Direct and indirect inactivation of tumor cell protective catalase by salicylic acid and anthocyanidins reactivates intercellular ROS signaling and allows for synergistic effects

Carcinogenesis

Volumn 36, Issue 3, 2014, Pages 400-411

  Scheit, Katrin ^a,b   Bauer, Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Klinik Immenstadt ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIDIN DERIVATIVE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; CASPASE 3; CASPASE 8; CATALASE; CYANIDIN; DELPHINIDIN; HYDROGEN PEROXIDE; MALVIDIN 3 O GALACTOSIDE; MALVIDIN CHLORIDE; MEMBRANE ASSOCIATED CATALASE; N(G) NITROARGININE METHYL ESTER; PELARGONIN; PEONIDIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SALICYLIC ACID; SINGLET OXYGEN; UNCLASSIFIED DRUG; ANTHOCYANIN; PEROXYNITROUS ACID;

ADULT; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER RESISTANCE; CARCINOMA CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME REACTIVATION; EWING SARCOMA CELL LINE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CARCINOMA; CELL MEMBRANE; DRUG EFFECTS; ENZYME ACTIVATION; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTHOCYANINS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CATALASE; CELL LINE, TUMOR; CELL MEMBRANE; DRUG SYNERGISM; ENZYME ACTIVATION; HUMANS; PEROXYNITROUS ACID; REACTIVE OXYGEN SPECIES; SALICYLIC ACID; SIGNAL TRANSDUCTION; SINGLET OXYGEN;

EID: 84924479014     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgv010     Document Type: Article

References (51)

