Fol. Biol. 2022, 68, 59-71
https://doi.org/10.14712/fb2022068020059
Docosahexaenoic Acid Reverses Epithelial-Mesenchymal Transition and Drug Resistance by Impairing the PI3K/AKT/Nrf2/GPX4 Signalling Pathway in Docetaxel-Resistant PC3 Prostate Cancer Cells
References
1. Ashrafizadeh, M., Mirzaei, S., Hashemi, F., Zarrabi, A., Zabolian, A., Saleki, H., Sharifzadeh, S. O., Soleymani, L., Daneshi, S., Hushmandi, K., Khan, H., Kumar, A. P., Aref, A. R., Samarghandian, S. (2021) New insight towards development of paclitaxel and docetaxel resistance in cancer cells: EMT as a novel molecular mechanism and therapeutic possibilities. Biomed. Pharmacother. 141, 111824.
<https://doi.org/10.1016/j.biopha.2021.111824>
2. Bougnoux, P., Hajjaji, N., Ferrasson, M. N., Giraudeau, B., Couet, C., Le Floch, O. (2009) Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: a phase II trial. Br. J. Cancer 101, 1978-1985.
<https://doi.org/10.1038/sj.bjc.6605441>
3. Chen, B., Zhang, Y., Li, C., Xu, P., Gao, Y., Xu, Y. (2021) CNTN-1 promotes docetaxel resistance and epithelial-tomesenchymal transition via the PI3K/Akt signaling pathway in prostate cancer. Arch. Med. Sci. 17, 152-165.
<https://doi.org/10.5114/aoms.2020.92939>
4. Curtin, J. F., Cotter, T. G. (2004) JNK regulates HIPK3 expression and promotes resistance to Fas-mediated apoptosis in DU 145 prostate carcinoma cells. J. Biol. Chem. 279, 17090-17100.
<https://doi.org/10.1074/jbc.M307629200>
5. Deng, J., Bai, X., Feng, X., Ni, J., Beretov, J., Graham, P., Li, Y. (2019) Inhibition of PI3K/Akt/mTOR signaling pathway alleviates ovarian cancer chemoresistance through reversing epithelial-mesenchymal transition and decreasing cancer stem cell marker expression. BMC Cancer 19, 618.
<https://doi.org/10.1186/s12885-019-5824-9>
6. Dongre, A., Weinberg, R. A. (2019) New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer. Nat. Rev. Mol. Cell. Biol. 20, 69-84.
<https://doi.org/10.1038/s41580-018-0080-4>
7. Du, B., Shim, J. S. (2016) Targeting epithelial-mesenchymal transition (EMT) to overcome drug resistance in cancer. Molecules 21, 965.
<https://doi.org/10.3390/molecules21070965>
8. Du, J., Wang, T., Li, Y., Zhou, Y., Wang, X., Yu, X., Ren, X., An, Y., Wu, Y., Sun, W., Fan, W., Zhu, Q., Wang, Y., Tong, X. (2019) DHA inhibits proliferation and induces ferroptosis of leukemia cells through autophagy dependent degradation of ferritin. Free Radic. Biol. Med. 131, 356-369.
<https://doi.org/10.1016/j.freeradbiomed.2018.12.011>
9. El-Ashmawy, N. E., Al-Ashmawy, G. M., Amr, E. A., Khedr, E. G. (2020) Inhibition of lovastatin- and docosahexaenoic acid-initiated autophagy in triple negative breast cancer reverted resistance and enhanced cytotoxicity. Life Sci. 259, 118212.
<https://doi.org/10.1016/j.lfs.2020.118212>
10. Elgendy, S. M., Alyammahi, S. K., Alhamad, D. W., Abdin, S. M., Omar, H. A. (2020) Ferroptosis: an emerging approach for targeting cancer stem cells and drug resistance. Crit. Rev. Oncol. Hematol. 155, 103095.
<https://doi.org/10.1016/j.critrevonc.2020.103095>
11. Esteve, J. M., Knecht, E. (2011) Mechanisms of autophagy and apoptosis: recent developments in breast cancer cells. World J. Biol. Chem. 2, 232-238.
<https://doi.org/10.4331/wjbc.v2.i10.232>
12. Gao, L., Loveless, J., Shay, C., Teng, Y. (2020) Targeting ROS-mediated crosstalk between autophagy and apoptosis in cancer. Adv. Exp. Med. Biol. 1260, 1-12.
<https://doi.org/10.1007/978-3-030-42667-5_1>
13. Hokaiwado, N., Takeshita, F., Naiki-Ito, A., Asamoto, M., Ochiya, T., Shirai, T. (2008) Glutathione S-transferase pi mediates proliferation of androgen-independent prostate cancer cells. Carcinogenesis 29, 1134-1138.
