Upregulation of extrinsic apoptotic pathway in curcumin-mediated antiproliferative effect on human pancreatic carcinogenesis

Journal of Cellular Biochemistry

Volumn 114, Issue 12, 2013, Pages 2654-2665

  Youns, Mahmoud ^a,b   Fathy, Gihan Mahmoud ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b Ein Helwan   (Egypt)

Author keywords

APOPTOSIS AND COX 2; CURCUMIN; MICROARRAY; PANCREATIC CANCER

Indexed keywords

BIOLOGICAL MARKER; CURCUMIN; DNA FRAGMENT; HISTONE; SULFORHODAMINE B;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BAX GENE; BCL2L10 GENE; BID GENE; CANCER CELL CULTURE; CANCER PREVENTION; CARCINOGENESIS; CASP 8 GENE; CASP3 GENE; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; COX 2 GENE; CURCUMA LONGA; CYTOPLASM; DOWN REGULATION; FLOW CYTOMETRY; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MARKER GENE; METASTASIS; MICROARRAY ANALYSIS; NDRG 1 GENE; NFKAPPAB GENE; PANCREAS CANCER; PANCREAS CARCINOGENESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TNFR GENE; TUMOR GENE; UPREGULATION;

APOPTOSIS AND COX-2; CURCUMIN; MICROARRAY; PANCREATIC CANCER;

APOPTOSIS; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CURCUMIN; CYCLOOXYGENASE 2; CYTOPLASM; DNA FRAGMENTATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84885625894     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24612     Document Type: Article

References (69)

