Eriocalyxin B-induced apoptosis in pancreatic adenocarcinoma cells through thiol-containing antioxidant systems and downstream signalling pathways

Current Molecular Medicine

Volumn 14, Issue 5, 2014, Pages 673-689

  Li, L ^a   Yue, G G L ^a   Pu, J X ^b   Sun, H D ^b   Fung, K P ^a   Leung, P C ^a   Han, Q B ^c   Lau, C B S ^a   Leung, P S ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b KUNMING INSTITUTE OF BOTANY   (China)

^c HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

Apoptosis; Eriocalyxin B; Pancreatic cancer; Reactive oxygen species; Thiols

Indexed keywords

DITERPENOID; ERIOCALYXIN B; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; REACTIVE OXYGEN METABOLITE; THIOL DERIVATIVE; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG; ANTIOXIDANT; DITERPENE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; MOUSE; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PANCREAS ADENOCARCINOMA; PROTEIN EXPRESSION; SPECTROPHOTOMETRY; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; METABOLISM; NUDE MOUSE; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL LINE, TUMOR; DITERPENES; GLUTATHIONE; HUMANS; MALE; MICE; MICE, NUDE; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84904048819     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524014666140603102459     Document Type: Article

References (63)

1. Stathis A, Moore MJ. Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 2010; 7(3): 163-72.
2. Benhar M, Engelberg D, Levitzki A. ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep 2002; 3(5): 420-5.
3. Ozben T. Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci 2007; 96(9): 2181-96.
4. Conklin KA. Chemotherapy-associated oxidative stress: impact on chemotherapeutic effectiveness. Integr Cancer Ther 2004; 3(4): 294-300.
5. Gupta SC, Hevia D, Patchva S, et al. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 2012; 16(11): 1295-322.
6. Acharya A, Das I, Chandhok D, Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxid Med Cell Longev 2010; 3(1): 23-34.
7. Mandal PK, Schneider M, Kolle P, et al. Loss of thioredoxin reductase 1 renders tumors highly susceptible to pharmacologic glutathione deprivation. Cancer Res 2010; 70(22): 9505-14.
8. Di Mascio P, Murphy ME, Sies H. Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 1991; 53(1 Suppl): 194S-200S.
9. Scarbrough PM, Mapuskar KA, Mattson DM, et al. Simultaneous inhibition of glutathione- and thioredoxindependent metabolism is necessary to potentiate 17AAGinduced cancer cell killing via oxidative stress. Free Radic Biol Med 2012; 52(2): 436-43.
10. Huber WW, Parzefall W. Thiols and the chemoprevention of cancer. Curr Opin Pharmacol 2007; 7(4): 404-9.
11. Arner ES, Holmgren A. The thioredoxin system in cancer. Semin Cancer Biol 2006; 16(6): 420-6.
12. Mukherjee A, Martin SG. The thioredoxin system: a key target in tumour and endothelial cells. Br J Radiol 2008; 81: S57-68.
13. Powis G, Kirkpatrick DL. Thioredoxin signaling as a target for cancer therapy. Curr Opin Pharmacol 2007; 7(4): 392-7.
14. Mukherjee A, Westwell AD, Bradshaw TD, et al. Cytotoxic and antiangiogenic activity of AW464 (NSC 706704), a novel thioredoxin inhibitor: an in vitro study. Br J Cancer 2005; 92(2): 350-8.
15. Urig S, Becker K. On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin Cancer Biol 2006; 16(6): 452-65.
16. Lu J, Papp LV, Fang J, et al. Inhibition of mammalian thioredoxin reductase by some flavonoids: implications for myricetin and quercetin anticancer activity. Cancer Res 2006; 66(8): 4410-8.
17. Pramanik KC, Srivastava SK. Apoptosis signal-regulating kinase 1-thioredoxin complex dissociation by capsaicin causes pancreatic tumor growth suppression by inducing apoptosis. Antioxid Redox Signal 2012; 17(10): 1417-32.
