Effect of cyclooxygenase genotype and dietary fish oil on colonic eicosanoids in mice

Journal of Nutritional Biochemistry

Volumn 23, Issue 8, 2012, Pages 966-976

  Neilson, Andrew P ^a   Djuric, Zora ^a   Ren, Jianwei ^a   Hong, Yu H ^a   Sen, Ananda ^a   Lager, Corey ^a   Jiang, Yan ^a   Reuven, Shony ^a   Smith, William L ^a   Brenner, Dean E ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Colon cancer; Cyclooxygenase; EPA; Fish oil; Hydroxyeicosatetraenoic acids; Prostaglandin E2

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; 5 HYDROXYICOSATETRAENOIC ACID; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; FATTY ACID; FISH OIL; ICOSANOID; KI 67 ANTIGEN; LIPOXYGENASE; MENHADEN OIL; OLIVE OIL; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COLON MUCOSA; CONTROLLED STUDY; CRYPT CELL; DIET SUPPLEMENTATION; ENZYME INHIBITION; FEMALE; GENE DELETION; GENOTYPE; IMMUNOHISTOCHEMISTRY; LIPID COMPOSITION; LIQUID CHROMATOGRAPHY; METABOLITE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY;

ANIMALS; CELL PROLIFERATION; COLON; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; DIETARY FATS, UNSATURATED; EICOSANOIDS; FEMALE; FISH OILS; GENOTYPE; HYDROXYEICOSATETRAENOIC ACIDS; MEMBRANE PROTEINS; MICE; MICE, INBRED STRAINS;

MUS;

EID: 84863999409     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2011.05.003     Document Type: Article

References (66)

