Antagonism of arachidonic acid is linked to the antitumorigenic effect of dietary eicosapentaenoic acid in Apc(Min/+) mice

Journal of Nutrition

Volumn 130, Issue 5, 2000, Pages 1153-1158

  Hansen Petrik, Melissa B ^a   McEntee, Michael F ^a   Chiu, Chun Hung ^a   Whelan, Jay ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Apc; Arachidonic acid; Cancer; Eicosapentaenoic acid; Mice

Indexed keywords

ARACHIDONIC ACID; ICOSAPENTAENOIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARACHIDONIC ACID METABOLISM; ARTICLE; CANCER GENETICS; COLON POLYPOSIS; DIET SUPPLEMENTATION; DIETARY INTAKE; FAT INTAKE; GENE MUTATION; INTESTINE CANCER; LIPID COMPOSITION; MALE; MOUSE; NONHUMAN;

ANIMALIA;

EID: 0142141255     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/130.5.1153     Document Type: Article

References (53)

1. American Institute of Nutrition (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123: 1939-1951.
2. Anti, M., Marra, G., Armelao, F., Bartoli, G.M., Ficarelli, R., Percesepe, A., De Vitis, I., Maria, G., Sofo, L., Rapaccini, G. L., Gentiloni, N., Piccioni, E. & Miggiano, G. (1992) Effect of ω-3 fatty acids on rectal mucosal cell proliferation in subjects at risk for colon cancer. Gastroenterology 103: 883-891.
3. 2 release in healthy subjects. Gastroenterology 105: 1317-1322.
4. Boolbool, S. K., Dannenberg, A. J., Chadburn, A., Martucci, C., Quo, X.-J., Ramonetti, J. T., Abreu-Goris, M., Newmark, H. L., Lipkin, M. L., DeCosse, J. J. & Bertagnolli, M. M. (1996) Cyclooxygenase-2 overexpression and tumor formation are blocked by sulindac in a murine model of familial adenomatous polyposis. Cancer Res. 56: 2556-2560.
5. Caygill, C. P., Charlett, A. & Hill, M. J. (1996) Fat, fish, fish oil and cancer. Br. J. Cancer 74: 159-164.
6. Chan, T. A., Morin, P. J., Vogelstein, B. & Kinzler, K. W. (1998) Mechanisms underlying nonsteroidal anti-inflammatory drug-mediated apoptosis. Proc. Natl. Acad. Sci. U.S.A. 95: 681-686.
7. Chang, W.-C.L., Chapkin, R. S. & Lupton, J. R. (1998) Fish oil blocks azoxymethane-induced rat colon tumorigenesis by increasing cell differentiation and apoptosis rather than decreasing cell proliferation. J. Nutr. 128: 491-497.
8. Charalambous, D., Skinner, S. A. & O'Brien, P. E. (1998) Sulindac inhibits colorectal tumour growth, but not prostaglandin synthesis in the rat. J. Gastroenterol. Hepatol. 13: 1195-1200.
9. Chiu, C.-H., McEntee, M. F. & Whelan, J. (1997) Sulindac causes rapid regression of preexisting tumors in Min/+ mice independent of prostaglandin biosynthesis. Cancer Res. 57: 4267-4273.
10. Chulada, P. C., Loftin, C. D., Winn, V. D., Young, D. A., Tiano, H. F., Eling, T. E. & Langenbach, R. (1996) Relative activities of retrovirally expressed murine prostaglandin synthase-1 and -2 depend on source of arachidonic acid. Arch. Biochem. Biophys. 330: 301-313.
11. Gonzalez, M. J., Schemmel, R. A., Gray, J. I., Dugan, L., Sheffield, L G. & Welsch, C. W. (1991) Effect of dietary fat on growth of MCF-7 and MDA-MB231 human breast carcinomas in athymic nude mice: relationship between carcinoma growth and lipid peroxidation product levels. Carcinogenesis 12: 1231-1235.
12. Hamilton, L. C., Mitchell, J. A., Tomlinson, A. M. & Warner, T. D. (1999) Synergy between cyclo-oxygenase-2 induction and arachidonic acid supply in vivo: consequences for nonsteroidal anti-inflammatory drug efficacy. FASEB J. 13: 245-251.
13. Hendrickse, C. W., Keighley, M.R.B. & Neoptolemos, J. P. (1995) Dietary ω-3 fats reduce proliferation and tumor yields at colorectal anastomosis in rats. Gastroenterology 109: 431-439.
14. Hoyert, D. L., Kochanek, K. D. & Murphy, S. L. (1999) Deaths: Final Data for 1997. National Center for Health Statistics. Natl. Vital Stat. Rep. 47: 1-105.
15. Min mouse model by the nonsteroidal anti-inflammatory drug piroxicam. Cancer Res. 56: 710-714.
