Mechanistic evaluation of the signaling events regulating curcumin-mediated chemosensitization of breast cancer cells to 5-fluorouracil

Cell Death and Disease

Volumn 4, Issue 2, 2013, Pages

  Vinod, B S ^a   Antony, J ^a   Nair, H H ^a   Puliyappadamba, V T ^a   Saikia, M ^a   Shyam Narayanan, S ^a   Bevin, A ^a   John Anto, R ^a  

^a RAJIV GANDHI CENTRE FOR BIOTECHNOLOGY   (India)

Author keywords

5 FU; Chemosensitization; Curcumin; NF B; Synergistic effect; Thymidylate synthase

Indexed keywords

CELL RECEPTOR; CURCUMIN; FLUOROURACIL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; THYMIDYLATE SYNTHASE;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CHEMOSENSITIZATION; CLINICAL EVALUATION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG RESISTANCE; ENZYME INDUCTION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANNEXIN A5; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CASPASES; CELL LINE, TUMOR; CURCUMIN; DNA FRAGMENTATION; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; FLUOROURACIL; HUMANS; MCF-7 CELLS; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THYMIDYLATE SYNTHASE; UP-REGULATION;

EID: 84875988418     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.26     Document Type: Article

References (53)

1. Aggarwal BB, Shishodia S, Takada Y, Banerjee S, Newman RA, Bueso-Ramos CE et al. Curcumin suppresses the paclitaxel-induced nuclear factor-kappaB pathway in breast cancer cells and inhibits lung metastasis of human breast cancer in nude mice. Clin Cancer Res 2005; 11: 7490-7498.
2. Sreekanth CN, Bava SV, Sreekumar E, Anto RJ. Molecular evidences for the chemosensitizing efficacy of liposomal curcumin in paclitaxel chemotherapy in mouse models of cervical cancer. Oncogene 2011; 30: 3139-3152.
3. Vinod BS, Maliekal TT, Anto RJ. Phytochemicals as chemosensitizers: from molecular mechanism to clinical significance. Antioxid Redox Signal 2012; e-pub ahead of print 9 October 2012; doi:10.1089/ars.2012.4573.
4. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 2003; 3: 330-338.
5. Chu E, Callender MA, Farrell MP, Schmitz JC. Thymidylate synthase inhibitors as anticancer agents: from bench to bedside. Cancer Chemother Pharmacol 2003; 52(Suppl 1): S80-S89.
6. Ghoshal K, Jacob ST. An alternative molecular mechanism of action of 5-fluorouracil, a potent anticancer drug. Biochem Pharmacol 1997; 53: 1569-1575.
7. Major PP, Egan E, Herrick D, Kufe DW. 5-Fluorouracil incorporation in DNA of human breast carcinoma cells. Cancer Res 1982; 42: 3005-3009.
8. Cho IJ, Chang HJ, Lee KE, Won HS, Choi MY, Nam EM et al. A case of Wernicke's encephalopathy following fluorouracil-based chemotherapy. J Korean Med Sci 2009; 24: 747-750.
9. Chu E, Koeller DM, Johnston PG, Zinn S, Allegra CJ. Regulation of thymidylate synthase in human colon cancer cells treated with 5-fluorouracil and interferon-gamma. Mol Pharmacol 1993; 43: 527-533.
10. Swain SM, Lippman ME, Egan EF, Drake JC, Steinberg SM, Allegra CJ. Fluorouracil and high-dose leucovorin in previously treated patients with metastatic breast cancer. J Clin Oncol 1989; 7: 890-899.
11. Lenz HJ, Hayashi K, Salonga D, Danenberg KD, Danenberg PV, Metzger R et al. P53 point mutations and thymidylate synthase messenger RNA levels in disseminated colorectal cancer: an analysis of response and survival. Clin Cancer Res 1998; 4: 1243-1250.
12. Rahman L, Voeller D, Rahman M, Lipkowitz S, Allegra C, Barrett JC et al. Thymidylate synthase as an oncogene: a novel role for an essential DNA synthesis enzyme. Cancer Cell 2004; 5: 341-351.
13. Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, Kalyanaraman B. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem J 2002; 367: 729-740.
14. Nakanishi C, Toi M. Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005; 5: 297-309.
15. Kodach LL, Bos CL, Duran N, Peppelenbosch MP, Ferreira CV, Hardwick JC. Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Aktmediated signal transduction in human colorectal cancer cells. Carcinogenesis 2006; 27: 508-516.