1. Ishikawa T.O., Herschman H.R. Tumor formation in a mouse model of colitis-associated colon cancer does not require COX-1 or COX-2 expression. Carcinogenesis 2010, 31:729-736.
2. Nakanishi M., Montrose D.C., Clark P., Nambiar P.R., Belinsky G.S., Claffey K.P., et al. Genetic deletion of mPGES-1 suppresses intestinal tumorigenesis. Cancer Res 2008, 68:3251-3259.
3. McLean M.H., Murray G.I., Fyfe N., Hold G.L., Mowat N.A.G., El-Omar E.M. COX-2 expression in sporadic colorectal adenomatous polyps is linked to adenoma characteristics. Histopathology 2008, 52:806-815.
4. Pugh S., Thomas G.A. Patients with adenomatous polyps and carcinomas have increased colonic mucosal prostaglandin E2. Gut 1994, 35:675-678.
5. Giardiello F.M., Spannhake E.W., Dubois R.N., Hylind L.M., Robinson C.R., Hubbard W.C., et al. Prostaglandin levels in human colorectal mucosa - effects of sulindac in patients with familial adenomatous polyposis. Digest Dis Sci 1998, 43:311-316.
6. Shureiqi I., Wojno K.J., Poore J.A., Reddy R.G., Moussalli M.J., Spindler S.A., et al. Decreased 13-S-hydroxyoctadecadienoic acid levels and 15-lipoxygenase-1 expression in human colon cancers. Carcinogenesis 1999, 20:1985-1995.
7. Magnusson C., Ehrnstrom R., Olsen J., Sjolander A. An increased expression of cysteinyl leukotriene 2 receptor in colorectal adenocarcinomas correlates with high differentiation. Cancer Res 2007, 67:9190-9198.
8. Shureiqi I., Chen D.N., Day R.S., Zuo X.S., Hochman F.L., Ross W.A., et al. Profiling lipoxygenase metabolism in specific steps of colorectal tumorigenesis. Cancer Prev Res 2010, 3:829-838.
9. Vonkeman H.E., van de Laar M. Nonsteroidal anti-inflammatory drugs: adverse effects and their prevention. Semin Arthritis Rheum 2010, 39:294-312.
10. Moonen H., Dommels Y., van Zwam M., van Herwijnen M., Kleinjans J., Alink G., et al. Effects of polyunsaturated fatty acids on prostaglandin synthesis and cyclooxygenase-mediated DNA adduct formation by heterocyclic aromatic amines in human adenocarcinoma colon cells. Mol Carcinog 2004, 40:180-188.
11. Nieves D., Moreno J.J. Effect of arachidonic and eicosapentaenoic acid metabolism on RAW 264.7 macrophage proliferation. J Cell Physiol 2006, 208:428-434.
12. Strasser T., Fischer S., Weber P.C. Leukotriene-B5 is formed in human-neutrophils after dietary supplementation with eicosapentaenoic acid. Proc Natl Acad Sci USA 1985, 82:1540-1543.
13. 3 from eicosapentaenoic acid in human lung cancer cells. J Lipid Res 2004, 45:1030-1039.
14. Wada M., DeLong C.J., Hong Y.H., Rieke C.J., Song I., Sidhu R.S., et al. Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J Biol Chem 2007, 282:22254-22266.
15. Bagga D., Wang L., Farias-Eisner R., Glaspy J.A., Reddy S.T. Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc Natl Acad Sci USA 2003, 100:1751-1756.
16. Nkondjock A., Shatenstein B., Maisonneuve P., Ghadirian P. Specific fatty acids and human colorectal cancer: an overview. Cancer Detect Prev 2003, 27:55-66.
17. Bartsch H., Nair J., Owen R.W. Dietary polyunsaturated fatty acids and cancers of the breast and colorectum: emerging evidence for their role as risk modifiers. Carcinogenesis 1999, 20:2209-2218.
18. Chapkin R.S., McMurray D.N., Lupton J.R. Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroen 2007, 23:48-54.
19. Calviello G., Serini S., Piccioni E. n-3 polyunsaturated fatty acids and the prevention of colorectal cancer: Molecular mechanisms involved. Curr Med Chem 2007, 14:3059-3069.
20. Broughton K.S., Wade J.W. Total fat and (n-3):(n-6) fat ratios influence eicosanoid production in mice. J Nutr 2002, 132:88-94.
21. Anti M., Armelao F., Marra G., Percesepe A., Bartoli G.M., Palozza P., et al. Effects of different doses of fish-oil on rectal cell-proliferation in patients with sporadic colonic adenomas. Gastroenterology 1994, 107:1709-1718.