16. Jen, J., Powell, S. M., Papadopoulos, N., Smith, K. J., Hamilton, S. R., Vogelstein, B. & Kinzler, K. W. (1994) Molecular determinants of dysplasia in colorectal lesions. Cancer Res. 54: 5523-5526.
17. Kargman, S. L., O'Neill, G. P., Vickers, P. J., Evans, J. F., Mancini, J. A. & Jothy, S. (1995) Expression of prostaglandin G/H synthase-1 and -2 protein in human colon cancer. Cancer Res. 55: 2556-2559.
18. Kato, I., Akhmedkhanov, A., Koenig, K., Toniolo, P. G., Shore, R. E. & Riboli, E. (1997) Prospective study of diet and female colorectal cancer: The New York University Women's Health Study. Nutr. Cancer 28: 276-281.
19. Kawamori, T., Rao, C. V., Seibert, K. & Reddy, B. S. (1998) Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res. 58: 409-412.
20. Kim, D.-Y., Chung, K.-H. & Lee, J.-H. (1998) Stimulatory effects of high-fat diets on colon cell proliferation depend on the type of dietary fat and site of the colon. Nutr. Cancer 30: 118-123.
21. Kinzler, K. W. & Vogelstein, B. (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170.
22. Latham, P., Lund, E. K. & Johnson, I. T. (1999) Dietary n-3 PUFA increases the apoptotic response to 1,2-dimethylnydrazine, reduces mitosis and suppresses the induction of carcinogenesis in the rat colon. Carcinogenesis 20: 645-650.
23. Levy, D. B., Smith, K. J., Beazer-Barclay, Y., Hamilton, S. R., Vogelstein, B. & Kinzler, K. W. (1994) Inactivation of both APC alleles in human and mouse tumors. Cancer Res. 54: 5953-5958.
24. Li, B., Birdwell, C. & Whelan, J. (1994) Antithetic relationship of dietary arachidonic acid and eicosapentaenoic acid on eicosanoid production in vivo. J. Lipid Res. 35: 1869-1877.
25. Lindner, M. A. (1991) A fish oil diet inhibits colon cancer in mice. Nutr. Cancer 15: 1-11.
26. Mann, N. J., Warrick, G. E., O'Dea, K., Knapp, H. R. & Sinclair, A. J. (1994) The effect of linoleic, arachidonic and eicosapentaenoic acid supplementation on prostacyclin production in rats. Lipids 29: 157-162.
27. Markwell, M.A.K., Haas, S. M., Tolbert, N. E. & Bieber, L. L. (1981) Protein determinations in membrane and lipoprotein samples: manual and automated procedures. Methods Enzymol. 72: 296-303.
28. Mei, J. M., Hord, N. G., Winterstein, D. F., Donald, S. P. & Phang, J. M. (1999) Differential expression of prostaglandin endoperoxide H synthase-2 and formation of activated β-catenin-LEF-1 transcription complex in mouse colonic epithelial cells contrasting in Apc. Carcinogenesis 20: 737-740.
29. Minoura, T., Takata, T., Sakaguchi, M., Takada, H., Yamamura, M., Hioto, K. & Yamamoto, M. (1988) Effect of dietary eicosapentaenoic acid on azoxymethane-induced colon carcinogenesis in rats. Cancer Res. 48: 4790-4794.
30. Miyoshi, Y., Nagase, H., Ando, H., Horii, A., Ichii, S., Nakatsuru, S., Aoki, T., Miki, Y., Mori, T. & Nakamura, Y. (1992) Somatic mutations of the APC gene in colorectal tumors: mutation cluster regions in the APC gene. Hum. Mol. Genet. 1: 229-233.
31. Nakatsugi, S., Fukutake, M., Takahashi, M., Fukuda, K., Isoi, T., Taniguchi, Y., Sugimura, T. & Wakabayashi, K. (1997) Suppression of intestinal polyp development by nimesulide, a selective cyclooxygenase-2 inhibitor, in Min mice. Jpn. J. Cancer Res. 88: 1117-1120.
32. National Research Council (1985) Guide for the Care and Use of Laboratory Animals. Publication no. 85-23 (rev.). National Institutes of Health, Bethesda, MD.
33. Nelson, R. L., Tanure, J. C., Andrianopoulos, G., Souza, G. & Lands, W.E.M. (1988) A comparison of dietary fish oil and corn oil in experimental colorectal carcinogenesis. Nutr. Cancer 11: 215-220.
34. Δ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87: 803-809.
35. Δ716 knockout mice. Carcinogenesis 16: 2605-2607.
36. Paulsen, J. E., Elvsaas, I.-K.O., Steffensen, I.-L. & Alexander, J. (1997) A fish oil derived concentrate enriched in eicosapentaenoic and docosahexaenoic acid as ethyl ester suppresses the formation and growth of intestinal polyps in the Min mouse. Carcinogenesis 18: 1905-1910.