16. Wang W, McLeod HL, Cassidy J. Disulfiram-mediated inhibition of NF-kappaB activity enhances cytotoxicity of 5-fluorouracil in human colorectal cancer cell lines. Int J Cancer 2003; 104: 504-511.
17. Wu H, Li W, Wang T, Shu Y, Liu P. Paeoniflorin suppress NF-kappaB activation through modulation of I kappaB alpha and enhances 5-fluorouracil-induced apoptosis in human gastric carcinoma cells. Biomed Pharmacother 2008; 62: 659-666.
18. Jin W, Wu L, Liang K, Liu B, Lu Y, Fan Z. Roles of the PI-3K and MEK pathways in Rasmediated chemoresistance in breast cancer cells. Br J Cancer 2003; 89: 185-191.
19. Perez-Tenorio G, Stal O. Activation of AKT/PKB in breast cancer predicts a worse outcome among endocrine treated patients. Br J Cancer 2002; 86: 540-545.
20. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001; 410: 37-40.
21. Kunnumakkara AB, Anand P, Aggarwal BB. Curcumin inhibits proliferation, invasion, angiogenesis and metastasis of different cancers through interaction with multiple cell signaling proteins. Cancer Lett 2008; 269: 199-225.
22. Kanai M, Yoshimura K, Asada M, Imaizumi A, Suzuki C, Matsumoto S et al. A phase I/II study of gemcitabine-based chemotherapy plus curcumin for patients with gemcitabineresistant pancreatic cancer. Cancer Chemother Pharmacol 2011; 68: 157-164.
23. Bava SV, Puliappadamba VT, Deepti A, Nair A, Karunagaran D, Anto RJ. Sensitization of taxol-induced apoptosis by curcumin involves down-regulation of nuclear factor-kappaB and the serine/threonine kinase Akt and is independent of tubulin polymerization. J Biol Chem 2005; 280: 6301-6308.
24. Li Y, Revalde JL, Reid G, Paxton JW. Modulatory effects of curcumin on multi-drug resistance-associated protein 5 in pancreatic cancer cells. Cancer Chemother Pharmacol 2011; 68: 603-610.
25. Patel BB, Majumdar AP. Synergistic role of curcumin with current therapeutics in colorectal cancer: minireview. Nutr Cancer 2009; 61: 842-846.
26. Tian F, Fan T, Zhang Y, Jiang Y, Zhang X. Curcumin potentiates the antitumor effects of 5- FU in treatment of esophageal squamous carcinoma cells through downregulating the activation of NF-kappaB signaling pathway in vitro and in vivo. Acta Biochim Biophys Sin (Shanghai) 2012; 44: 847-855.
27. Peters GJ, Backus HH, Freemantle S, van Triest B, Codacci-Pisanelli G, van der Wilt CL et al. Induction of thymidylate synthase as a 5-fluorouracil resistance mechanism. Biochim Biophys Acta 2002; 1587: 194-205.
28. Jackman AL, Kelland LR, Kimbell R, Brown M, GibsonW, Aherne GWet al. Mechanisms of acquired resistance to the quinazoline thymidylate synthase inhibitor ZD1694 (Tomudex) in one mouse and three human cell lines. Br J Cancer 1995; 71: 914-924.
29. Bava SV, Sreekanth CN, Thulasidasan AK, Anto NP, Cheriyan VT, Puliyappadamba VT et al. Akt is upstream and MAPKs are downstream of NF-kappaB in paclitaxel-induced survival signaling events, which are down-regulated by curcumin contributing to their synergism. Int J Biochem Cell Biol 2011; 43: 331-341.
30. Peters GJ, van der Wilt CL, van Triest B, Codacci-Pisanelli G, Johnston PG, van Groeningen CJ et al. Thymidylate synthase and drug resistance. Eur J Cancer 1995; 31A: 1299-1305.
31. Chu E, Zinn S, Boarman D, Allegra CJ. Interaction of gamma interferon and 5-fluorouracil in the H630 human colon carcinoma cell line. Cancer Res 1990; 50: 5834-5840.
32. Copur S, Aiba K, Drake JC, Allegra CJ, Chu E. Thymidylate synthase gene amplification in human colon cancer cell lines resistant to 5-fluorouracil. Biochem Pharmacol 1995; 49: 1419-1426.
33. Kawate H, Landis DM, Loeb LA. Distribution of mutations in human thymidylate synthase yielding resistance to 5-fluorodeoxyuridine. J Biol Chem 2002; 277: 36304-36311.
34. Ferguson PJ, Collins O, Dean NM, DeMoor J, Li CS, Vincent MD et al. Antisense downregulation of thymidylate synthase to suppress growth and enhance cytotoxicity of 5-FUdR, 5-FU and Tomudex in HeLa cells. Br J Pharmacol 1999; 127: 1777-1786.
