G-Protein-Coupled Receptor 120 Mediates DHA-Induced Apoptosis by Regulating IP3R, ROS and, ER Stress Levels in Cisplatin-Resistant Cancer Cells |
Shin, Jong-Il
(Department of Biological Sciences, Konkuk University)
Jeon, Yong-Joon (Department of Biological Sciences, Konkuk University) Lee, Sol (Department of Biological Sciences, Konkuk University) Lee, Yoon Gyeong (Department of Biological Sciences, Konkuk University) Kim, Ji Beom (Department of Biological Sciences, Konkuk University) Lee, Kyungho (Department of Biological Sciences, Konkuk University) |
1 | Han, J., Back, S.H., Hur, J., Lin, Y.H., Gildersleeve, R., Shan, J., Yuan, C.L., Krokowski, D., Wang, S., Hatzoglou, M., et al. (2013). ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15, 481-490. DOI |
2 | Harding, H.P., Calfon, M., Urano, F., Novoa, I., and Ron, D. (2002). Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18, 575-599. DOI |
3 | Hirasawa, A., Tsumaya, K., Awaji, T., Katsuma, S., Adachi, T., Yamada, M., Sugimoto, Y., Miyazaki, S., and Tsujimoto, G. (2005). Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat. Med. 11, 90-94. DOI |
4 | Hopkins, M.M., and Meier, K.E. (2017). Free fatty acid receptors and cancer: from nutrition to pharmacology. Handb. Exp. Pharmacol. 236, 233-251. DOI |
5 | Itoh, Y., Kawamata, Y., Harada, M., Kobayashi, M., Fujii, R., Fukusumi, S., Ogi, K., Hosoya, M., Tanaka, Y., Uejima, H., et al. (2003). Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173-176. DOI |
6 | Ivanova, H., Vervliet, T., Missiaen, L., Parys, J.B., De Smedt, H., and Bultynck, G. (2014). Inositol 1,4,5-trisphosphate receptor-isoform diversity in cell death and survival. Biochim. Biophys. Acta 1843, 2164-2183. DOI |
7 | Jakobsen, C.H., Storvold, G.L., Bremseth, H., Follestad, T., Sand, K., Mack, M., Olsen, K.S., Lundemo, A.G., Iversen, J.G., Krokan, H.E., et al. (2008). DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis. J. Lipid Res. 49, 2089-2100. DOI |
8 | Rutkowski, D.T., and Kaufman, R.J. (2004). A trip to the ER: coping with stress. Trends Cell Biol. 14, 20-28. DOI |
9 | Sancho-Martinez, S.M., Prieto-Garcia, L., Prieto, M., Lopez-Novoa, J.M., and Lopez-Hernandez, F.J. (2012). Subcellular targets of cisplatin cytotoxicity: an integrated view. Pharmacol. Ther. 136, 35-55. DOI |
10 | Saris, C.P., van de Vaart, P.J., Rietbroek, R.C., and Blommaert, F.A. (1996). In vitro formation of DNA adducts by cisplatin, lobaplatin and oxaliplatin in calf thymus DNA in solution and in cultured human cells. Carcinogenesis 17, 2763-2769. DOI |
11 | Senatorov, I.S., and Moniri, N.H. (2018). The role of free-fatty acid receptor-4 (FFA4) in human cancers and cancer cell lines. Biochem. Pharmacol. 150, 170-180. DOI |
12 | Shah, B.P., Liu, P., Yu, T., Hansen, D.R., and Gilbertson, T.A. (2012). TRPM5 is critical for linoleic acid-induced CCK secretion from the enteroendocrine cell line, STC-1. Am. J. Physiol. Cell Physiol. 302, C210-219. DOI |
13 | Shin, J.I., Jeon, Y.J., Lee, S., Lee, Y.G., Kim, J.B., Kwon, H.C., Kim, S.H., Kim, I., Lee, K., and Han, Y.S. (2018). Apoptotic and anti-inflammatory effects of eupatorium japonicum thunb. in rheumatoid arthritis fibroblast-like synoviocytes. Biomed. Res. Int. 2018, 1383697. |
14 |
Begum, G., Kintner, D., Liu, Y., Cramer, S.W., and Sun, D. (2012). DHA inhibits ER |
15 | So, J.S. (2018). Roles of endoplasmic reticulum stress in immune responses. Mol. Cells 41, 705-716. DOI |