18. Bartosz G. Reactive oxygen species: destroyers or messengers? Biochem Pharmacol 2009; 77(8): 1303-15.
19. Na HK, Surh YJ. Transcriptional regulation via cysteine thiol modification: a novel molecular strategy for chemoprevention and cytoprotection. Mol Carcinog 2006; 45(6): 368-80.
20. Batra S, Sahu RP, Kandala PK, Srivastava SK. Benzyl isothiocyanate-mediated inhibition of histone deacetylase leads to NF-kappaB turnoff in human pancreatic carcinoma cells. Mol Cancer Ther 2010; 9(6): 1596-608.
21. Lau ST, Lin ZX, Leung PS. Role of reactive oxygen species in brucein D-mediated p38-mitogen-activated protein kinase and nuclear factor-kappaB signalling pathways in human pancreatic adenocarcinoma cells. Br J Cancer 2010; 102(3): 583-93.
22. Jutooru I, Chadalapaka G, Lei P, Safe S. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. J Biol Chem 2010; 285(33): 25332-44.
23. Zhang YW, Jiang XX, Chen QS, et al. Eriocalyxin B induces apoptosis in lymphoma cells through multiple cellular signaling pathways. Exp Hematol 2010; 38(3): 191-201.
24. Leung CH, Grill SP, Lam W, et al. Eriocalyxin B inhibits nuclear factor-kappaB activation by interfering with the binding of both p65 and p50 to the response element in a noncompetitive manner. Mol Pharmacol 2006; 70(6): 1946-55.
25. Wang L, Zhao WL, Yan JS, et al. Eriocalyxin B induces apoptosis of t(8;21) leukemia cells through NF-kappaB and MAPK signaling pathways and triggers degradation of AML1- ETO oncoprotein in a caspase-3-dependent manner. Cell Death Differ 2007; 14(2): 306-17.
26. Li L, Yue GG, Lau CB, et al. Eriocalyxin B induces apoptosis and cell cycle arrest in pancreatic adenocarcinoma cells through caspase- and p53-dependent pathways. Toxicol Appl Pharmacol 2012; 262(1): 80-90.
27. Sun HD, Huang SX, Han QB. Diterpenoids from Isodon species and their biological activities. Nat Prod Rep 2006; 23(5): 673-98.
28. Zhao Y, Niu XM, Qian LP, et al. Synthesis and cytotoxicity of some new eriocalyxin B derivatives. Eur J Med Chem 2007; 42(4): 494-502.
29. Dal Piaz F, Braca A, Belisario MA, De Tommasi N. Thioredoxin system modulation by plant and fungal secondary metabolites. Curr Med Chem 2010; 17(5): 479-94.
30. Han QB, Yu T, Lai F, et al. Quick identification of apoptosis inducer from Isodon eriocalyx by a drug discovery platform composed of analytical high-speed counter-current chromatography and the fluorescence-based caspase-3 biosensor detection. Talanta 2010; 82(4): 1521-7.
31. Wang ZY, Xun YL. New diterpenoid constituents of Rabdosia eriocalyx. Acta Bot Yunnanica 1982; 4: 407-11.
32. Ahamed J, Burg N, Yoshinaga K, et al. In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-beta1. Blood 2008; 112(9): 3650-60.
33. Sun Y, St Clair DK, Xu Y, Crooks PA, St Clair WH. A NADPH oxidase-dependent redox signaling pathway mediates the selective radiosensitization effect of parthenolide in prostate cancer cells. Cancer Res 2010; 70(7): 2880-90.
34. Offen D, Ziv I, Sternin H, Melamed E, Hochman A. Prevention of dopamine-induced cell death by thiol antioxidants: possible implications for treatment of Parkinson's disease. Exp Neurol 1996; 141(1): 32-9.
35. Ludke A, Sharma AK, Bagchi AK, Singal PK. Subcellular basis of vitamin C protection against doxorubicin-induced changes in rat cardiomyocytes. Mol Cell Biochem 2012; 360(1-2): 215-24.
36. Fukumura H, Sato M, Kezuka K, et al. Effect of ascorbic acid on reactive oxygen species production in chemotherapy and hyperthermia in prostate cancer cells. J Physiol Sci 2012; 62(3): 251-7.
37. Ghezzi P. Regulation of protein function by glutathionylation. Free Radic Res 2005; 39(6): 573-80.
38. Kayanoki Y, Fujii J, Islam KN, et al. The protective role of glutathione peroxidase in apoptosis induced by reactive oxygen species. J Biochem 1996; 119(4): 817-22.