35. Bras-Goncalves RA, Pocard M, Formento JL, Poirson-Bichat F, De Pinieux G, Pandrea I et al. Synergistic efficacy of 3n-butyrate and 5-fluorouracil in human colorectal cancer xenografts via modulation of DNA synthesis. Gastroenterology 2001; 120: 874-888.
36. Di Gennaro E, Bruzzese F, Pepe S, Leone A, Delrio P, Subbarayan PR et al. Modulation of thymidilate synthase and p53 expression by HDAC inhibitor vorinostat resulted in synergistic antitumor effect in combination with 5FU or raltitrexed. Cancer Biol Ther 2009; 8: 782-791.
37. Jin HS, Lee DH, Kim DH, Chung JH, Lee SJ, Lee TH. cIAP1, cIAP2, and XIAP act cooperatively via nonredundant pathways to regulate genotoxic stress-induced nuclear factor-kappaB activation. Cancer Res 2009; 69: 1782-1791.
38. Ferguson PJ, DeMoor JM, Vincent MD, Koropatnick J. Antisense-induced down-regulation of thymidylate synthase and enhanced cytotoxicity of 5-FUdR in 5-FUdR-resistant HeLa cells. Br J Pharmacol 2001; 134: 1437-1446.
39. Okabe T, Okamoto I, Tsukioka S, Uchida J, Iwasa T, Yoshida T et al. Synergistic antitumor effect of S-1 and the epidermal growth factor receptor inhibitor gefitinib in non-small cell lung cancer cell lines: role of gefitinib-induced down-regulation of thymidylate synthase. Mol Cancer Ther 2008; 7: 599-606.
40. Johnston PG, Mick R, Recant W, Behan KA, Dolan ME, Ratain MJ et al. Thymidylate synthase expression and response to neoadjuvant chemotherapy in patients with advanced head and neck cancer. J Natl Cancer Inst 1997; 89: 308-313.
41. Pestalozzi BC, Peterson HF, Gelber RD, Goldhirsch A, Gusterson BA, Trihia H et al. Prognostic importance of thymidylate synthase expression in early breast cancer. J Clin Oncol 1997; 15: 1923-1931.
42. Wang W, Cassidy J. Constitutive nuclear factor-kappa B mRNA, protein overexpression and enhanced DNA-binding activity in thymidylate synthase inhibitor-resistant tumour cells. Br J Cancer 2003; 88: 624-629.
43. Wang HE, Wu HC, Kao SJ, Tseng FW, Wang YS, Yu HM et al. Modulation of 5-fluorouracil cytotoxicity through thymidylate synthase and NF-kappaB down-regulation and its application on the radiolabelled iododeoxyuridine therapy on human hepatoma cell. Biochem Pharmacol 2005; 69: 617-626.
44. Clarke R, Morwood J, van den Berg HW, Nelson J, Murphy RF. Effect of cytotoxic drugs on estrogen receptor expression and response to tamoxifen in MCF-7 cells. Cancer Res 1986; 46: 6116-6119.
45. Cheng AL, Hsu CH, Lin JK, Hsu MM, Ho YF, Shen TS et al. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res 2001; 21: 2895-2900.
46. Deepa G, Thulasidasan AK, Anto RJ, Pillai JJ, Kumar GV. Cross-linked acrylic hydrogel for the controlled delivery of hydrophobic drugs in cancer therapy. Int J Nanomed 2012; 7: 4077-4088.
47. Nair KL, Thulasidasan AK, Deepa G, Anto RJ, Kumar GS. Purely aqueous PLGA nanoparticulate formulations of curcumin exhibit enhanced anticancer activity with dependence on the combination of the carrier. Int J Pharm 2012; 425: 44-52.
48. Li L, Ahmed B, Mehta K, Kurzrock R. Liposomal curcumin with and without oxaliplatin: effects on cell growth, apoptosis, and angiogenesis in colorectal cancer. Mol Cancer Ther 2007; 6: 1276-1282.
49. Narayanan NK, Nargi D, Randolph C, Narayanan BA. Liposome encapsulation of curcumin and resveratrol in combination reduces prostate cancer incidence in PTEN knockout mice. Int J Cancer 2009; 125: 1-8.
50. Choi EJ, Kim GH. 5-Fluorouracil combined with apigenin enhances anticancer activity through induction of apoptosis in human breast cancer MDA-MB-453 cells. Oncol Rep 2009; 22: 1533-1537.
51. Meiyanto E, Hermawan A. Anindyajati. Natural products for cancer-targeted therapy: citrus flavonoids as potent chemopreventive agents. Asian Pac J Cancer Prev 2012; 13: 427-436.
52. Chou TC. Drug combination studies and their synergy quantification using the Chou- Talalay method. Cancer Res 2010; 70: 440-446.
53. Puliyappadamba VT, Cheriyan VT, Thulasidasan AK, Bava SV, Vinod BS, Prabhu PR et al. Nicotine-induced survival signaling in lung cancer cells is dependent on their p53 status while its down-regulation by curcumin is independent. Mol Cancer 2010; 9: 220.