22. Anti M., Marra G., Armelao F., Bartoli G.M., Ficarelli R., Percesepe A., et al. Effect of omega-3-fatty-acids on rectal mucosal cell-proliferation in subjects at risk for colon cancer. Gastroenterology 1992, 103:883-891.
23. Huang Y.C., Jessup J.M., Forse R.A., Flickner S., Pleskow D. Anastopoulos HT, et al. n-3 Fatty acids decrease colonic epithelial cell proliferation in high-risk bowel mucosa. Lipids 1996, 31:S313-S317.
24. 2 release in healthy-subjects. Gastroenterology 1993, 105:1317-1322.
25. 3. Carcinogenesis 2008, 29:790-796.
26. Al-Salihi M.A., Terrece Pearman A., Doan T., Reichert E.C., Rosenberg D.W., Prescott S.M., et al. Transgenic expression of cyclooxygenase-2 in mouse intestine epithelium is insufficient to initiate tumorigenesis but promotes tumor progression. Cancer Lett 2009, 273:225-232.
27. Oshima M., Dinchuk J.E., Kargman S.L., Oshima H., Hancock B., Kwong E., et al. Suppression of intestinal polyposis in Apc-716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996, 87:803-809.
28. Djuric Z., Ren J.W., Blythe J., VanLoon G., Sen A. A Mediterranean dietary intervention in healthy American women changes plasma carotenoids and fatty acids in distinct clusters. Nutr Res 2009, 29:156-163.
29. Stark K.D. The percentage of n-3 highly unsaturated fatty acids in total HUFA as a biomarker for omega-3 fatty acid status in tissues. Lipids 2008, 43:45-53.
30. Wu Y., Fang B., Yang X.Q., Wang L., Chen D., Krasnykh V., et al. Therapeutic molecular targeting of 15-lipoxygenase-1 in colon cancer. Mol Ther 2008, 16:886-892.
31. Shureiqi I., Jiang W., Zuo X.S., Wu Y.Q., Stimmel J.B., Leesnitzer L.M., et al. The 15-lipoxygenase-1 product 13-S-hydroxyoctadecadienoic acid down-regulates PPAR-delta to induce apoptosis in colorectal cancer cells. Proc Natl Acad Sci USA 2003, 100:9968-9973.
32. Yuri M., Sasahira T., Nakai K., Ishimaru S., Ohmori H., Kuniyasu H. Reversal of expression of 15-lipoxygenase-1 to cyclooxygenase-2 is associated with development of colonic cancer. Histopathology 2007, 51:520-527.
33. Melstrom L.G., Bentrem D.J., Salabat M.R., Kennedy T.J., Ding X.Z., Strouch M., et al. Overexpression of 5-lipoxygenase in colon polyps and cancer and the effect of 5-LOX inhibitors in vitro and in a murine model. Clin Cancer Res 2008, 14:6525-6530.
34. Kennedy T.J., Talamonti M., Ujiki M., Ding X.Z., Ternent C.A., Bell R.H., et al. Lipoxygenase expression in colon polyps and inhibition of colon cancer growth by lipoxygenase blockade. J Am Coll Surg 2004, 199:S78.
35. Merchant N., Chung D.H., Townsend C.M., Heslin M.J. Tumor-associated down-regulation of 15-lipoxygenase-1 is reversed by celecoxib in colorectal cancer - Discussion. Ann Surg 2005, 241:946-947.
36. Dommels Y.E.M., Haring M.M.G., Keestra N.G.M., Alink G.M., van Bladeren P.J., van Ommen B. The role of cyclooxygenase in n-6 and n-3 polyunsaturated fatty acid mediated effects on cell proliferation, PGE(2) synthesis and cytotoxicity in human colorectal carcinoma cell lines. Carcinogenesis 2003, 24:385-392.
37. Qiao L., Kozoni V., Tsioulias G.J., Koutsos M.I., Hanif R., Shiff S.J., et al. Selected eicosanoids increase the proliferation rate of human colon carcinoma cell lines and mouse colonocytes in vivo. BBA-Lipid Lipid Met 1995, 1258:215-223.
38. Strater J., Koretz K., Gunthert A.R., Moller P. In-situ detection of enterocytic apoptosis in normal colonic mucosa and in familial adenomatous polyposis. Gut 1995, 37:819-825.
39. Risio M., Lipkin M., Newmark H., Yang K., Rossini F.P., Steele V.E., et al. Apoptosis, cell replication, and Western-style diet-induced tumorigenesis in mouse colon. Cancer Res 1996, 56:4910-4916.