<https://doi.org/10.1093/carcin/bgn097>
14. 2015) Omega-3 fatty acids and cardiovascular disease. Eur. Rev. Med. Pharmacol. Sci. 19, 441-445.
, A. P., Aggarwal, K. K., Zhang, P. Y. (
15. Jing, K., Wu, T., Lim, K. (2013) Omega-3 polyunsaturated fatty acids and cancer. Anticancer Agents Med. Chem. 13, 1162-1177.
<https://doi.org/10.2174/18715206113139990319>
16. Kim, K. Y., Kim, S. H., Yu, S. N., Park, S. G., Kim, Y. W., Nam, H. W., An, H. H., Yu, H. S., Kim, Y. W., Ji, J. H., Seo, Y. K., Ahn, S. C. (2017) Lasalocid induces cytotoxic apoptosis and cytoprotective autophagy through reactive oxygen species in human prostate cancer PC-3 cells. Biomed. Pharmacother. 88, 1016-1024.
<https://doi.org/10.1016/j.biopha.2017.01.140>
17. Kim, N., Jeong, S., Jing, K., Shin, S., Kim, S., Heo, J. Y., Kweon, G. R., Park, S. K., Wu, T., Park, J. I., Lim, K. (2015) Docosahexaenoic acid induces cell death in human non-small cell lung cancer cells by repressing mTOR via AMPK activation and PI3K/Akt inhibition. Biomed. Res. Int. 2015, 239764.
<https://doi.org/10.1155/2015/239764>
18. Kosaka, T., Miyajima, A., Shirotake, S., Suzuki, E., Kikuchi, E., Oya, M. (2011) Long-term androgen ablation and docetaxel up-regulate phosphorylated Akt in castration resistant prostate cancer. J. Urol. 185, 2376-2381.
<https://doi.org/10.1016/j.juro.2011.02.016>
19. Kranzbuhler, B., Salemi, S., Mortezavi, A., Sulser, T., Eberli, D. (2019) Combined N-terminal androgen receptor and autophagy inhibition increases the antitumor effect in enzalutamide sensitive and enzalutamide resistant prostate cancer cells. Prostate 79, 206-214.
<https://doi.org/10.1002/pros.23725>
20. Li, J., Cao, F., Yin, H. L., Huang, Z. J., Lin, Z. T., Mao, N., Sun, B., Wang, G. (2020) Ferroptosis: past, present and future. Cell Death Dis. 11, 88.
<https://doi.org/10.1038/s41419-020-2298-2>
21. Liu, C. M., Kao, C. L., Tseng, Y. T., Lo, Y. C., Chen, C. Y. (2017) Ginger phytochemicals inhibit cell growth and modulate drug resistance factors in docetaxel resistant prostate cancer cell. Molecules 22, 1477.
<https://doi.org/10.3390/molecules22091477>
22. Liu, T., Zhang, X., Du, L., Wang, Y., Liu, X., Tian, H., Wang, L., Li, P., Zhao, Y., Duan, W., Xie, Y., Sun, Z., Wang, C. (2019) Exosome-transmitted miR-128-3p increase chemosensitivity of oxaliplatin-resistant colorectal cancer. Mol. Cancer 18, 43.
<https://doi.org/10.7150/jca.26723>
23. Mansinho, A., Macedo, D., Fernandes, I., Costa, L. (2018) Castration-resistant prostate cancer: mechanisms, targets and treatment. Adv. Exp. Med. Biol. 1096, 117-133.
<https://doi.org/10.1007/978-3-319-99286-0_7>
24. Merendino, N., Molinari, R., Loppi, B., Pessina, G., M, D. A., Tomassi, G.,Velotti, F. (2003) Induction of apoptosis in human pancreatic cancer cells by docosahexaenoic acid. Ann. N. Y. Acad. Sci. 1010, 361-364.
<https://doi.org/10.1196/annals.1299.143>
25. Nehme, A., Varadarajan, P., Sellakumar, G., Gerhold, M., Niedner, H., Zhang, Q., Lin, X., Christen, R. D. (2001) Modulation of docetaxel-induced apoptosis and cell cycle arrest by all-trans retinoic acid in prostate cancer cells. Br. J. Cancer 84, 1571-1576.
<https://doi.org/10.1054/bjoc.2001.1818>
26. Newell, M., Goruk, S., Mazurak, V., Postovit, L., Field, C. J. (2019) Role of docosahexaenoic acid in enhancement of docetaxel action in patient-derived breast cancer xenografts. Breast Cancer Res. Treat. 177, 357-367.
