Silibinin induces mitochondrial NOX4-mediated endoplasmic reticulum stress response and its subsequent apoptosis

BMC Cancer

Volumn 16, Issue 1, 2016, Pages

  Kim, Sang Hun ^a   Kim, Kwang Youn ^b   Yu, Sun Nyoung ^a,c   Seo, Young Kyo ^b   Chun, Sung Sik ^d   Yu, Hak Sun ^a,c   Ahn, Soon Cheol ^a,c  

^a Pusan National University School of Medicine   (South Korea)

^b Ulsan National Institute of Science and Technology   (South Korea)

^c Pusan National University   (South Korea)

^d International University of Korea   (South Korea)

Author keywords

Apoptosis; Ca2+; Endoplasmic reticulum stress; NOX; Reactive oxygen species; Silibinin

Indexed keywords

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SILIBININ; ANTINEOPLASTIC AGENT; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SILYMARIN;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE POTENTIAL; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; ENDOPLASMIC RETICULUM; MALE; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; MALE; MITOCHONDRIA; NADPH OXIDASE; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SILYMARIN;

EID: 84978200057     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-016-2516-6     Document Type: Article

References (46)

1. Dewaele M, Maes H, Agostinis P. ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy. 2010;6(7):838-54.
2. Li ZY, Yang Y, Ming M, Liu B. Mitochondrial ROS generation for regulation of autophagic pathways in cancer. Biochem Biophys Res Commun. 2011;414(1):5-8.
3. Holmstrom KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol. 2014;15(6):411-21.
4. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84.
5. Huang J, Lam GY, Brumell JH. Autophagy signaling through reactive oxygen species. Antioxid Redox Signal. 2011;14(11):2215-31.
6. Hickman JA. Apoptosis induced by anticancer drugs. Cancer Metastasis Rev. 1992;11(2):121-39.
7. Canman CE, Gilmer TM, Coutts SB, Kastan MB. Growth factor modulation of p53-mediated growth arrest versus apoptosis. Genes Dev. 1995;9(5):600-11.
8. Chan WH, Yu JS. Inhibition of UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermal carcinoma A431 cells by genistein. J Cell Biochem. 2000;78(1):73-84.
9. Kim KY, Yu SN, Lee SY, Chun SS, Choi YL, Park YM, et al. Salinomycin-induced apoptosis of human prostate cancer cells due to accumulated reactive oxygen species and mitochondrial membrane depolarization. Biochem Biophys Res Commun. 2011;413(1):80-6.
10. Ouyang YB, Carriedo SG, Giffard RG. Effect of Bcl-x(L) overexpression on reactive oxygen species, intracellular calcium, and mitochondrial membrane potential following injury in astrocytes. Free Radic Biol Med. 2002;33(4):544-51.
11. Quan Z, Gu J, Dong P, Lu J, Wu X, Wu W, et al. Reactive oxygen species-mediated endoplasmic reticulum stress and mitochondrial dysfunction contribute to cirsimaritin-induced apoptosis in human gallbladder carcinoma GBC-SD cells. Cancer Lett. 2010;295(2):252-9.
12. Arshad M, Ye Z, Gu X, Wong CK, Liu Y, Li D, et al. RNF13, a RING finger protein, mediates endoplasmic reticulum stress-induced apoptosis through the inositol-requiring enzyme (IRE1alpha)/c-Jun NH2-terminal kinase pathway. J Biol Chem. 2013;288(12):8726-36.
13. Patil C, Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol. 2001;13(3):349-55.
14. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999;13(10):1211-33.
15. Moenner M, Pluquet O, Bouchecareilh M, Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 2007;67(22):10631-4.
16. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem. 2002;277(37):34287-94.
17. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11(4):381-9.
18. Vermeulen K, Van Bockstaele DR, Berneman ZN. Apoptosis: mechanisms and relevance in cancer. Ann Hematol. 2005;84(10):627-39.
19. Preston GA, Barrett JC, Biermann JA, Murphy E. Effects of alterations in calcium homeostasis on apoptosis during neoplastic progression. Cancer Res. 1997;57(3):537-42.
20. Zhu LP, Yu XD, Ling S, Brown RA, Kuo TH. Mitochondrial Ca(2+)homeostasis in the regulation of apoptotic and necrotic cell deaths. Cell Calcium. 2000;28(2):107-17.
21. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene. 2008;27(50):6407-18.