1. Bauer, G. (2012) Tumor cell-protective catalase as a novel target for rational therapeutic approaches based on specific intercellular ROS signaling. Anticancer Res., 32, 2599-2624.
2. Feig, D.I. et al. (1994) Reactive oxygen species in tumorigenesis. Cancer Res., 54(7 suppl.), 1890-1894.
3. Storz, P. (2005) Reactive oxygen species in tumor progression. Front. Biosci., 10, 1881-1896.
4. Cerutti, P.A. (1995) Prooxidant states and tumor promotion. Free Radic. Biol. Med., 18, 775-794.
5. Irani, K. et al. (1997) Mitogenic signaling mediated by oxidants in Rastransformed fibroblasts. Science, 275, 1649-1652.
6. Suh, Y.A. et al. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature, 401, 79-82.
7. Herdener, M. et al. (2000) Target cell-derived superoxide anions cause efficiency and selectivity of intercellular induction of apoptosis. Free Radic. Biol. Med., 29, 1260-1271.
8. Heigold, S. et al. (2002) Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts. Carcinogenesis, 23, 929-941.
9. Deichman, G.J. et al. (1998) Cell transforming genes and tumor progression:in vivo unified secondary phenotypic cell changes. Int. J. Cancer, 75, 277-283.
10. Deichman, G.I. (2002) Early phenotypic changes of in vitro transformed cells during in vivo progression: possible role of the host innate immunity. Semin. Cancer Biol., 12, 317-326.
11. Bechtel, W. et al. (2009) Catalase protects tumor cells from apoptosis induction by intercellular ROS signaling. Anticancer Res., 29, 4541-4557.
12. Heinzelmann, S. et al. (2010) Multiple protective functions of catalase against intercellular apoptosis-inducing ROS signaling of human tumor cells. Biol. Chem., 391, 675-693.
13. Brunelli, L. et al. (2001) Modulation of catalase peroxidatic and catalatic activity by nitric oxide. Free Radic. Biol. Med., 30, 709-714.
14. Borovic, S. et al. (2007) Differential sensitivity to 4-hydroxynonenal for normal and malignant mesenchymal cells. Redox Rep., 12, 50-54.
15. Durner, J. et al. (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci., 2, 266-274.
16. Elwood, P.C. et al. (2009) Aspirin, salicylates, and cancer. Lancet, 373, 1301-1309.
17. Aas, A.T. et al. (1995) Growth inhibition of rat glioma cells in vitro and in vivo by aspirin. J. Neurooncol., 24, 171-180.
18. Bellosillo, B. et al. (1998) Aspirin and salicylate induce apoptosis and activation of caspases in B-cell chronic lymphocytic leukemia cells. Blood, 92, 1406-1414.
19. Klampfer, L. et al. (1999) Sodium salicylate activates caspases and induces apoptosis of myeloid leukemia cell lines. Blood, 93, 2386-2394.
20. Chung, Y.M. et al. (2003) Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylateinduced apoptosis. Free Radic. Biol. Med., 34, 434-442.
21. Battaglia, V. et al. (2005) Oxidative stress is responsible for mitochondrial permeability transition induction by salicylate in liver mitochondria. J. Biol. Chem., 280, 33864-33872.
22. Elder, D.J.E. et al. (1996) Differential growth inhibition by the aspirin metabolite salicylate in human colorectal tumor cell lines: enhanced apoptosis in carcinoma and in vitro-transformed adenoma relative to adenoma relative to adenoma cell lines. Cancer Res., 56, 2273-2276.
23. Hou, D.X. et al. (2004) Molecular mechanisms behind the chemopreventive effects of anthocyanidins. J. Biomed. Biotechnol., 2004, 321-325.
24. Chang, Y.C. et al. (2005) Hibiscus anthocyanins rich extract-induced apoptotic cell death in human promyelocytic leukemia cells. Toxicol. Appl. Pharmacol., 205, 201-212.
25. Chen, P.N. et al. (2005) Cyanidin 3-glucoside and peonidin 3-glucoside inhibit tumor cell growth and induce apoptosis in vitro and suppress tumor growth in vivo. Nutr. Cancer, 53, 232-243.
26. Shih, P.H. et al. (2005) Effects of anthocyanidin on the inhibition of proliferation and induction of apoptosis in human gastric adenocarcinoma cells. Food Chem. Toxicol., 43, 1557-1566.
27. Feng, R. et al. (2007) Cyanidin-3-rutinoside, a natural polyphenol antioxidant, selectively kills leukemic cells by induction of oxidative stress. J. Biol. Chem., 282, 13468-13476.
28. Reddivari, L. et al. (2007) Anthocyanin fraction from potato extracts is cytotoxic to prostate cancer cells through activation of caspasedependent and caspase-independent pathways. Carcinogenesis, 28, 2227-2235.
29. Wang, L.S. et al. (2008) Anthocyanins and their role in cancer prevention. Cancer Lett., 269, 281-290.
30. Rao, C.V. et al. (1995) Chemoprevention of colon carcinogenesis by sulindac, a nonsteroidal anti-inflammatory agent. Cancer Res., 55, 1464-1472.
31. Giardiello, F.M. et al. (1995) The role of nonsteroidal anti-inflammatory drugs in colorectal cancer prevention. Eur. J. Cancer, 31A, 1071-1076.
32. Hanif, R. et al. (1996) Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem. Pharmacol., 52, 237-245.
33. Rigas, B. et al. (2000) Is inhibition of cyclooxygenase required for the chemopreventive effect of NSAIDs in colon cancer? A model reconciling the current contradiction. Med. Hypotheses, 54, 210-215.
34. Durner, J. et al. (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J. Biol. Chem., 271, 28492-28501.
35. Gardner, P.R. et al. (2001) Dioxygen-dependent metabolism of nitric oxide in mammalian cells. Free Radic. Biol. Med., 31, 191-204.
36. Hallstrom, C.K. et al. (2004) Nitric oxide metabolism in mammalian cells: substrate and inhibitor profiles of a NADPH-cytochrome P450 oxidoreductase-coupled microsomal nitric oxide dioxygenase. Free Radic. Biol. Med., 37, 216-228.
37. Di Mascio, P. et al. (1994) Singlet molecular oxygen production in the reaction of peroxynitrite with hydrogen peroxide. FEBS Lett., 355, 287-289.
38. Davison, A.J. et al. (1986) Mechanism of the inhibition of catalase by ascorbate. J. Biol. Chem., 261, 1193-1200.
39. Jones, D.P. et al. (1981) Conversion of catalase to the secondary catalase- peroxide complex (compound II) by alpha-methyldopa. Mol. Pharmacol., 20, 159-164.
40. Thun, M.J. et al. (1991) Aspirin use and reduced risk of fatal colon cancer. N. Engl. J. Med., 325, 1593-1596.
41. Harris, R.E. et al. (1996) Nonsteroidal antiinflammatory drugs and breast cancer. Epidemiology, 7, 203-205.
42. Rothwell, P.M. et al. (2011) Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet, 377, 31-41.
43. Rothwell, P.M. et al. (2012) Short-term effects of daily aspirin on cancer incidence, mortality, and non-vascular death: analysis of the time course of risks and benefits in 51 randomised controlled trials. Lancet, 379, 1602-1612.
44. Sagone, A.L. Jr et al. (1987) Oxidation of salicylates by stimulated granulocytes:evidence that these drugs act as free radical scavengers in biological systems. J. Immunol., 138, 2177-2183.
45. Brown, G.C. (1995) Reversible binding and inhibition of catalase by nitric oxide. Eur. J. Biochem., 232, 188-191.
46. Zhuang, S. et al. (2001) Protein kinase C inhibits singlet oxygeninduced apoptosis by decreasing caspase-8 activation. Oncogene, 20, 6764-6776.
47. Suzuki, Y. et al. (1998) Rapid and specific reactive oxygen species generation via NADPH oxidase activation during Fas-mediated apoptosis. FEBS Lett., 425, 209-212.
48. Reinehr, R. et al. (2005) Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J. Biol. Chem., 280, 27179-27194.
49. Selleri, C. et al. (1997) Induction of nitric oxide synthase is involved in the mechanism of Fas-mediated apoptosis in haemopoietic cells. Br. J. Haematol., 99, 481-489.
50. Escobar, J.A. et al. (1996) Sod and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radic. Biol. Med., 20, 285-290.
51. Girotti, A.W. (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J. Lipid Res., 39, 1529-1542.