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Vol. 64 No. 6: Advances in mechanism and treatment strategy of cancer

Issue Published : May 19, 2018

Icariin inhibits autophagy and promotes apoptosis in SKVCR cells through mTOR signal pathway

https://doi.org/10.14715/cmb/2018.64.6.2
Shaoyan Jiang
Pharmacy department, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, Guangdong, China
Hong Chang
Pharmacy department, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, Guangdong, China
Shaojie Deng
Pharmacy department, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, Guangdong, China
Danyi Fan
Pharmacy department, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, Guangdong, China

Corresponding Author(s) : Shaoyan Jiang

syjiangdoc@163.com

Cellular and Molecular Biology, Vol. 64 No. 6: Advances in mechanism and treatment strategy of cancer
Article Published : May 15, 2018

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Abstract

Autophagy is a conserved biological process, which is regulated by mTOR pathway and is reported to be a self-protective process of cancer cells to counteract apoptosis. Icariin is an active flavonoid that is reported to inhibit autophagy. In this study, we investigated whether Icariin could induce a reduction of cell proliferation by inhibiting autophagy. SKVCR cells, which are resistant to vincristine, were used for the investigation. We used CCK8 test and flow cytometry assay to study the effects of Icariin on cell proliferation, cell apoptosis and cell circle. We performed transmission electron microscope (TEM), immunohistochemical assay and western blotting assay to study the level of autophagy after Icariin treatment. Finally, we investigated whether the mTOR pathway is a target of Icariin by using mTOR inhibitor rapamycin and detected autophagy and apoptosis via flow cytometry assay, TEM, immunohistochemical assay and western blotting assay. Decreased proliferation and increased apoptosis was observed after Icariin treatment in SKVCR cells, together with decreased level of autophagy. Application of rapamycin could reverse the anti-autophagic and pro- apoptotic effect of Icariin. Icariin can inhibit autophagy and promote apoptosis in SKVCR cells by activating mTOR signal pathway. Icariin attenuates tumorigenesis by inhibiting autophagy and inducing apoptosis.

