Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells

Journal of Agricultural and Food Chemistry

Volumn 54, Issue 3, 2006, Pages 980-985

  Adams, Lynn S ^a   Seeram, Navindra P ^a   Aggarwal, Bharat B ^b   Takada, Yasunari ^b   Sand, Daniel ^a   Heber, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

AKT; Cancer; COX 2; NF B; Pomegranate

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTINEOPLASTIC AGENT; CYCLOOXYGENASE 2; PROTEIN KINASE; PUNICALAGIN; TANNIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BEVERAGE; CELL STRAIN HT29; CHEMISTRY; DRUG EFFECT; FRUIT; HUMAN; INFLAMMATION; METABOLISM; POMEGRANATE; SIGNAL TRANSDUCTION;

ANTI-INFLAMMATORY AGENTS; ANTINEOPLASTIC AGENTS; BEVERAGES; CYCLOOXYGENASE 2; FRUIT; HT29 CELLS; HUMANS; HYDROLYZABLE TANNINS; INFLAMMATION; PROTEIN KINASES; PUNICACEAE; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

LYTHRACEAE; PUNICA GRANATUM;

EID: 33244454723     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf052005r     Document Type: Article

References (46)

1. Boik, J. Mutations, gene expression, and proliferation. In Natural Compounds in Cancer Therapy, 1st ed.; S. Farnell, Ed. Oregon Medical Press: Princeton, MN, 2001; p 22.
2. Pohl, C.; Hombach, A.; Kruis, W. Chronic inflammatory bowel disease and cancer. Hepato - gastroenterology 2000, 47, 57-70.
3. Lewis, J. D.; Deren, G. R. Cancer risk in patients with inflammatory bowel disease. Gastroenterol. Clin. North Am. 1999, 28, 459-477.
4. Block, G.; Patterson, B.; Subar, A. Fruit, vegetables and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer 1992, 18, 1-29.
5. Afaq, F.; Saleem, M.; Krueger, C. G.; Reed, J. D.; Mukhtar, H. Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF-kappaB pathways and inhibits skin tumorigenesis in CD-1 mice. Int. J. Cancer 2005, 113 (3), 423-33.
6. Aviram, M.; Dornfield, L.; Rosenblatt, M.; Volkova, N.; Kaplan, M.; Coleman, R.; Hayek, T.; Presser, D.; Fuhrman, B. Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am. J. Clin. Nutr. 2000, 71, 1062-76.
7. Kaplan, M.; Hayek, T.; Raz, A.; Coleman, R.; Dornfield, L.; Vaya, J.; Aviram, M. Pomegranate juice supplementation to atherosclerotic mice reduces macrophage lipid peroxidation, cellular cholesterol accumulation and development of atherosclerosis. J. Nutr. 2001, 131, 2082-9.
8. Gu, L.; Kelm, M.; Hammerstone, J. F.; Beecher, G.; Holden, J.; Haytowitz, D.; Gebhardt, S.; Prior, R. Concentrations of proanthocyanidins in common foods and estimations of normal consumption. J. Nutr. 2004, 134, 613-7.
9. Cerda, B.; Ceron, J. J.; Tomas-Barberan, F. A.; Espin, J. C. Repeated oral administration of high doses of pomegranate ellagitannin punicalagin to rats for 37 days is not toxic. J. Agric. Food Chem. 2003, 51, 3493-501.
10. Cerda, B.; Llorach, R.; Ceron, J. J.; Espin, J. C.; Tomas-Barberan, F. A. Evaluation of the bioavailability and metabolism in the rat of punicalagin, an antioxidant polyphenol from pomegranate juice. Eur. J. Nutr. 2003, 42, 18-28.
11. Seeram, N. P.; Adams, L. S.; Henning, S. M.; Niu, Y.; Zhang, Y.; Nair, M. G.; Heber, D. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem. 2005, 16 (6), 360-7.
12. Aviram, M.; Rosenblatt, M.; Gaitani, D.; Nitecki, S.; Hoffman, A.; Dornfield, L.; Volkova, N.; Presser, D.; Attias, J.; Liker, H.; et al. Pomegranate juice consumption for 3 years by patients with carotid artery stenosis (CAS) reduces common carotid intima-media thickness (IMT), blood pressure and LDL oxidation. Clin. Nutr. 2004, 23, 423-33.
13. Gil, M. I.; Tomas-Barberan, F. A.; Hess-Pierce, B.; Holcroft, D. M.; Kader, A. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J. Agric. Food Chem. 2000, 48, 4581-4589.