37. Peri, K. G., Varma, D. R. & Chemtob, S. (1997) Stimulation of prostaglandin G/H synthase-2 expression by arachidonic acid monoxygenase product, 14,15-epoxyeicosatrienoic acid. FEBS Lett. 416: 269-272.
38. Piazza, G. A., Alberts, D. S., Hixson, L. J., Shipp Paranka, N., Li, H., Finn, T., Bogert, C., Guillen, J. M., Brendel, K., Gross, P. H., Sperl, G., Ritchie, J., Burt, R. W., Ellsworth, L., Ahnen, D. J. & Pamukcu, R. (1997a) Sulindac sulfone inhibits azoxymethane-induced colon carcinogenesis in rats without reducing prostaglandin levels. Cancer Res. 57: 2909-2915.
39. Piazza, G. A., Rahm, A. K., Finn, T. S., Fryer, B. H., Li, H., Stoumen, A. L., Pamukcu, R. & Ahnen, D. J. (1997b) Apoptosis primarily accounts for the growth-inhibitory properties of sulindac metabolites and involves a mechanism that is independent of cyclooxygenase inhibition, cell cycle arrest, and p53 induction. Cancer Res. 57: 2452-2459.
40. Powell, S. M., Zilz, N., Beazer-Barclay, Y., Bryan, T. M., Hamilton, S. R., Thibodeau, S. N., Vogelstein, B. & Kinzler, K. W. (1992) APC mutations occur early during colorectal tumorigenesis. Nature (Lond.) 359: 235-237.
41. Reddy, B. S., Burill, C. & Rigotty, J. (1991) Effect of diets high in ω-3 and ω-6 fatty acids on initiation and postinitiation stages of colon carcinogenesis. Cancer Res. 51: 487-491.
42. Reddy, B. S. & Maruyama, H. (1986) Effect of dietary fish oil on azoxymethane-induced colon carcinogenesis in male F344 rats. Cancer Res. 46: 3367-3370.
43. Min mouse by piroxicam: kinetics, strain effects and resistance to chemosuppression. Carcinogenesis 20: 51-58.
44. Sano, H., Kawahito, Y., Wilder, R. L., Hashiramoto, A., Mukai, S., Asai, K., Kimura, S., Kato, H., Kondo, M. & Hla, T. (1995) Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res. 55: 3785-3789.
45. Sheng, H., Shao, J., Kirkland, S. C., Isakson, P., Coffey, R. J., Morrow, J., Beauchamp, R. D. & DuBois, R. N. (1997) Inhibition of human colon cancer cell growth by selective inhibition of cyclooxygenase-2. J. Clin. Investig. 99: 2254-2259.
46. Simmons, D. L., Botting, R. M., Robertson, P. M., Madsen, M. L. & Vane, J. R. (1999) Induction of an acetaminophen-sensitive cyclooxygenase with reduced sensitivity to nonsteroid anti-inflammatory drugs. Proc. Natl. Acad. Sci. U.S.A. 96: 3275-3280.
47. Singh, J., Hamid, R. & Reddy, B. S. (1997) Dietary fat and colon cancer: modulation of cyclooxygenase-2 by types and amount of dietary fat during the postinitiation stage of colon carcinogenesis. Cancer Res. 57: 3465-3470.
48. Smith, K. J., Johnson, K. A., Bryan, T. M., Hill, D. E., Markowitz, S., Willson, J.K.V., Paraskeva, C., Petersen, G. M., Hamilton, S. R., Vogelstein, B. & Kinzler, K. W. (1993) The APC gene product in normal and tumor cells. Proc. Natl. Acad. Sci. U.S.A. 90: 2846-2850.
49. Tsujii, M. & DuBois, R. N. (1995) Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperaxide synthase 2. Cell 83: 493-501.
50. Wasan, H. S., Novelli, M., Bee, J. & Bodmer, W. F. (1997) Dietary fat influences on polyp phenotype in multiple intestinal neoplasia mice. Proc. Natl. Acad. Sci. U.S.A. 94: 3308-3313.
51. Whelan, J., Broughton, K. S., Surette, M. E. & Kinsella, J. E. (1992) Dietary arachidonic and linoleic acids: comparative effects on tissue lipids. Lipids 27: 85-88.
52. Whelan, J., Surette, M. E., Hardardóttir, I., Lu, G., Golemboski, K. A., Larsen, E. & Kinsella, J. E. (1993) Dietary arachidonate enhances tissue arachidonate levels and eicosanoid production in Syrian hamsters. J. Nutr. 123: 2174-2185.
53. Williams, C. S., Luongo, C., Radhika, A., Zhang, T., Lamps, L. W., Nanney, L. B., Beauchamp, R. D. & DuBois, R. N. (1996) Elevated cyclooxygenase-2 levels in Min mouse adenomas. Gastroenterology 111: 1134-1140.