22. Wellington K, Jarvis B. Silymarin: a review of its clinical properties in the management of hepatic disorders. BioDrugs. 2001;15(7):465-89.
23. Tyagi A, Agarwal C, Harrison G, Glode LM, Agarwal R. Silibinin causes cell cycle arrest and apoptosis in human bladder transitional cell carcinoma cells by regulating CDKI-CDK-cyclin cascade, and caspase 3 and PARP cleavages. Carcinogenesis. 2004;25(9):1711-20.
24. Agarwal C, Singh RP, Dhanalakshmi S, Tyagi AK, Tecklenburg M, Sclafani RA, et al. Silibinin upregulates the expression of cyclin-dependent kinase inhibitors and causes cell cycle arrest and apoptosis in human colon carcinoma HT-29 cells. Oncogene. 2003;22(51):8271-82.
25. Bousserouel S, Bour G, Kauntz H, Gosse F, Marescaux J, Raul F. Silibinin inhibits tumor growth in a murine orthotopic hepatocarcinoma model and activates the TRAIL apoptotic signaling pathway. Anticancer Res. 2012;32(7):2455-62.
26. Katiyar SK, Roy AM, Baliga MS. Silymarin induces apoptosis primarily through a p53-dependent pathway involving Bcl-2/Bax, cytochrome c release, and caspase activation. Mol Cancer Ther. 2005;4(2):207-16.
27. Liang Q, Wang XP, Chen TS. Resveratrol protects rabbit articular chondrocyte against sodium nitroprusside-induced apoptosis via scavenging ROS. Apoptosis. 2014;19(9):1354-63.
28. Graham KA, Kulawiec M, Owens KM, Li X, Desouki MM, Chandra D, et al. NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther. 2010;10(3):223-31.
29. Dai DF, Rabinovitch PS, Ungvari Z. Mitochondria and cardiovascular aging. Circ Res. 2012;110(8):1109-24.
30. Moungjaroen J, Nimmannit U, Callery PS, Wang L, Azad N, Lipipun V, et al. Reactive oxygen species mediate caspase activation and apoptosis induced by lipoic acid in human lung epithelial cancer cells through Bcl-2 down-regulation. J Pharmacol Exp Ther. 2006;319(3):1062-9.
31. Liu MJ, Wang Z, Li HX, Wu RC, Liu YZ, Wu QY. Mitochondrial dysfunction as an early event in the process of apoptosis induced by woodfordin I in human leukemia K562 cells. Toxicol Appl Pharmacol. 2004;194(2):141-55.
32. Kim SH, Kim KY, Yu SN, Jeon HJ, Jin YR, Lee CM, et al. Silibinin inhibits cell growth and induces apoptosis through cell-cycle arrest in PC-3 prostate cancer cells. J Life Sci. 2011;21:1573-8.
33. Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem. 2006;281(11):7260-70.
34. Malhotra JD, Miao H, Zhang K, Wolfson A, Pennathur S, Pipe SW, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci U S A. 2008;105(47):18525-30.
35. Milhavet O, McMahon HE, Rachidi W, Nishida N, Katamine S, Mange A, et al. Prion infection impairs the cellular response to oxidative stress. Proc Natl Acad Sci U S A. 2000;97(25):13937-42.
36. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer. 2001;1(1):34-45.
37. Mateen S, Tyagi A, Agarwal C, Singh RP, Agarwal R. Silibinin inhibits human nonsmall cell lung cancer cell growth through cell-cycle arrest by modulating expression and function of key cell-cycle regulators. Mol Carcinog. 2010;49(3):247-58.
38. Singh RP, Deep G, Blouin MJ, Pollak MN, Agarwal R. Silibinin suppresses in vivo growth of human prostate carcinoma PC-3 tumor xenograft. Carcinogenesis. 2007;28(12):2567-74.
39. Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 2000;5(5):415-8.
40. Chen K, Kirber MT, Xiao H, Yang Y, Keaney Jr JF. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol. 2008;181(7):1129-39.
41. Kuroda J, Nakagawa K, Yamasaki T, Nakamura K, Takeya R, Kuribayashi F, et al. The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells. 2005;10(12):1139-51.
42. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004;24(4):677-83.
43. Jung JS, Ahn YH, Moon BI, Kim HS. Exogenous C2 Ceramide Suppresses Matrix Metalloproteinase Gene Expression by Inhibiting ROS Production and MAPK Signaling Pathways in PMA-Stimulated Human Astroglioma Cells. Int J Mol Sci. 2016;17(4). doi: 10.3390/ijms17040477.
44. Deniaud A, Sharaf el dein O, Maillier E, Poncet D, Kroemer G, Lemaire C, et al. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene. 2008;27(3):285-99.
45. Faitova J, Krekac D, Hrstka R, Vojtesek B. Endoplasmic reticulum stress and apoptosis. Cell Mol Biol Lett. 2006;11(4):488-505.
46. Cryns V, Yuan J. Proteases to die for. Genes Dev. 1998;12(11):1551-70.