14. Seeram, N. P.; Lee, R.; Hardy, M. L.; Heber, D. Large-scale purification of ellagitannins from pomegranate husk, a byproduct of the commercial juice industry. Sep. Purif. Technol. 2005, 41, 49-55.
15. Zhang, X.; Morham, S. G.; Langenbach, R.; Baggs, R. B.; Young, D. A. Lack of cyclooxygenase-2 inhibits growth of teratocarcinomas in mice. Exp. Cell Res. 2000, 254 (2), 232-40.
16. Handler, J. A.; Danilowicz, R. M.; Eling, E. Mitogenic signaling by epidermal growth factor (EGF), but not platelet-derived growth factor, requires arachidonic acid metabolism in BALB/c 3T3 cells. Modulation of EGF-dependent c-myc expression by prostaglandins. J. Biol. Chem. 1990, 265, 3669-3673.
17. Hara, A.; Yoshimi, N.; Niwa, M.; Ino, N.; Mori, H. Apoptosis induced by NS-398, a selective cyclooxygenase-2 inhibitor, in human colorectal cancer cell lines. Jpn. J. Cancer Res. 1997, 88 (6), 600-4.
18. Sheng, H.; Shao, J.; Kirkland, S. C.; Isakson, P.; Coffey, R. J.; Morrow, J.; Beauchamp, R.; DuBois, R. Inhibition of human colon cancer cell growth by selective inhibition of cycloosygenase-2. J. Clin. Invest. 1997, 99, 2254-2259.
19. Tsuji, S.; Kawano, S.; Sawaoka, H.; Takei, Y.; Kobayashi, I.; Nagano, K.; Fusamoto, H.; Kamato, T. Evidence for involvement of cyclooxygenase-2 in proliferation of two gastrointestinal cancer cell lines. Prostaglandins, Leukotrienes Essent. Fatty Acids 1996, 55, 179-183.
20. Aggarwal, B.; Swaroop, P.; Protiva, P.; Raj, S. V.; Shirin, H.; Holt, P. R. Cox-2 is needed but not sufficient for apoptosis induced by Cox-2 selective inhibitors in colon cancer cells. Apoptosis 2003, 8 (6), 649-54.
21. Li, M.; Wu, X.; Xu, X. C. Induction of apoptosis in colon cancer cells by cyclooxygenase-2 inhibitor NS398 through a cytochrome c-dependent pathway. Clin. Cancer Res. 2001, 7, 1010-1016.
22. Lu, X.; Xie, W.; Reed, D.; Bradshaw, W. S.; Simmons, D. L. Nonsteroidal antiinflammatory drugs cause apoptosis and induce cyclooxygenases in chicken embryo fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 7961-7965.
23. Steinbach, G.; Lynch, P. M.; Phillips, R. K.; Wallace, M. H.; Hawk, E.; Gordon, G. B.; Wakabayashi, N.; Saunders, B.; Shen, Y.; Fujimura, T.; et al. The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N. Engl. J. Med. 2000, 342, 1946-1952.
24. Waddell, W. R.; Ganser, G. F.; Cerise, E. J.; Loughry, R. W. Sulindac for polyposis of the colon. Am. J. Surg. 1989, 157, 175-179.
25. Maehama, T.; Dixon, J. E. The tumour suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273, 13375-13378.
26. Lynch, E. D.; Ostermeyer, E. A.; Lee, M. K.; Arena, J. F.; Ji, H.; Dann, J.; et al. Inherited mutations in PTEN that are associated with breast cancer, Cowden disease and juvenile polyposis. Am. J. Hum. Genet. 1997, 61, 1254-1260.
27. Petiot, A.; Ogier-Denis, E.; Blommaart, E. F.; Meijer, A. J.; Codogno, P. Distinct classes of phosphatidylinositol 3-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 2000, 275, 992-998.
28. Schultz, R. M.; Merriman, R. L.; Andis, S. L.; Bonjouklian, R.; Grindey, G. B.; Rutherford, P. G.; Gallegos, A.; Massey, K.; Powis, G. In vitro and in vivo antitumor activity of the phosphatidylinositol 3-kinase inhibitor wortmannin. Anticancer Res. 1995, 15, 1135-1139.
29. Paik, J.; Lee, J. Y.; Hwang, D. Signaling pathways for TNFα-induced COX-2 expression: mediation through MAP kinases and NFkB, and inhibition by certain nonsteroidal antiinflammatory drugs. Adv. Exp. Med. Biol. 2002, 507, 503-8.
30. Chun, K. S.; Surh, Y. J. Signal transduction pathways regulating cyclooxygenase-2 expression: potential molecular targets for chemoprevention. Biochem. Pharmacol. 2004, 68 (6), 1089-100.
