The role of the catecholic and the electrophilic moieties of caffeic acid in Nrf2/Keap1 pathway activation in ovarian carcinoma cell lines

Redox Biology

Volumn 4, Issue , 2015, Pages 48-59

  Sirota, R ^a   Gibson, D ^a   Kohen, R ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Caffeic acid; Cisplatin; Coffee; Nrf2; Polyphenols

Indexed keywords

CAFFEIC ACID; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE P1; HEME OXYGENASE 1; HYDROGEN PEROXIDE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2; TRIGONELLINE; ANTIOXIDANT; CAFFEIC ACID DERIVATIVE; CATECHOL; CATECHOL DERIVATIVE; COFFEE; KEAP1 PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; POLYPHENOL; SIGNAL PEPTIDE;

ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER COMBINATION CHEMOTHERAPY; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; ELECTROPHILICITY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; MONOTHERAPY; NUCLEOPHILICITY; OVARY CARCINOMA; OXIDATIVE STRESS; PHASE 2 CLINICAL TRIAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; BIOSYNTHESIS; CHEMISTRY; COFFEE; DRUG EFFECTS; METABOLISM; OVARIAN NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTIOXIDANTS; CAFFEIC ACIDS; CATECHOLS; CELL LINE, TUMOR; COFFEE; FEMALE; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; NF-E2-RELATED FACTOR 2; OVARIAN NEOPLASMS; OXIDATIVE STRESS; POLYPHENOLS; SIGNAL TRANSDUCTION;

EID: 84917710616     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2014.11.012     Document Type: Article

References (53)