16 | Stamp, L.K., James, M.J., and Cleland, L.G. (2005). Diet and rheumatoid arthritis: a review of the literature. Semin. Arthritis Rheum. 35, 77-94. DOI |
17 |
Szabadkai, G., Bianchi, K., Varnai, P., De Stefani, D., Wieckowski, M.R., Cavagna, D., Nagy, A.I., Balla, T., and Rizzuto, R. (2006). Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial |
18 | Aires, V., Hichami, A., Filomenko, R., Ple, A., Rebe, C., Bettaieb, A., and Khan, N.A. (2007). Docosahexaenoic acid induces increases in [Ca2+]i via inositol 1,4,5-triphosphate production and activates protein kinase C gamma and -delta via phosphatidylserine binding site: implication in apoptosis in U937 cells. Mol. Pharmacol. 72, 1545-1556. DOI |
19 | Begum, G., Harvey, L., Dixon, C.E., and Sun, D. (2013). ER stress and effects of DHA as an ER stress inhibitor. Translational Stroke Research 4, 635-642. DOI |
20 | Burns, C.P., Luttenegger, D.G., Dudley, D.T., Buettner, G.R., and Spector, A.A. (1979). Effect of modification of plasma membrane fatty acid composition on fluidity and methotrexate transport in L1210 murine leukemia cells. Cancer Res. 39, 1726-1732. |
21 | Cao, S.S., and Kaufman, R.J. (2014). Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxidants & Redox Signaling 21, 396-413. DOI |
22 | Chamras, H., Ardashian, A., Heber, D., and Glaspy, J.A. (2002). Fatty acid modulation of MCF-7 human breast cancer cell proliferation, apoptosis and differentiation. J. Nutr. Biochem. 13, 711-716. DOI |
23 | Corsetto, P.A., Colombo, I., Kopecka, J., Rizzo, A.M., and Riganti, C. (2017). Omega-3 long chain polyunsaturated fatty acids as sensitizing agents and multidrug resistance revertants in cancer therapy. Int. J. Mol. Sci. 18, 2770. DOI |
24 | Khalfoun, B., Thibault, F., Watier, H., Bardos, P., and Lebranchu, Y. (1997). Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6. Adv. Exp. Med. Biol. 400B, 589-597. |
25 | Kang, K.S., Wang, P., Yamabe, N., Fukui, M., Jay, T., and Zhu, B.T. (2010). Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS One 5, e10296. DOI |
26 | Kato, T., Hancock, R.L., Mohammadpour, H., McGregor, B., Manalo, P., Khaiboullina, S., Hall, M.R., Pardini, L., and Pardini, R.S. (2002). Influence of omega-3 fatty acids on the growth of human colon carcinoma in nude mice. Cancer Lett. 187, 169-177. DOI |
27 | Katsuma, S., Hatae, N., Yano, T., Ruike, Y., Kimura, M., Hirasawa, A., and Tsujimoto, G. (2005). Free fatty acids inhibit serum deprivation-induced apoptosis through GPR120 in a murine enteroendocrine cell line STC-1. J. Biol. Chem. 280, 19507-19515. DOI |
28 | Kim, H.S., Lim, J.M., Kim, J.Y., Kim, Y., Park, S., and Sohn, J. (2016). Panaxydol, a component of Panax ginseng, induces apoptosis in cancer cells through EGFR activation and ER stress and inhibits tumor growth in mouse models. Int. J. Cancer 138, 1432-1441. DOI |
29 | Lee, S., and Min, K.T. (2018). The Interface Between ER and Mitochondria: Molecular Compositions and Functions. Mol. Cells 41, 1000-1007. DOI |
30 | Li, G., Mongillo, M., Chin, K.T., Harding, H., Ron, D., Marks, A.R., and Tabas, I. (2009). Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J. Cell Biol. 186, 783-792. DOI |
31 | Torigoe, T., Izumi, H., Ishiguchi, H., Yoshida, Y., Tanabe, M., Yoshida, T., Igarashi, T., Niina, I., Wakasugi, T., Imaizumi, T., et al. (2005). Cisplatin resistance and transcription factors. Curr. Med. Chem. Anticancer Agents 5, 15-27. DOI |