1. Alhamdani MS, Youns M, Buchholz M, Gress TM, Beckers MC, Marechal D, Bauer A, Schroder C, Hoheisel JD,. 2012. Immunoassay-based proteome profiling of 24 pancreatic cancer cell lines. J Proteomics 75: 3747-3759.
2. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB,. 2007. Bioavailability of curcumin: Problems and promises. Mol Pharm 4: 807-818.
3. Berger JM, Gamblin SJ, Harrison SC, Wang JC,. 1996. Structure and mechanism of DNA topoisomerase II. Nature 379: 225-232.
4. Brouet I, Ohshima H,. 1995. Curcumin, an anti-tumour promoter and anti-inflammatory agent, inhibits induction of nitric oxide synthase in activated macrophages. Biochem Biophys Res Commun 206: 533-540.
5. Chiang KC, Yu CC, Chen JR, Huang YT, Huang CC, Yeh CN, Tsai CS, Chen LW, Chen HC, Hsu JT, Wang CH, Chen HY,. 2012. Oncocytic-type intraductal papillary mucinous neoplasm (IPMN)-derived invasive oncocytic pancreatic carcinoma with brain metastasis-A case report. World J Surg Oncol 10: 138.
6. Chidambara Murthy KN, Jayaprakasha GK, Patil BS,. 2013. Citrus limonoids and curcumin additively inhibit human colon cancer cells. Food Funct 4 (5): 803-810.
7. Chung MY, Lim TG, Lee KW,. 2013. Molecular mechanisms of chemopreventive phytochemicals against gastroenterological cancer development. World J Gastroenterol 19: 984-993.
8. Cort A, Timur M, Ozdemir E, Ozben T,. 2013. Effects of curcumin on bleomycin-induced apoptosis in human malignant testicular germ cells. J Physiol Biochem 69: 289-296.
9. Dempe S, Lavie M, Struyf S, Bhat R, Verbeke H, Paschek S, Berghmans N, Geibig R, Rommelaere J, Van Damme J, Dinsart C,. 2012. Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: Implication of leucocyte recruitment. Cancer Immunol Immunother 61: 2113-2123.
10. Ellen TP, Ke Q, Zhang P, Costa M,. 2008. NDRG1, a growth and cancer related gene: Regulation of gene expression and function in normal and disease states. Carcinogenesis 29: 2-8.
11. Fujimura T, Ohta T, Oyama K, Miyashita T, Miwa K,. 2006. Role of cyclooxygenase-2 in the carcinogenesis of gastrointestinal tract cancers: A review and report of personal experience. World J Gastroenterol 12: 1336-1345.
12. Fulda S, Debatin KM,. 2004. Apoptosis signaling in tumor therapy. Ann N Y Acad Sci 1028: 150-156.
13. Fulda S, Debatin KM,. 2006. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25: 4798-4811.
14. Gandhy SU, Kim K, Larsen L, Rosengren RJ, Safe S,. 2012. Curcumin and synthetic analogs induce reactive oxygen species and decreases specificity protein (Sp) transcription factors by targeting microRNAs. BMC Cancer 12: 564.
15. Glienke W, Maute L, Wicht J, Bergmann L,. 2010. Curcumin inhibits constitutive STAT3 phosphorylation in human pancreatic cancer cell lines and down-regulation of survivin/BIRC5 gene expression. Cancer Invest 28: 166-171.
16. Goel A, Aggarwal BB,. 2010. Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr Cancer 62: 919-930.
17. Goel A, Kunnumakkara AB, Aggarwal BB,. 2008. Curcumin as "Curecumin": From kitchen to clinic. Biochem Pharmacol 75: 787-809.
18. Hartojo W, Silvers AL, Thomas DG, Seder CW, Lin L, Rao H, Wang Z, Greenson JK, Giordano TJ, Orringer MB, Rehemtulla A, Bhojani MS, Beer DG, Chang AC,. 2010. Curcumin promotes apoptosis, increases chemosensitivity, and inhibits nuclear factor kappaB in esophageal adenocarcinoma. Transl Oncol 3: 99-108.
19. Hidaka H, Ishiko T, Furuhashi T, Kamohara H, Suzuki S, Miyazaki M, Ikeda O, Mita S, Setoguchi T, Ogawa M,. 2002. Curcumin inhibits interleukin 8 production and enhances interleukin 8 receptor expression on the cell surface:Impact on human pancreatic carcinoma cell growth by autocrine regulation. Cancer 95: 1206-1214.
20. Hu P, Huang P, Chen MW,. 2013. Curcumin attenuates cyclooxygenase-2 expression via inhibition of the NF-kappaB pathway in lipopolysaccharide- stimulated human gingival fibroblasts. Cell Biol Int 37: 443-448.
21. Ip SW, Wu SY, Yu CC, Kuo CL, Yu CS, Yang JS, Lin ZP, Chiou SM, Chung HK, Ho HC, Chung JG,. 2011. Induction of apoptotic death by curcumin in human tongue squamous cell carcinoma SCC-4 cells is mediated through endoplasmic reticulum stress and mitochondria-dependent pathways. Cell Biochem Funct 29: 641-650.
22. Jobin C, Bradham CA, Russo MP, Juma B, Narula AS, Brenner DA, Sartor RB,. 1999. Curcumin blocks cytokine-mediated NF-kappa B activation and proinflammatory gene expression by inhibiting inhibitory factor I-kappa B kinase activity. J Immunol 163: 3474-3483.
23. Kakar SS, Roy D,. 1994. Curcumin inhibits TPA induced expression of c-fos, c-jun, and c-myc proto-oncogenes messenger RNAs in mouse skin. Cancer Lett 87: 85-89.
