum neurotoxin A in E. coli and its purification as a vaccine candidate against botulism. Sci J Kurdistan Univ Med Sci 2011 Aug 10;16(2):36-44.
Taheri Z, Asadzadeh Aghdaei H, Irani S, Modarressi MH, Noormohammadi Z. Clinical Correlation of miR-200c/141 Cluster DNA Methylation and miR-141 Expression with the Clinicopathological Features of Colorectal Primary Lesions/Tumors. Rep Biochem Mol Biol, 2019; 8(3):208-215.
Esfandi F, Fallah H, Arsang-Jang S, Taheri M, Ghafouri-Fard S. The Expression of CCAT2, UCA1, PANDA and GHET1 Long Non-coding RNAs in Lung Cancer. Rep Biochem Mol Biol, 2019; 8(1):36-41.
Azari I, Ghafouri-Fard S, Omrani MD, Arsang-Jang S, Kordi Tamandani DM, Saroone Rigi M, Rafiee S, Pouresmaeili F, Taheri M. Expression of Long Non-Coding RNAs in Placentas of Intrauterine Growth Restriction (IUGR) Pregnancies. Rep Biochem Mol Biol 2019; 8(1):25-31.