Keywords

Icariin Autophagy Apoptosis SKVCR cell-lines Multidrug resistance.
Jiang, S., Chang, H., Deng, S., & Fan, D. (2018). Icariin inhibits autophagy and promotes apoptosis in SKVCR cells through mTOR signal pathway. Cellular and Molecular Biology, 64(6), 4–10. https://doi.org/10.14715/cmb/2018.64.6.2
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References
  1. Ren F, Shen J, Shi H, Hornicek FJ, Kan Q, Duan Z. Novel mechanisms and approaches to overcome multidrug resistance in the treatment of ovarian cancer. Biochimica et biophysica acta. Dec 2016; 1866(2): 266-275.
  2. Penson RT, Oliva E, Skates SJ et al. Expression of multidrug resistance-1 protein inversely correlates with paclitaxel response and survival in ovarian cancer patients: a study in serial samples. Gynecologic oncology. Apr 2004; 93(1): 98-106.
  3. Hooks SB, Murph MM. Cellular deficiency in the RGS10 protein facilitates chemoresistant ovarian cancer. Future medicinal chemistry. Aug 2015; 7(12): 1483-1489.
  4. Lord CJ, Tutt AN, Ashworth A. Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors. Annual review of medicine. 2015; 66: 455-470.
  5. Marchetti C, Palaia I, De Felice F et al. Tyrosine-kinases inhibitors in recurrent platinum-resistant ovarian cancer patients. Cancer treatment reviews. Jan 2016; 42: 41-46.
  6. Muralidhar GG, Barbolina MV. The miR-200 Family: Versatile Players in Epithelial Ovarian Cancer. International journal of molecular sciences. Jul 24 2015; 16(8): 16833-16847.
  7. Kimmelman AC, White E. Autophagy and Tumor Metabolism. Cell metabolism. May 02 2017; 25(5): 1037-1043.
  8. Mahase S, Rattenni RN, Wesseling P et al. Hypoxia-Mediated Mechanisms Associated with Antiangiogenic Treatment Resistance in Glioblastomas. The American journal of pathology. May 2017; 187(5): 940-953.
  9. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nature reviews Molecular cell biology. Sep 2007; 8(9): 741-752.
  10. Galluzzi L, Pietrocola F, Bravo-San Pedro JM et al. Autophagy in malignant transformation and cancer progression. The EMBO journal. Apr 01 2015; 34(7): 856-880.
  11. Russell RC, Yuan HX, Guan KL. Autophagy regulation by nutrient signaling. Cell research. Jan 2014; 24(1): 42-57.
  12. Hata AN, Engelman JA, Faber AC. The BCL2 Family: Key Mediators of the Apoptotic Response to Targeted Anticancer Therapeutics. Cancer discovery. May 2015; 5(5): 475-487.
  13. Galluzzi L, Pietrocola F, Levine B, Kroemer G. Metabolic control of autophagy. Cell. Dec 04 2014; 159(6): 1263-1276.
  14. Kaur A, Sharma S. Mammalian target of rapamycin (mTOR) as a potential therapeutic target in various diseases. Inflammopharmacology. Jun 2017; 25(3): 293-312.
  15. Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. Mar 09 2017; 168(6): 960-976.
  16. Ikenoue T, Hong S, Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods in enzymology. 2009; 452: 165-180.
  17. Ostenfeld MS, Hoyer-Hansen M, Bastholm L et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy. May 2008; 4(4): 487-499.
  18. Cohen A, Hall MN. An amino acid shuffle activates mTORC1. Cell. Feb 06 2009; 136(3): 399-400.
  19. Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: Targeting autophagy signalling in cancer cells -'trick or treats'? The FEBS journal. Nov 2009; 276(21): 6084-6096.
  20. Liang B, Kong D, Liu Y et al. Autophagy inhibition plays the synergetic killing roles with radiation in the multi-drug resistant SKVCR ovarian cancer cells. Radiation oncology (London, England). Dec 17 2012; 7: 213.
  21. Liang B, Liu X, Liu Y et al. Inhibition of autophagy sensitizes MDR-phenotype ovarian cancer SKVCR cells to chemotherapy. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie. Aug 2016; 82: 98-105.
  22. Algandaby MM, Breikaa RM, Eid BG, Neamatallah TA, Abdel-Naim AB, Ashour OM. Icariin protects against thioacetamide-induced liver fibrosis in rats: Implication of anti-angiogenic and anti-autophagic properties. Pharmacological reports : PR. Feb 24 2017; 69(4): 616-624.
  23. Li H, Yuan Y, Zhang Y, Zhang X, Gao L, Xu R. Icariin Inhibits AMPK-Dependent Autophagy and Adipogenesis in Adipocytes In vitro and in a Model of Graves' Orbitopathy In vivo. Frontiers in physiology. 2017; 8: 45.
  24. Tang Y, Jacobi A, Vater C, Zou L, Zou X, Stiehler M. Icariin promotes angiogenic differentiation and prevents oxidative stress-induced autophagy in endothelial progenitor cells. Stem cells (Dayton, Ohio). Jun 2015; 33(6): 1863-1877.
  25. Yoshimori T, Yamagata F, Yamamoto A et al. The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Molecular biology of the cell. Feb 2000; 11(2): 747-763.
  26. Buys TP, Chari R, Lee EH et al. Genetic changes in the evolution of multidrug resistance for cultured human ovarian cancer cells. Genes, chromosomes & cancer. Dec 2007; 46(12): 1069-1079.
  27. Hill BT, Whelan RD, Hurst HC, McClean S. Identification of a distinctive P-glycoprotein-mediated resistance phenotype in human ovarian carcinoma cells after their in vitro exposure to fractionated X-irradiation. Cancer. Jun 15 1994; 73(12): 2990-2999.
  28. Xue Y, Hou S, Ji H, Han X. Evolution from genetics to phenotype: reinterpretation of NSCLC plasticity, heterogeneity, and drug resistance. Protein & cell. Mar 2017; 8(3): 178-190.
  29. Zhang Q, Feng Y, Kennedy D. Multidrug-resistant cancer cells and cancer stem cells hijack cellular systems to circumvent systemic therapies, can natural products reverse this? Cellular and molecular life sciences : CMLS. Mar 2017; 74(5): 777-801.
  30. Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. Apr 01 2005; 23(10): 2411-2422.
  31. Meschini S, Condello M, Marra M, Formisano G, Federici E, Arancia G. Autophagy-mediated chemosensitizing effect of the plant alkaloid voacamine on multidrug resistant cells. Toxicology in vitro : an international journal published in association with BIBRA. Mar 2007; 21(2): 197-203.
  32. Luo S, Rubinsztein DC. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell death and differentiation. Feb 2010; 17(2): 268-277.
  33. Pagliarini V, Wirawan E, Romagnoli A et al. Proteolysis of Ambra1 during apoptosis has a role in the inhibition of the autophagic pro-survival response. Cell death and differentiation. Sep 2012; 19(9): 1495-1504.
  34. Wei Y, Sinha S, Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy. Oct 2008; 4(7): 949-951.
  35. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Molecular cell. Jun 20 2008; 30(6): 678-688.
  36. Reed JC. Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell death and differentiation. Aug 2006; 13(8): 1378-1386.
  37. Mirzayans R, Andrais B, Kumar P, Murray D. The Growing Complexity of Cancer Cell Response to DNA-Damaging Agents: Caspase 3 Mediates Cell Death or Survival? International journal of molecular sciences. May 11 2016; 17(5).
  38. Wiman KG, Zhivotovsky B. Understanding cell cycle and cell death regulation provides novel weapons against human diseases. Journal of internal medicine. May 2017; 281(5): 483-495.
  39. Dunlop EA, Tee AR. mTOR and autophagy: a dynamic relationship governed by nutrients and energy. Seminars in cell & developmental biology. Dec 2014; 36: 121-129.
  40. Wong PM, Puente C, Ganley IG, Jiang X. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy. Feb 01 2013; 9(2): 124-137.
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References