24. Kawamori T, Lubet R, Steele VE, Kelloff GJ, Kaskey RB, Rao CV, Reddy BS,. 1999. Chemopreventive effect of curcumin, a naturally occurring anti-inflammatory agent, during the promotion/progression stages of colon cancer. Cancer Res 59: 597-601.
25. Ketron AC, Gordon ON, Schneider C, Osheroff N,. 2013. Oxidative metabolites of curcumin poison human type II topoisomerases. Biochemistry 52: 221-227.
26. Khan N, Afaq F, Mukhtar H,. 2007. Apoptosis by dietary factors: The suicide solution for delaying cancer growth. Carcinogenesis 28: 233-239.
27. Kunnumakkara AB, Guha S, Krishnan S, Diagaradjane P, Gelovani J, Aggarwal BB,. 2007. Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factor-kappaB-regulated gene products. Cancer Res 67: 3853-3861.
28. Kuo ML, Huang TS, Lin JK,. 1996. Curcumin, an antioxidant and anti-tumor promoter, induces apoptosis in human leukemia cells. Biochim Biophys Acta 1317: 95-100.
29. Lee KW, Bode AM, Dong Z,. 2011. Molecular targets of phytochemicals for cancer prevention. Nat Rev Cancer 11: 211-218.
30. Lev-Ari S, Zinger H, Kazanov D, Yona D, Ben-Yosef R, Starr A, Figer A, Arber N,. 2005. Curcumin synergistically potentiates the growth inhibitory and pro-apoptotic effects of celecoxib in pancreatic adenocarcinoma cells. Biomed Pharmacother 59 (Suppl 2): S276-S280.
31. Lev-Ari S, Vexler A, Starr A, Ashkenazy-Voghera M, Greif J, Aderka D, Ben-Yosef R,. 2007. Curcumin augments gemcitabine cytotoxic effect on pancreatic adenocarcinoma cell lines. Cancer Invest 25: 411-418.
32. Li D, Xie K, Wolff R, Abbruzzese JL,. 2004a. Pancreatic cancer. Lancet 363: 1049-1057.
33. Li L, Aggarwal BB, Shishodia S, Abbruzzese J, Kurzrock R,. 2004b. Nuclear factor-kappaB and IkappaB kinase are constitutively active in human pancreatic cells, and their down-regulation by curcumin (diferuloylmethane) is associated with the suppression of proliferation and the induction of apoptosis. Cancer 101: 2351-2362.
34. Lu YP, Chang RL, Lou YR, Huang MT, Newmark HL, Reuhl KR, Conney AH,. 1994. Effect of curcumin on 12-O-tetradecanoylphorbol-13-acetate- and ultraviolet B light-induced expression of c-Jun and c-Fos in JB6 cells and in mouse epidermis. Carcinogenesis 15: 2363-2370.
35. Makin G, Dive C,. 2001. Apoptosis and cancer chemotherapy. Trends Cell Biol 11: S22-S26.
36. Martin-Cordero C, Lopez-Lazaro M, Galvez M, Ayuso MJ,. 2003. Curcumin as a DNA topoisomerase II poison. J Enzyme Inhib Med Chem 18: 505-509.
37. Masuelli L, Benvenuto M, Fantini M, Marzocchella L, Sacchetti P, Di Stefano E, Tresoldi I, Izzi V, Bernardini R, Palumbo C, Mattei M, Lista F, Galvano F, Modesti A, Bei R,. 2013. Curcumin induces apoptosis in breast cancer cell lines and delays the growth of mammary tumors in neu transgenic mice. J Biol Regul Homeost Agents 27: 105-119.
38. Mielgo A, Schmid MC,. 2013. Impact of tumour associated macrophages in pancreatic cancer. BMB Rep 46: 131-138.
39. Mulyaningsih S, Youns M, El-Readi MZ, Ashour ML, Nibret E, Sporer F, Herrmann F, Reichling J, Wink M,. 2010. Biological activity of the essential oil of Kadsura longipedunculata (Schisandraceae) and its major components. J Pharm Pharmacol 62: 1037-1044.
40. Nakatani Y, Kleffmann T, Linke K, Condon SM, Hinds MG, Day CL,. 2013. Regulation of ubiquitin transfer by XIAP, a dimeric RING E3 ligase. Biochem J 450: 629-638.
41. Parasramka MA, Gupta SV,. 2012. Synergistic effect of garcinol and curcumin on antiproliferative and apoptotic activity in pancreatic cancer cells. J Oncol 2012: 709739.
42. Park W, Amin AR, Chen ZG, Shin DM,. 2013. New perspectives of curcumin in cancer prevention. Cancer Prev Res (Phila) 6: 387-400.
43. Plummer SM, Holloway KA, Manson MM, Munks RJ, Kaptein A, Farrow S, Howells L,. 1999. Inhibition of cyclo-oxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-kappaB activation via the NIK/IKK signalling complex. Oncogene 18: 6013-6020.
44. Qiao Q, Jiang Y, Li G,. 2013. Inhibition of the PI3K/AKT-NF-kappaB pathway with curcumin enhanced radiation-induced apoptosis in human Burkitt's lymphoma. J Pharmacol Sci 121: 247-256.
45. Ramachandran C, Rodriguez S, Ramachandran R, Raveendran Nair PK, Fonseca H, Khatib Z, Escalon E, Melnick SJ,. 2005. Expression profiles of apoptotic genes induced by curcumin in human breast cancer and mammary epithelial cell lines. Anticancer Res 25: 3293-3302.
46. Rao J, Xu DR, Zheng FM, Long ZJ, Huang SS, Wu X, Zhou WH, Huang RW, Liu Q,. 2011. Curcumin reduces expression of Bcl-2, leading to apoptosis in daunorubicin-insensitive CD34+ acute myeloid leukemia cell lines and primary sorted CD34+ acute myeloid leukemia cells. J Transl Med 9: 71.