<https://doi.org/10.1007/s10549-019-05331-8>
27. Ouyang, D. Y., Xu, L. H., He, X. H., Zhang, Y. T., Zeng, L. H., Cai, J. Y., Ren, S. (2013) Autophagy is differentially induced in prostate cancer LNCaP, DU145 and PC-3 cells via distinct splicing profiles of ATG5. Autophagy 9, 20-32.
<https://doi.org/10.4161/auto.22397>
28. Park, J. H., Kim, Y. H., Park, E. H., Lee, S. J., Kim, H., Kim, A., Lee, S. B., Shim, S., Jang, H., Myung, J. K., Park, S., Lee, S. J., Kim, M. J. (2019) Effects of metformin and phenformin on apoptosis and epithelial-mesenchymal transition in chemoresistant rectal cancer. Cancer Sci. 110, 2834-2845.
<https://doi.org/10.1111/cas.14124>
29. Poorani, R., Bhatt, A. N., Dwarakanath, B. S., Das, U. N. (2016) COX-2, aspirin and metabolism of arachidonic, eicosapentaenoic and docosahexaenoic acids and their physiological and clinical significance. Eur. J. Pharmacol. 785, 116-132.
<https://doi.org/10.1016/j.ejphar.2015.08.049>
30. Rosenfeld, M. R., Ye, X., Supko, J. G., Desideri, S., Grossman, S. A., Brem, S., Mikkelson, T., Wang, D., Chang, Y. C., Hu, J., McAfee, Q., Fisher, J., Troxel, A. B., Piao, S., Heitjan, D. F., Tan, K. S., Pontiggia, L., O'Dwyer, P. J., Davis, L. E., Amaravadi, R. K. (2014) A phase I/II trial of hydroxychloroquine in conjunction with radiation therapy and concurrent and adjuvant temozolomide in patients with newly diagnosed glioblastoma multiforme. Autophagy 10, 1359-1368.
<https://doi.org/10.4161/auto.28984>
31. Ryabaya, O. O., Inshakov, A. N., Egorova, A. V., Emelyanova, M. A., Nasedkina, T. V., Zasedatelev, A. S., Khochenkov, D. A., Stepanova, E. V. (2017) Autophagy inhibitors chloroquine and LY294002 enhance temozolomide cytotoxicity on cutaneous melanoma cell lines in vitro. Anticancer Drugs 28, 307-315.
<https://doi.org/10.1097/CAD.0000000000000463>
32. Shahidi, F., Ambigaipalan, P. (2018) Omega-3 polyunsaturated fatty acids and their health benefits. Annu. Rev. Food Sci. Technol. 9, 345-381.
<https://doi.org/10.1146/annurev-food-111317-095850>
33. Shaikh, I. A., Brown, I., Schofield, A. C., Wahle, K. W., Heys, S. D. (2008) Docosahexaenoic acid enhances the efficacy of docetaxel in prostate cancer cells by modulation of apoptosis: the role of genes associated with the NF-κB pathway. Prostate 68, 1635-1646.
<https://doi.org/10.1002/pros.20830>
34. Shekari, N., Javadian, M., Ghasemi, M., Baradaran, B., Darabi, M., Kazemi, T. (2020) Synergistic beneficial effect of docosahexaenoic acid (DHA) and docetaxel on the expression level of matrix metalloproteinase-2 (MMP-2) and microRNA- 106b in gastric cancer. J. Gastrointest. Cancer 51, 70-75.
<https://doi.org/10.1007/s12029-019-00205-0>
35. Shin, D., Kim, E. H., Lee, J., Roh, J. L. (2018) Nrf2 inhibition reverses resistance to GPX4 inhibitor-induced ferroptosis in head and neck cancer. Free Radic. Biol. Med. 129, 454- 462.
<https://doi.org/10.1016/j.freeradbiomed.2018.10.426>
36. Shin, S., Jing, K., Jeong, S., Kim, N., Song, K. S., Heo, J. Y., Park, J. H., Seo, K. S., Han, J., Park, J. I., Kweon, G. R., Park, S. K., Wu, T., Hwang, B. D., Lim, K. (2013) The omega-3 polyunsaturated fatty acid DHA induces simultaneous apoptosis and autophagy via mitochondrial ROSZ-mediated Akt-mTOR signaling in prostate cancer cells expressing mutant p53. Biomed Res. Int. 2013, 568671.