32 | Taniuchi, S., Miyake, M., Tsugawa, K., Oyadomari, M., and Oyadomari, S. (2016). Integrated stress response of vertebrates is regulated by four eIF2alpha kinases. Sci. Rep. 6, 32886. DOI |
33 | Terry, P.D., Rohan, T.E., and Wolk, A. (2003). Intakes of fish and marine fatty acids and the risks of cancers of the breast and prostate and of other hormone-related cancers: a review of the epidemiologic evidence. Am. J. Clin. Nutr. 77, 532-543. DOI |
34 | Timmer-Bosscha, H., Hospers, G.A., Meijer, C., Mulder, N.H., Muskiet, F.A., Martini, I.A., Uges, D.R., and de Vries, E.G. (1989). Influence of docosahexaenoic acid on cisplatin resistance in a human small cell lung carcinoma cell line. J. Natl. Cancer Inst. 81, 1069-1075. DOI |
35 | Usanova, S., Piee-Staffa, A., Sied, U., Thomale, J., Schneider, A., Kaina, B., and Koberle, B. (2010). Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression. Mol. Cancer 9, 248. DOI |
36 | Das, U.N., and Madhavi, N. (2011). Effect of polyunsaturated fatty acids on drug-sensitive and resistant tumor cells in vitro. Lipids Health Dis. 10, 159. DOI |
37 | Verfaillie, T., Rubio, N., Garg, A.D., Bultynck, G., Rizzuto, R., Decuypere, J.P., Piette, J., Linehan, C., Gupta, S., Samali, A., et al. (2012). PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ. 19, 1880-1891. DOI |
38 | Wang, S.F., Chen, M.S., Chou, Y.C., Ueng, Y.F., Yin, P.H., Yeh, T.S., and Lee, H.C. (2016). Mitochondrial dysfunction enhances cisplatin resistance in human gastric cancer cells via the ROS-activated GCN2-eIF2alpha-ATF4-xCT pathway. Oncotarget 7, 74132-74151. DOI |
39 | Crnkovic, S., Riederer, M., Lechleitner, M., Hallstrom, S., Malli, R., Graier, W.F., Lindenmann, J., Popper, H., Olschewski, H., Olschewski, A., et al. (2012). Docosahexaenoic acid-induced unfolded protein response, cell cycle arrest, and apoptosis in vascular smooth muscle cells are triggered by Ca(2)(+)-dependent induction of oxidative stress. Free Radic. Biol. Med. 52, 1786-1795. DOI |
40 | Dai, J., Shen, J., Pan, W., Shen, S., and Das, U.N. (2013). Effects of polyunsaturated fatty acids on the growth of gastric cancer cells in vitro. Lipids Health Dis. 12, 71. DOI |
41 | Eastman, A. (1983). Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cisdichloro(ethylenediamine)platinum(II). Biochemistry 22, 3927-3933. DOI |
42 | Fasano, E., Serini, S., Piccioni, E., Toesca, A., Monego, G., Cittadini, A.R., Ranelletti, F.O., and Calviello, G. (2012). DHA induces apoptosis by altering the expression and cellular location of GRP78 in colon cancer cell lines. Biochim. Biophys. Acta 1822, 1762-1772. DOI |
43 | Galluzzi, L., Senovilla, L., Vitale, I., Michels, J., Martins, I., Kepp, O., Castedo, M., and Kroemer, G. (2012). Molecular mechanisms of cisplatin resistance. Oncogene 31, 1869-1883. DOI |
44 | Gelsomino, G., Corsetto, P.A., Campia, I., Montorfano, G., Kopecka, J., Castella, B., Gazzano, E., Ghigo, D., Rizzo, A.M., and Riganti, C. (2013). Omega 3 fatty acids chemosensitize multidrug resistant colon cancer cells by down-regulating cholesterol synthesis and altering detergent resistant membranes composition. Mol. Cancer 12, 137. DOI |
45 | Narayanan, B.A., Narayanan, N.K., and Reddy, B.S. (2001). Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells. Int. J. Oncol. 19, 1255-1262. |