1. Radoï L., Paget-Bailly S., Menvielle G., Cyr D., Schmaus A., Carton M., et al. Tea and coffee consumption and risk of oral cavity cancer: results of a large population-based case-control study, the ICARE study. Cancer Epidemiology 2013, 37(3):284-289. http://www.ncbi.nlm.nih.gov/pubmed/23453554, 10.1016/j.canep.2013.02.001.
2. Sang L.X., Chang B., Li X.H., Jiang M. Consumption of coffee associated with reduced risk of liver cancer: a meta-analysis. BMC Gastroenterology 2013, 13:34. http://www.ncbi.nlm.nih.gov/pubmed/23433483, 10.1186/1471-230X-13-34.
3. Tian C., Wang W., Hong Z., Zhang X. Coffee consumption and risk of colorectal cancer: a dose-response analysis of observational studies. Cancer Causes Control 2013, 24(6):1265-1268. http://www.ncbi.nlm.nih.gov/pubmed/23546611, 10.1007/s10552-013-0200-6.
4. Wilson K.M., Bälter K., Möller E., Adami H.O., Andrén O., Andersson S.O., et al. Coffee and risk of prostate cancer incidence and mortality in the cancer of the prostate in Sweden Study. Cancer Causes & Control 2013, 24(8):1575-1581. http://www.ncbi.nlm.nih.gov/pubmed/23702886, 10.1007/s10552-013-0234-9.
5. Higdon J.V., Frei B. Coffee and health: a review of recent human research. Critical Reviews in Food Science and Nutrition 2006, 46(2):101-123. http://www.ncbi.nlm.nih.gov/pubmed/16507475, 10.1080/10408390500400009.
6. Pannala A.S., Rice-Evans C.A., Halliwell B., Singh S. Inhibition of peroxynitrite-mediated tyrosine nitration by catechin polyphenols. Biochemical and Biophysical Research Communications 1997, 232(1):164-168. http://www.ncbi.nlm.nih.gov/pubmed/9125123, 10.1006/bbrc.1997.6254.
7. Rice-Evans C.A., Miller N.J. Antioxidant activities of flavonoids as bioactive components of food. Biochemical Society Transactions 1996, 24(3):790-795.
8. Brown J.C., Jiang X. Activities of muscadine grape skin and polyphenolic constituents against Helicobacter pylori. Journal of Applied Microbiology 2013, 114(4):982-991. http://www.ncbi.nlm.nih.gov/pubmed/23294280, 10.1111/jam.12129.
9. Rashed K.N., Butnariu M. Isolation and antimicrobial and antioxidant evaluation of bio-active compounds from Eriobotrya japonica stems. Advanced Pharmaceutical Bulletin 2014, 4(1):75-81. http://www.ncbi.nlm.nih.gov/pubmed/24409413, 10.5681/apb.2014.012.
10. Chao C.Y., Mong M.C., Chan K.C., Yin M.C. Anti-glycative and anti-inflammatory effects of caffeic acid and ellagic acid in kidney of diabetic mice. Molecular Nutrition & Food Research 2010, 54(3):388-395. http://www.ncbi.nlm.nih.gov/pubmed/19885845, 10.1002/mnfr.200900087.
11. Hwang S.J., Kim Y.W., Park Y., Lee H.J., Kim K.W. Anti-inflammatory effects of chlorogenic acid in lipopolysaccharide-stimulated RAW 264.7 cells. Inflammation Research 2014, 63(1):81-90. http://www.ncbi.nlm.nih.gov/pubmed/24127072, 10.1007/s00011-013-0674-4.
12. Darvesh A.S., Bishayee A. Chemopreventive and therapeutic potential of tea polyphenols in hepatocellular cancer. Nutrition and Cancer 2013, 65(3):329-344. http://www.ncbi.nlm.nih.gov/pubmed/23530632, 10.1080/01635581.2013.767367.
13. Malerba S., Galeone C., Pelucchi C., Turati F., Hashibe M., La Vecchia C., et al. A meta-analysis of coffee and tea consumption and the risk of glioma in adults. Cancer Causes & Control 2013, 24(2):267-276. http://www.ncbi.nlm.nih.gov/pubmed/23247638, 10.1007/s10552-012-0126-4.
14. Sirota R., Gorelik S., Harris R., Kohen R., Kanner J. Coffee polyphenols protect human plasma from postprandial carbonyl modifications. Molecular Nutrition & Food Research 2013, 57(5):916-919. http://www.ncbi.nlm.nih.gov/pubmed/23322503, 10.1002/mnfr.201200557.
15. Erk T., Hauser J., Williamson G., Renouf M., Steiling H., Dionisi F., et al. Structure- and dose-absorption relationships of coffee polyphenols. Biofactors 2014, 40(1):103-112. http://www.ncbi.nlm.nih.gov/pubmed/23553742, 10.1002/biof.1101.
16. Manach C., Scalbert A., Morand C., Rémésy C., Jiménez L. Polyphenols: food sources and bioavailability. American Journal of Clinical Nutrition 2004, 79(5):727-747.
17. Vitaglione P., Fogliano V., Pellegrini N. Coffee, colon function and colorectal cancer. Food & Function 2012, 3(9):916-922. http://www.ncbi.nlm.nih.gov/pubmed/22627289, 10.1039/c2fo30037k.
18. Han S.G., Han S.S., Toborek M., Hennig B. EGCG protects endothelial cells against PCB 126-induced inflammation through inhibition of AhR and induction of Nrf2-regulated genes. Toxicology and Applied Pharmacology 2012, 261(2):181-188. http://www.ncbi.nlm.nih.gov/pubmed/22521609, 10.1016/j.taap.2012.03.024.