<https://doi.org/10.1155/2013/568671>
37. Simopoulos, A. P. (2002) The importance of the ratio of omega- 6/omega-3 essential fatty acids. Biomed. Pharmacother. 56, 365-379.
<https://doi.org/10.1016/S0753-3322(02)00253-6>
38. Smith, A. G., Macleod, K. F. (2019) Autophagy, cancer stem cells and drug resistance. J. Pathol. 247, 708-718. Song, E. A., Kim, H. (2016) Docosahexaenoic acid induces oxidative DNA damage and apoptosis, and enhances the chemosensitivity of cancer cells. Int. J. Mol. Sci. 17, 1257.
<https://doi.org/10.3390/ijms17081257>
39. Tsai, C. H., Shen, Y. C., Chen, H. W., Liu, K. L., Chang, J. W., Chen, P. Y., Lin, C. Y., Yao, H. T., Li, C. C. (2017) Docosahexaenoic acid increases the expression of oxidative stressinduced growth inhibitor 1 through the PI3K/Akt/Nrf2 signaling pathway in breast cancer cells. Food Chem. Toxicol. 108, 276-288.
<https://doi.org/10.1016/j.fct.2017.08.010>
40. van Brussel, J. P., van Steenbrugge, G. J., Romijn, J. C., Schroder, F. H., Mickisch, G. H. (1999) Chemosensitivity of prostate cancer cell lines and expression of multidrug resistance- related proteins. Eur. J. Cancer 35, 664-671.
<https://doi.org/10.1016/S0959-8049(98)00435-3>
41. Vijay, G. V., Zhao, N., Den Hollander, P., Toneff, M. J., Joseph, R., Pietila, M., Taube, J. H., Sarkar, T. R., Ramirez- Pena, E., Werden, S. J., Shariati, M., Gao, R., Sobieski, M., Stephan, C. C., Sphyris, N., Miura, N., Davies, P., Chang, J. T., Soundararajan, R., Rosen, J. M., Mani, S. A. (2019) GSK3β regulates epithelial-mesenchymal transition and cancer stem cell properties in triple-negative breast cancer. Breast Cancer Res. 21, 37.
<https://doi.org/10.1186/s13058-019-1125-0>
42. Wang, G., Zhao, D., Spring, D. J., DePinho, R. A. (2018a) Genetics and biology of prostate cancer. Genes Dev. 32, 1105-1140.
<https://doi.org/10.1101/gad.315739.118>
43. 2018b) Wogonoside reverses cisplatin resistance in SGC7901/cDDP cells through inhibition of PI3K/Akt/Nrf2/ARE signaling pathway. Sheng Li Xue Bao 70, 397-405. (in Chinese)
, L. J., Wang, S. G., Deng, T. X. (
44. Wright, T. J., McKee, C., Birch-Machin, M. A., Ellis, R., Armstrong, J. L., Lovat, P. E. (2013) Increasing the therapeutic efficacy of docetaxel for cutaneous squamous cell carcinoma through the combined inhibition of phosphatidylinositol 3-kinase/AKT signalling and autophagy. Clin. Exp. Dermatol. 38, 421-423.
<https://doi.org/10.1111/ced.12138>
45. 2019) Docosahexaenoic acid inhibits lipopolysaccharide-induced metastatic activities by decreasing inflammation on prostate cancer cell. Pharmazie 74, 675-679.
, Z., Chen, C. Y., Kao, C. L., Jiang, Y., Liu, C. M. (
46. Xu, Y., Yu, H., Qin, H., Kang, J., Yu, C., Zhong, J., Su, J., Li, H., Sun, L. (2012) Inhibition of autophagy enhances cisplatin cytotoxicity through endoplasmic reticulum stress in human cervical cancer cells. Cancer Lett. 314, 232-243.
<https://doi.org/10.1016/j.canlet.2011.09.034>
47. Yamaguchi, H., Hsu, J. L., Chen, C. T., Wang, Y. N., Hsu, M. C., Chang, S. S., Du, Y., Ko, H. W., Herbst, R., Hung, M. C. (2013) Caspase-independent cell death is involved in the negative effect of EGF receptor inhibitors on cisplatin in non-small cell lung cancer cells. Clin. Cancer Res. 19, 845-854.
<https://doi.org/10.1158/1078-0432.CCR-12-2621>
48. Zhang, Y., Wang, Y., Yuan, J., Qin, W., Liu, F., Wang, F., Zhang, G., Yang, X. (2012) Toll-like receptor 4 ligation confers chemoresistance to docetaxel on PC-3 human prostate cancer cells. Cell Biol. Toxicol. 28, 269-277.
<https://doi.org/10.1007/s10565-012-9221-2>