31. Jobin, C.; Morteau, O.; Han, D. S.; Balfour Sartor, R. Specific NFκB blockade selectively inhibits tumour necrosis factor-a-induced COX-2 but not constitutive COX-1 gene expression in HT-29 cells. Immunology 1998, 95, 537-543.
32. Chaturvedi, M. M.; Mukhopadhyay, A.; Aggarwal, B. B. Assay for redox sensitive transcription factors. Methods Enzymol. 2000, 319, 585-601.
33. Yao, M.; Lam, E. C.; Kelly, C. R.; Zhou, W.; Wolfe, M. M. Cyclooxygenase-2 selective inhibition with NS-398 suppresses proliferation and invasiveness and delays liver metastasis in colorectal cancer. Br. J. Cancer 2004, 90 (3), 712-9.
34. Kim, N. D.; Mehta, R.; Yu, W.; Neeman, I.; Livney, T.; Amichay, A.; Poirier, D.; Nicholls, P.; Kirby, A.; Jiang, W.; et al. Chemopreventive and adjuvant therapeutic potential of pomegranate (Punica granatum) for human breast cancer. Breast Cancer Res. Treat. 2002, 71 (3), 203-17.
35. Lansky, E. P.; Jiang, W.; Mo, H.; Bravo, L.; Froom, P.; Yu, W.; Harris, N. M.; Neeman, I.; Campbell, M. J. Possible synergistic prostate cancer suppression by anatomically discrete pomegranate fractions. Invest. New Drugs 2005, 23 (1), 11-20.
36. Albrecht, M.; Jiang, W.; Kumi-Diaka, J.; Lansky, E. P.; Gommersall, L. M.; Patel, A.; Mansel, R. E.; Neeman, I.; Geldof, A. A.; Campbell, M. J. Pomegranate extracts potently suppress proliferation, xenograft growth, and invasion of human prostate cancer cells. J. Med. Food 2004, 7 (3), 274-83.
37. Sheu, M. L.; Chao, K. F.; Sung, Y. J.; Lin, W. W.; Lin-Shiau, S. Y.; Liu, S. H. Activation of phosphoinositide 3-kinase in response to inflammation and nitric oxide leads to the up-regulation of cyclooxygenase-2 expression and subsequent cell proliferation in mesangial cells. Cell. Signalling 2005, 17 (8), 975-84.
38. Matsuura, H.; Sakaue, M.; Subbaramaiah, K.; Kamitani, H.; Eling, T. E.; Dannenberg, A. J.; Tanabe, T.; Inoue, H.; Arata, J.; Jetten, A. M. Regulation of cyclooxygenase-2 by interferon gamma and transforming growth factor alpha in normal human epidermal keratinocytes and squamous carcinoma cells. Role of mitogen-activated protein kinases. J. Biol. Chem. 1999, 274 (41), 29138-29148.
39. Shao, J.; Sheng, H.; Inoue, H.; Morrow, J. D.; DuBois, R. N. Regulation of constitutive cyclooxygenase-2 expression in colon carcinoma cells. J. Biol. Chem. 2000, 275 (43), 33951-33956.
40. Subbaramaiah, K.; Dannenberg, A. J. Cyclooxygenase 2: a molecular target for cancer prevention and treatment. Trends Pharmacol. Sci. 2003, 24 (2), 96-102.
41. Seeram, N. P.; Cichewicz, R. H.; Chandra, A.; Nair, M. G. Cyclooxygenase inhibitory and antioxidant compounds from crabapple fruits. J. Agric. Food Chem. 2003, 51 (7), 1948-51.
42. Wang, S. Y.; Feng, R.; Bowman, L.; Penhallegon, R.; Ding, M.; Lu, Y. Antioxidant activity in lingonberries (Vaccinium vitisidaea L.) and its inhibitory effect on activator protein-1, nuclear factor-kappaB, and mitogen-activated protein kinases activation. J. Agric. Food Chem. 2005, 53 (8), 3156-3166.
43. Zhang, F.; Altorki, N. K.; Mestre, J. R.; et al. Curcumin inhibitscyclooxygenase-2 transcription in bile acid- and phorbol ester treated human gastrointestinal epithelial cells. Carcinogenesis 1999, 20, 445-451.
44. Goel, A.; Boland, C. R.; Chauhan, D. P. Specific inhibition of cyclooxygenase-2 (COX-2) expression by dietary curcumin in HT-29 human colon cancer cells. Cancer Lett. 2001, 172, 111-118.
45. Hong, J.; Smith, T. J.; Ho, C. T.; August, D. A.; Yang, C. S. Effects of purified green and black tea polyphenols on cyclooxygenase- and lipoxygenase-dependent metabolism of arachidonic acid in human colon mucosa and colon tumor tissues. Biochem. Pharmacol. 2001, 62, 1175-1183.
46. Manach, C.; Donovan, J. Pharmacokinetics and Metabolism of Dietary Flavonoids in Humans. Free Radical Res. 2004, 38 (8), 771-785.