39. Sen CK. Cellular thiols and redox-regulated signal transduction. Curr Top Cell Regul 2000; 36: 1-30.
40. Deneke SM. Thiol-based antioxidants. Curr Top Cell Regul 2000; 36: 151-80.
41. Kirshner JR, He S, Balasubramanyam V, et al. Elesclomol induces cancer cell apoptosis through oxidative stress. Mol Cancer Ther 2008; 7(8): 2319-27.
42. Wang J, Yi J. Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther 2008; 7(12): 1875-84.
43. Traber MG, Atkinson J. Vitamin E, antioxidant and nothing more. Free Radic Biol Med 2007; 43(1): 4-15.
44. Padayatty SJ, Katz A, Wang Y, et al. Vitamin C as an antioxidant: evaluation of its role in disease prevention. J Am Coll Nutr 2003; 22(1): 18-35.
45. Cleland WW. Dithiothreitol, a New Protective Reagent for Sh Groups. Biochemistry 1964; 3: 480-2.
46. Lauterburg BH, Corcoran GB, Mitchell JR. Mechanism of action of N-acetylcysteine in the protection against the hepatotoxicity of acetaminophen in rats in vivo. J Clin Invest 1983; 71(4): 980-91.
47. Sandstrom PA, Mannie MD, Buttke TM. Inhibition of activation-induced death in T cell hybridomas by thiol antioxidants: oxidative stress as a mediator of apoptosis. J Leukoc Biol 1994; 55(2): 221-6.
48. Schnelldorfer T, Gansauge S, Gansauge F, et al. Glutathione depletion causes cell growth inhibition and enhanced apoptosis in pancreatic cancer cells. Cancer 2000; 89(7): 1440-7.
49. Franco R, Cidlowski JA. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 2009; 16(10): 1303-14.
50. Manna SK, Kuo MT, Aggarwal BB. Overexpression of gamma-glutamylcysteine synthetase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappa B and activator protein-1. Oncogene 1999; 18(30): 4371-82.
51. Kim SJ, Miyoshi Y, Taguchi T, et al. High thioredoxin expression is associated with resistance to docetaxel in primary breast cancer. Clin Cancer Res 2005; 11(23): 8425-30.
52. Miyazaki K, Noda N, Okada S, et al. Elevated serum level of thioredoxin in patients with hepatocellular carcinoma. Biotherapy 1998; 11(4): 277-88.
53. Powis G, Montfort WR. Properties and biological activities of thioredoxins. Annu Rev Biophys Biomol Struct 2001; 30:421-55.
54. Arnold NB, Ketterer K, Kleeff J, et al. Thioredoxin is downstream of Smad7 in a pathway that promotes growth and suppresses cisplatin-induced apoptosis in pancreatic cancer. Cancer Res 2004; 64(10): 3599-606.
55. Grek CL, Tew KD. Redox metabolism and malignancy. Curr Opin Pharmacol 2010; 10(4): 362-8.
56. Han H, Bearss DJ, Browne LW, et al. Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res 2002; 62(10): 2890-6.
57. Hori M, Nishida K. Oxidative stress and left ventricular remodelling after myocardial infarction. Cardiovasc Res 2009; 81(3): 457-64.
58. Saitoh M, Nishitoh H, Fujii M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998; 17(9): 2596-606.
59. Kwon SJ, Song JJ, Lee YJ. Signal pathway of hypoxiainducible factor-1alpha phosphorylation and its interaction with von Hippel-Lindau tumor suppressor protein during ischemia in MiaPaCa-2 pancreatic cancer cells. Clin Cancer Res 2005; 11(21): 7607-13.
60. Carlson BA, Yoo MH, Tobe R, et al. Thioredoxin reductase 1 protects against chemically induced hepatocarcinogenesis via control of cellular redox homeostasis. Carcinogenesis 2012; 33(9): 1806-13.
61. Simons AL, Parsons AD, Foster KA, et al. Inhibition of glutathione and thioredoxin metabolism enhances sensitivity to perifosine in head and neck cancer cells. J Oncol 2009; 519563.
62. Pramanik KC, Boreddy SR, Srivastava SK. Role of mitochondrial electron transport chain complexes in capsaicin mediated oxidative stress leading to apoptosis in pancreatic cancer cells. PLoS One 2011; 6(5): e20151.
63. Hirota K, Murata M, Sachi Y, et al. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NFkappaB. J Biol Chem 1999; 274(39): 27891-7.