46 | Liu, Z.W., Zhu, H.T., Chen, K.L., Dong, X., Wei, J., Qiu, C., and Xue, J.H. (2013). Protein kinase RNA-like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)-mediated endoplasmic reticulum stress-induced apoptosis in diabetic cardiomyopathy. Cardiovasc. Diabetol. 12, 158. DOI |
47 | Mandic, A., Hansson, J., Linder, S., and Shoshan, M.C. (2003). Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J. Biol. Chem. 278, 9100-9106. DOI |
48 | Mori, T.A., Woodman, R.J., Burke, V., Puddey, I.B., Croft, K.D., and Beilin, L.J. (2003). Effect of eicosapentaenoic acid and docosahexaenoic acid on oxidative stress and inflammatory markers in treated-hypertensive type 2 diabetic subjects. Free Radic. Biol. Med. 35, 772-781. DOI |
49 | Oh, D.Y., Talukdar, S., Bae, E.J., Imamura, T., Morinaga, H., Fan, W., Li, P., Lu, W.J., Watkins, S.M., and Olefsky, J.M. (2010). GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142, 687-698. DOI |
50 | Oyadomari, S., and Mori, M. (2004). Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389. DOI |
51 | Pedruzzi, E., Guichard, C., Ollivier, V., Driss, F., Fay, M., Prunet, C., Marie, J.C., Pouzet, C., Samadi, M., Elbim, C., et al. (2004). NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol. Cell. Biol. 24, 10703-10717. DOI |
52 | Xu, H., Choi, S.M., An, C.S., Min, Y.D., Kim, K.C., Kim, K.J., and Choi, C.H. (2005). Concentration-dependent collateral sensitivity of cisplatin-resistant gastric cancer cell sublines. Biochem. Biophys. Res. Commun. 328, 618-622. DOI |
53 | Ron, D., and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529. DOI |
54 | Wang, W., Ke, S., Chen, G., Gao, Q., Wu, S., Wang, S., Zhou, J., Yang, X., Lu, Y., and Ma, D. (2004). Effect of lung resistance-related protein on the resistance to cisplatin in human ovarian cancer cell lines. Oncol. Rep. 12, 1365-1370. |
55 | Watson, S.J., Brown, A.J., and Holliday, N.D. (2012). Differential signaling by splice variants of the human free fatty acid receptor GPR120. Mol. Pharmacol. 81, 631-642. DOI |
56 | Wek, R.C., Jiang, H.Y., and Anthony, T.G. (2006). Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11. DOI |
57 | Weldon, S.M., Mullen, A.C., Loscher, C.E., Hurley, L.A., and Roche, H.M. (2007). Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J. Nutr. Biochem. 18, 250-258. DOI |
58 | Yu, F., Megyesi, J., and Price, P.M. (2008). Cytoplasmic initiation of cisplatin cytotoxicity. Am. J. Physiol. Renal Physiol. 295, F44-52. DOI |
59 | Zijlstra, J.G., de Vries, E.G., Muskiet, F.A., Martini, I.A., Timmer-Bosscha, H., and Mulder, N.H. (1987). Influence of docosahexaenoic acid in vitro on intracellular adriamycin concentration in lymphocytes and human adriamycin-sensitive and -resistant small-cell lung cancer cell lines, and on cytotoxicity in the tumor cell lines. Int. J. Cancer 40, 850-856. DOI |
60 | Zhang, J.S., Zhou, S.F., Wang, Q., Guo, J.N., Liang, H.M., Deng, J.B., and He, W.Y. (2016). Gastrodin suppresses BACE1 expression under oxidative stress condition via inhibition of the PKR/eIF2alpha pathway in Alzheimer's disease. Neuroscience 325, 1-9. DOI |
61 | Gotoh, C., Hong, Y.H., Iga, T., Hishikawa, D., Suzuki, Y., Song, S.H., Choi, K.C., Adachi, T., Hirasawa, A., Tsujimoto, G., et al. (2007). The regulation of adipogenesis through GPR120. Biochem. Biophys. Res. Commun. 354, 591-597. DOI |
![]() |