Ren F, Shen J, Shi H, Hornicek FJ, Kan Q, Duan Z. Novel mechanisms and approaches to overcome multidrug resistance in the treatment of ovarian cancer. Biochimica et biophysica acta. Dec 2016; 1866(2): 266-275.

Penson RT, Oliva E, Skates SJ et al. Expression of multidrug resistance-1 protein inversely correlates with paclitaxel response and survival in ovarian cancer patients: a study in serial samples. Gynecologic oncology. Apr 2004; 93(1): 98-106.

Hooks SB, Murph MM. Cellular deficiency in the RGS10 protein facilitates chemoresistant ovarian cancer. Future medicinal chemistry. Aug 2015; 7(12): 1483-1489.

Lord CJ, Tutt AN, Ashworth A. Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors. Annual review of medicine. 2015; 66: 455-470.

Marchetti C, Palaia I, De Felice F et al. Tyrosine-kinases inhibitors in recurrent platinum-resistant ovarian cancer patients. Cancer treatment reviews. Jan 2016; 42: 41-46.

Muralidhar GG, Barbolina MV. The miR-200 Family: Versatile Players in Epithelial Ovarian Cancer. International journal of molecular sciences. Jul 24 2015; 16(8): 16833-16847.

Kimmelman AC, White E. Autophagy and Tumor Metabolism. Cell metabolism. May 02 2017; 25(5): 1037-1043.

Mahase S, Rattenni RN, Wesseling P et al. Hypoxia-Mediated Mechanisms Associated with Antiangiogenic Treatment Resistance in Glioblastomas. The American journal of pathology. May 2017; 187(5): 940-953.

Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nature reviews Molecular cell biology. Sep 2007; 8(9): 741-752.

Galluzzi L, Pietrocola F, Bravo-San Pedro JM et al. Autophagy in malignant transformation and cancer progression. The EMBO journal. Apr 01 2015; 34(7): 856-880.

Russell RC, Yuan HX, Guan KL. Autophagy regulation by nutrient signaling. Cell research. Jan 2014; 24(1): 42-57.

Hata AN, Engelman JA, Faber AC. The BCL2 Family: Key Mediators of the Apoptotic Response to Targeted Anticancer Therapeutics. Cancer discovery. May 2015; 5(5): 475-487.

Galluzzi L, Pietrocola F, Levine B, Kroemer G. Metabolic control of autophagy. Cell. Dec 04 2014; 159(6): 1263-1276.

Kaur A, Sharma S. Mammalian target of rapamycin (mTOR) as a potential therapeutic target in various diseases. Inflammopharmacology. Jun 2017; 25(3): 293-312.

Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. Mar 09 2017; 168(6): 960-976.

Ikenoue T, Hong S, Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods in enzymology. 2009; 452: 165-180.

Ostenfeld MS, Hoyer-Hansen M, Bastholm L et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy. May 2008; 4(4): 487-499.

Cohen A, Hall MN. An amino acid shuffle activates mTORC1. Cell. Feb 06 2009; 136(3): 399-400.

Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: Targeting autophagy signalling in cancer cells -'trick or treats'? The FEBS journal. Nov 2009; 276(21): 6084-6096.

Liang B, Kong D, Liu Y et al. Autophagy inhibition plays the synergetic killing roles with radiation in the multi-drug resistant SKVCR ovarian cancer cells. Radiation oncology (London, England). Dec 17 2012; 7: 213.

Liang B, Liu X, Liu Y et al. Inhibition of autophagy sensitizes MDR-phenotype ovarian cancer SKVCR cells to chemotherapy. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie. Aug 2016; 82: 98-105.

Algandaby MM, Breikaa RM, Eid BG, Neamatallah TA, Abdel-Naim AB, Ashour OM. Icariin protects against thioacetamide-induced liver fibrosis in rats: Implication of anti-angiogenic and anti-autophagic properties. Pharmacological reports : PR. Feb 24 2017; 69(4): 616-624.

Li H, Yuan Y, Zhang Y, Zhang X, Gao L, Xu R. Icariin Inhibits AMPK-Dependent Autophagy and Adipogenesis in Adipocytes In vitro and in a Model of Graves' Orbitopathy In vivo. Frontiers in physiology. 2017; 8: 45.

Tang Y, Jacobi A, Vater C, Zou L, Zou X, Stiehler M. Icariin promotes angiogenic differentiation and prevents oxidative stress-induced autophagy in endothelial progenitor cells. Stem cells (Dayton, Ohio). Jun 2015; 33(6): 1863-1877.

Yoshimori T, Yamagata F, Yamamoto A et al. The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Molecular biology of the cell. Feb 2000; 11(2): 747-763.

Buys TP, Chari R, Lee EH et al. Genetic changes in the evolution of multidrug resistance for cultured human ovarian cancer cells. Genes, chromosomes & cancer. Dec 2007; 46(12): 1069-1079.

Hill BT, Whelan RD, Hurst HC, McClean S. Identification of a distinctive P-glycoprotein-mediated resistance phenotype in human ovarian carcinoma cells after their in vitro exposure to fractionated X-irradiation. Cancer. Jun 15 1994; 73(12): 2990-2999.

Xue Y, Hou S, Ji H, Han X. Evolution from genetics to phenotype: reinterpretation of NSCLC plasticity, heterogeneity, and drug resistance. Protein & cell. Mar 2017; 8(3): 178-190.

Zhang Q, Feng Y, Kennedy D. Multidrug-resistant cancer cells and cancer stem cells hijack cellular systems to circumvent systemic therapies, can natural products reverse this? Cellular and molecular life sciences : CMLS. Mar 2017; 74(5): 777-801.

Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. Apr 01 2005; 23(10): 2411-2422.

Meschini S, Condello M, Marra M, Formisano G, Federici E, Arancia G. Autophagy-mediated chemosensitizing effect of the plant alkaloid voacamine on multidrug resistant cells. Toxicology in vitro : an international journal published in association with BIBRA. Mar 2007; 21(2): 197-203.

Luo S, Rubinsztein DC. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell death and differentiation. Feb 2010; 17(2): 268-277.

Pagliarini V, Wirawan E, Romagnoli A et al. Proteolysis of Ambra1 during apoptosis has a role in the inhibition of the autophagic pro-survival response. Cell death and differentiation. Sep 2012; 19(9): 1495-1504.

Wei Y, Sinha S, Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy. Oct 2008; 4(7): 949-951.

Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Molecular cell. Jun 20 2008; 30(6): 678-688.

Reed JC. Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell death and differentiation. Aug 2006; 13(8): 1378-1386.

Mirzayans R, Andrais B, Kumar P, Murray D. The Growing Complexity of Cancer Cell Response to DNA-Damaging Agents: Caspase 3 Mediates Cell Death or Survival? International journal of molecular sciences. May 11 2016; 17(5).

Wiman KG, Zhivotovsky B. Understanding cell cycle and cell death regulation provides novel weapons against human diseases. Journal of internal medicine. May 2017; 281(5): 483-495.

Dunlop EA, Tee AR. mTOR and autophagy: a dynamic relationship governed by nutrients and energy. Seminars in cell & developmental biology. Dec 2014; 36: 121-129.

Wong PM, Puente C, Ganley IG, Jiang X. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy. Feb 01 2013; 9(2): 124-137.

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