19. Hao E., Lang F., Chen Y., Zhang H., Cong X., Shen X., et al. Resveratrol alleviates endotoxin-induced myocardial toxicity via the Nrf2 transcription factor. PLOS One 2013, 8(7):e69452. http://www.ncbi.nlm.nih.gov/pubmed/23894482, 10.1371/journal.pone.0069452.
20. Zhao R., Yang B., Wang L., Xue P., Deng B., Zhang G., et al. Curcumin protects human keratinocytes against inorganic arsenite-induced acute cytotoxicity through an NRF2-dependent mechanism. Oxidative Medicine and Cellular Longevity 2013, 2013:412576. http://www.ncbi.nlm.nih.gov/pubmed/23710286, 10.1155/2013/412576.
21. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metabolism Reviews 2006, 38(4):769-789. http://www.ncbi.nlm.nih.gov/pubmed/17145701, 10.1080/03602530600971974.
22. Bryan H.K., Olayanju A., Goldring C.E., Park B.K. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochemical Pharmacology 2013, 85(6):705-717. http://www.ncbi.nlm.nih.gov/pubmed/23219527, 10.1016/j.bcp.2012.11.016.
23. Zhang M., An C., Gao Y., Leak R.K., Chen J., Zhang F. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Progress in Neurobiology 2013, 100:30-47. http://www.ncbi.nlm.nih.gov/pubmed/23025925, 10.1016/j.pneurobio.2012.09.003.
24. Acharya A., Das I., Chandhok D., Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxidative Medicine and Cellular Longevity 2010, 3(1):23-34. http://www.ncbi.nlm.nih.gov/pubmed/20716925, 10.4161/oxim.3.1.10095.
25. Wang X.J., Sun Z., Villeneuve N.F., Zhang S., Zhao F., Li Y., et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008, 29(6):1235-1243. http://www.ncbi.nlm.nih.gov/pubmed/18413364, 10.1093/carcin/bgn095.
26. Pasello M., Michelacci F., Scionti I., Hattinger C.M., Zuntini M., Caccuri A.M., et al. Overcoming glutathione S-transferase P1-related cisplatin resistance in osteosarcoma. Cancer Research 2008, 68(16):6661-6668. http://www.ncbi.nlm.nih.gov/pubmed/18701490, 10.1158/0008-5472.CAN-07-5840.
27. Dourado D.F., Fernandes P.A., Ramos M.J. Glutathione transferase classes alpha, pi, and mu: GSH activation mechanism. Journal of Physical Chemistry B 2010, 114(40):12972-12980. http://www.ncbi.nlm.nih.gov/pubmed/20853826, 10.1021/jp1053875.
28. Lu D., Shi H.C., Wang Z.X., Gu X.W., Zeng Y.J. Multidrug resistance-associated biomarkers PGP, GST-pi, Topo-II and LRP as prognostic factors in primary ovarian carcinoma. British Journal of Biomedical Science 2011, 68(2):69-74.
29. Schumaker L., Nikitakis N., Goloubeva O., Tan M., Taylor R., Cullen K.J. Elevated expression of glutathione S-transferase pi and p53 confers poor prognosis in head and neck cancer patients treated with chemoradiotherapy but not radiotherapy alone. Clinical Cancer Research 2008, 14(18):5877-5883. http://www.ncbi.nlm.nih.gov/pubmed/18794100, 10.1158/1078-0432.CCR-08-0998.
30. Halliwell B. Are polyphenols antioxidants or pro-oxidants? What do we learn from cell culture and in vivo studies?. Archives of Biochemistry and Biophysics 2008, 476(2):107-112. http://www.ncbi.nlm.nih.gov/pubmed/18284912, 10.1016/j.abb.2008.01.028.
31. Pecorelli A., Bocci V., Acquaviva A., Belmonte G., Gardi C., Virgili F., et al. NRF2 activation is involved in ozonated human serum upregulation of HO-1 in endothelial cells. Toxicology and Applied Pharmacology 2013, 267(1):30-40. http://www.ncbi.nlm.nih.gov/pubmed/23253326, 10.1016/j.taap.2012.12.001.
32. Soroka Y., Sagi A., Khalaila I., Abdu U., Milner Y. Changes in protein kinase C during vitellogenesis in the crayfish Cherax quadricarinatus -possible activation by methyl farnesoate. General and Comparative Endocrinology 2000, 118(2):200-208. http://www.ncbi.nlm.nih.gov/pubmed/10890562, 10.1006/gcen.2000.7471.
33. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254. http://www.ncbi.nlm.nih.gov/pubmed/942051, 10.1016/0003-2697(76)90527-3.
34. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 1974, 249(22):7130-7139.
35. Beutler E., Duron O., Kelly B.M. Improved method for the determination of blood glutathione. Journal of Laboratory and Clinical Medicine 1963, 61:882-888. http://www.ncbi.nlm.nih.gov/pubmed/13967893.
36. White C.C., Viernes H., Krejsa C.M., Botta D., Kavanagh T.J. Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Analytical Biochemistry 2003, 318(2):175-180. 10.1016/S0003-2697(03)00143-X.
37. Portugal-Cohen M., Kohen R. Exposure of human keratinocytes to ischemia, hyperglycemia and their combination induces oxidative stress via the enzymes inducible nitric oxide synthase and xanthine oxidase. Journal of Dermatological Science 2009, 55(2):82-90. http://www.ncbi.nlm.nih.gov/pubmed/19539448, 10.1016/j.jdermsci.2009.05.006.