47. Schmidt BH, Osheroff N, Berger JM,. 2012. Structure of a topoisomerase II-DNA-nucleotide complex reveals a new control mechanism for ATPase activity. Nat Struct Mol Biol 19: 1147-1154.
48. Siegel R, Naishadham D, Jemal A,. 2013. Cancer statistics, 2013. CA Cancer J Clin 63: 11-30.
49. Stan SD, Singh SV, Brand RE,. 2010. Chemoprevention strategies for pancreatic cancer. Nat Rev Gastroenterol Hepatol 7: 347-356.
50. Stasinopoulos I, O'Brien DR, Wildes F, Glunde K, Bhujwalla ZM,. 2007. Silencing of cyclooxygenase-2 inhibits metastasis and delays tumor onset of poorly differentiated metastatic breast cancer cells. Mol Cancer Res 5: 435-442.
51. Subramanian M, Sreejayan N, Rao MN, Devasagayam TP, Singh BB,. 1994. Diminution of singlet oxygen-induced DNA damage by curcumin and related antioxidants. Mutat Res 311: 249-255.
52. Sun M, Estrov Z, Ji Y, Coombes KR, Harris DH, Kurzrock R,. 2008. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol Cancer Ther 7: 464-473.
53. Sun XD, Liu XE, Huang DS,. 2013. Curcumin reverses the epithelial-mesenchymal transition of pancreatic cancer cells by inhibiting the Hedgehog signaling pathway. Oncol Rep 29: 2401-2407.
54. Swamy MV, Citineni B, Patlolla JM, Mohammed A, Zhang Y, Rao CV,. 2008. Prevention and treatment of pancreatic cancer by curcumin in combination with omega-3 fatty acids. Nutr Cancer 60 (Suppl 1): 81-89.
55. Thakkar A, Sutaria D, Grandhi BK, Wang J, Prabhu S,. 2013. The molecular mechanism of action of aspirin, curcumin and sulforaphane combinations in the chemoprevention of pancreatic cancer. Oncol Rep 29: 1671-1677.
56. Tjensvoll K, Nordgard O, Smaaland R,. 2013. Circulating tumor cells in pancreatic cancer patients: Methods of detection and clinical implications. Int J Cancer. doi: 10.1002/ijc.28134
57. Wang W, Abbruzzese JL, Evans DB, Larry L, Cleary KR, Chiao PJ,. 1999. The nuclear factor-kappa B RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin Cancer Res 5: 119-127.
58. Wang Z, Zhang Y, Banerjee S, Li Y, Sarkar FH,. 2006. Notch-1 down-regulation by curcumin is associated with the inhibition of cell growth and the induction of apoptosis in pancreatic cancer cells. Cancer 106: 2503-2513.
59. Wei D, Peng JJ, Gao H, Li H, Li D, Tan Y, Zhang T,. 2013. Digoxin down-regulates NDRG1 and VEGF through the inhibition of HIF-1alpha under hypoxic conditions in human lung adenocarcinoma A549 Cells. Int J Mol Sci 14: 7273-7285.
60. Yallapu MM, Ebeling MC, Jaggi M, Chauhan SC,. 2013. Plasma proteins interaction with curcumin nanoparticles: Implications in cancer therapeutics. Curr Drug Metab 14 (4): 504-515.
61. Yang CL, Ma YG, Xue YX, Liu YY, Xie H, Qiu GR,. 2012. Curcumin induces small cell lung cancer NCI-H446 cell apoptosis via the reactive oxygen species-mediated mitochondrial pathway and not the cell death receptor pathway. DNA Cell Biol 31: 139-150.
62. Yip-Schneider MT, Barnard DS, Billings SD, Cheng L, Heilman DK, Lin A, Marshall SJ, Crowell PL, Marshall MS, Sweeney CJ,. 2000. Cyclooxygenase-2 expression in human pancreatic adenocarcinomas. Carcinogenesis 21: 139-146.
63. Youns M, Efferth T, Hoheisel JD,. 2009a. Microarray analysis of gene expression in medicinal plant research. Drug Discov Ther 3: 200-207.
64. Youns M, Efferth T, Reichling J, Fellenberg K, Bauer A, Hoheisel JD,. 2009b. Gene expression profiling identifies novel key players involved in the cytotoxic effect of Artesunate on pancreatic cancer cells. Biochem Pharmacol 78: 273-283.
65. Youns M, Hoheisel JD, Efferth T,. 2010. Toxicogenomics for the prediction of toxicity related to herbs from traditional Chinese medicine. Planta Med 76: 2019-2025.
66. Youns M, Efferth T, Hoheisel JD,. 2011. Transcript profiling identifies novel key players mediating the growth inhibitory effect of NS-398 on human pancreatic cancer cells. Eur J Pharmacol 650: 170-177.
67. Yu J, Peng Y, Wu LC, Xie Z, Deng Y, Hughes T, He S, Mo X, Chiu M, Wang QE, He X, Liu S, Grever MR, Chan KK, Liu Z,. 2013. Curcumin down-regulates DNA methyltransferase 1 and plays an anti-leukemic role in acute myeloid leukemia. PLoS ONE 8: 55934.
68. Zhang CY, Zhang L, Yu HX, Bao JD, Sun Z, Lu RR,. 2013. Curcumin inhibits invasion and metastasis in K1 papillary thyroid cancer cells. Food Chem 139: 1021-10218.
69. Zhuang M, Guan S, Wang H, Burlingame AL, Wells JA,. 2013. Substrates of IAP ubiquitin ligases identified with a designed orthogonal E3 ligase, the NEDDylator. Mol Cell 49: 273-282.