38. Arlt A., Sebens S., Krebs S., Geismann C., Grossmann M., Kruse M.L., et al. Inhibition of the Nrf2 transcription factor by the alkaloid trigonelline renders pancreatic cancer cells more susceptible to apoptosis through decreased proteasomal gene expression and proteasome activity. Oncogene 2013, 32(40):4825-4835. http://www.ncbi.nlm.nih.gov/pubmed/23108405, 10.1038/onc.2012.493.
39. Wang G., Gong Y., Burczynski F.J., Hasinoff B.B. Cell lysis with dimethyl sulphoxide produces stable homogeneous solutions in the dichlorofluorescein oxidative stress assay. Free Radical Research 2008, 42(5):435-441. http://www.ncbi.nlm.nih.gov/pubmed/18484276, 10.1080/10715760802074462.
40. Halliwell B. Cell culture, oxidative stress, and antioxidants: avoiding pitfalls. Biomedical Journal 2014, 37(3):99-105. http://www.ncbi.nlm.nih.gov/pubmed/24923566, 10.4103/2319-4170.128725.
41. Fadel O., El Kirat K., Morandat S. The natural antioxidant rosmarinic acid spontaneously penetrates membranes to inhibit lipid peroxidation in situ. Biochimica et Biophysica Acta 2011, 1808(12):2973-2980. http://www.ncbi.nlm.nih.gov/pubmed/21864504, 10.1016/j.bbamem.2011.08.011.
42. Sato Y., Itagaki S., Kurokawa T., Ogura J., Kobayashi M., Hirano T., et al. In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. International Journal of Pharmaceutics 2011, 403(1-2):136-138. http://www.ncbi.nlm.nih.gov/pubmed/20933071, 10.1016/j.ijpharm.2010.09.035.
43. Calabrese V., Cornelius C., Dinkova-Kostova A.T., Calabrese E.J., Mattson M.P. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxidants & Redox Signaling 2010, 13(11):1763-1811. http://www.ncbi.nlm.nih.gov/pubmed/20446769, 10.1089/ars.2009.3074.
44. Bao L.J., Jaramillo M.C., Zhang Z.B., Zheng Y.X., Yao M., Zhang D.D., et al. Nrf2 induces cisplatin resistance through activation of autophagy in ovarian carcinoma. International Journal of Clinical andExperimental Pathology 2014, 7(4):1502-1513.
45. Lister A., Nedjadi T., Kitteringham N.R., Campbell F., Costello E., Lloyd B., et al. Nrf2 is overexpressed in pancreatic cancer: implications for cell proliferation and therapy. Molecular Cancer 2011, 10:37. http://www.ncbi.nlm.nih.gov/pubmed/21489257, 10.1186/1476-4598-10-37.
46. Peklak-Scott C., Smitherman P.K., Townsend A.J., Morrow C.S. Role of glutathione S-transferase P1-1 in the cellular detoxification of cisplatin. Molecular Cancer Therapeutics 2008, 7(10):3247-3255. http://www.ncbi.nlm.nih.gov/pubmed/18852128, 10.1158/1535-7163.MCT-08-0250.
47. Rolland D., Raharijaona M., Barbarat A., Houlgatte R., Thieblemont C. Inhibition of GST-pi nuclear transfer increases mantle cell lymphoma sensitivity to cisplatin, cytarabine, gemcitabine, bortezomib and doxorubicin. Anticancer Research 2010, 30(10):3951-3957.
48. Tew K.D., Townsend D.M. Regulatory functions of glutathione S-transferase P1-1 unrelated to detoxification. Drug Metabolism Reviews 2011, 43(2):179-193. http://www.ncbi.nlm.nih.gov/pubmed/21351850, 10.3109/03602532.2011.552912.
49. Hirano G., Izumi H., Yasuniwa Y., Shimajiri S., Ke-Yong W., Sasagiri Y., et al. Involvement of riboflavin kinase expression in cellular sensitivity against cisplatin. International Journal of Oncology 2011, 38(4):893-902. http://www.ncbi.nlm.nih.gov/pubmed/21308351, 10.3892/ijo.2011.938.
50. Baek S.M., Kwon C.H., Kim J.H., Woo J.S., Jung J.S., Kim Y.K. Differential roles of hydrogen peroxide and hydroxyl radical in cisplatin-induced cell death in renal proximal tubular epithelial cells. Journal of Laboratory and Clinical Medicine 2003, 142(3):178-186. http://www.ncbi.nlm.nih.gov/pubmed/14532906, 10.1016/S0022-2143(03)00111-2.
51. Kilic U., Kilic E., Tuzcu Z., Tuzcu M., Ozercan I.H., Yilmaz O., et al. Melatonin suppresses cisplatin-induced nephrotoxicity via activation of Nrf-2/HO-1 pathway. Nutrition & Metabolism 2013, 10(1):7. http://www.ncbi.nlm.nih.gov/pubmed/23311701, 10.1186/1743-7075-10-7.
52. So H., Kim H., Kim Y., Kim E., Pae H.O., Chung H.T., et al. Evidence that cisplatin-induced auditory damage is attenuated by downregulation of pro-inflammatory cytokines via Nrf2/HO-1. Journal of the Association forResearch in Otolaryngology 2008, 9(3):290-306. http://www.ncbi.nlm.nih.gov/pubmed/18584244, 10.1007/s10162-008-0126-y.
53. Ploemen J.H., van Ommen B., de Haan A., Schefferlie J.G., van Bladeren P.J. In vitro and in vivo reversible and irreversible inhibition of rat glutathione S-transferase isoenzymes by caffeic acid and its 2-S-glutathionyl conjugate. Food and Chemical Toxicology 1993, 31(7):475-482. http://www.ncbi.nlm.nih.gov/pubmed/8340025, 10.1016/0278-6915(93)90106-9.