40. Courtney E., Matthews S., Finlayson C., Di Pierro D., Belluzzi A., Roda E., et al. Eicosapentaenoic acid (EPA) reduces crypt cell proliferation and increases apoptosis in normal colonic mucosa in subjects with a history of colorectal adenomas. Int J Colorectal Dis 2007, 22:765-776.
41. Vijay-Kumar M., Vanegas S.M., Patel N., Aitken J.D., Ziegler T.R., Ganji V. Fish oil rich diet in comparison to saturated fat rich diet offered protection against lipopolysaccharide-induced inflammation and insulin resistance in mice (research). Nutr Metab 2011, 8:16.
42. Baltgalvis K.A., Berger F.G., Peña M.M.O., Davis J.M., Carson J.A. The interaction of a high-fat diet and regular moderate intensity exercise on intestinal polyp development in ApcMin/+ mice. Cancer Prev Res 2009, 2:641-649.
43. Sandee D., Sivanuntakorn S., Vichai V., Kramyu J., Kirtikara K. Up-regulation of microsomal prostaglandin E synthase-1 in COX-1 and COX-2 knock-out mouse fibroblast cell lines. Prostag Oth Lipid M 2009, 88:111-116.
44. Zhang J., Goorha S., Raghow R., Ballou L.R. The tissue-specific, compensatory expression of cyclooxygenase-1 and -2 in transgenic mice. Prostag Oth Lipid M 2002, 67:121-135.
45. Kirtikara K., Morham S.G., Raghow R., Laulederkind S.J.F., Kanekura T., Goorha S., et al. Compensatory prostaglandin E-2 biosynthesis in cyclooxygenase 1 or 2 null cells. J Exp Med 1998, 187:517-523.
46. Zijlstra F.J., Vandijk A.P.M., Garrelds I.M., Ouwendijk R.J.T., Wilson J.H.P. Species-differences in the pattern of eicosanoids produced by inflamed and noninflamed tissue. Agents Actions 1992, C73-C75.
47. Zijlstra F.J., Wilson J.H.P. 15-HETE is the main eicosanoid present in mucus of ulcerative proctocolitis. Prostag Leukotr Ess 1991, 43:55-59.
48. Zijlstra F.J., Vandijk A.P.M., Wilson J.H.P., Vanriemsdijkoverbeeke I.C., Vincent J.E., Ouwendijk R.J.T. 15-HETE is the main eicosanoid formed by human colonic mucosa. Agents Actions 1992, C53-C59.
49. Zijlstra F.J., Vandijk A.P.M., Ouwendijk R.J.T., Vanriemsdijkoverbeeke I.C., Wilson J.H.P. Eicosanoid production by the mucosa in inflammatory bowel-disease after 5-ASA treatment. Agents Actions 1993, 38:C122-C124.
50. Brash A.R. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 1999, 274:23679-23682.
51. Funk C.D., Chen X.S., Johnson E.N., Zhao L. Lipoxygenase genes and their targeted disruption. Prostag Oth Lipid M 2002, 68-69:303-312.
52. Lipkin M., Uehara K., Winawer S., Sanchez A., Bauer C., Phillips R., et al. 7th-Day Adventist vegetarians have a quiescent proliferative activity in colonic mucosa. Cancer Lett 1985, 26:139-144.
53. McTiernan A., Yasui Y., Sorensen B., Irwin M.L., Morgan A., Rudolph R.E., et al. Effect of a 12-month exercise intervention on patterns of cellular proliferation in colonic crypts: a randomized controlled trial. Cancer Epidem Biomar 2006, 15:1588-1597.
54. Hong M.Y., Turner N.D., Carroll R.J., Chapkin R.S., Lupton J.R. Differential response to DNA damage may explain different cancer susceptibility between small and large intestine. Exp Biol Med 2005, 230:464-471.
55. Barnes C.J., Lee M., Hardman W.E., Cameron I.L. Aspirin suppresses 1,2-dimethylhydrazine-induced alteration of proliferative parameters in rat colonic crypts. Cell Proliferat 1996, 29:467-473.
56. Dirks P., Freeman H.J. Effects of differing purified cellulose, pectin and hemicellulose fiber diets on mucosal morphology in the rat small and large-intestine. Clin Invest Med 1987, 10:32-38.
57. Heitman D.W., Ord V.A., Hunter K.E., Cameron I.L. Effect of dietary cellulose on cell-proliferation and progression of 1,2-dimethylhydrazine-induced colon carcinogenesis in rats. Cancer Res 1989, 49:5581-5585.
58. Salim E.I., Wanibuchi H., Morimura K., Murai T., Makino S., Nomura T., et al. Induction of tumors in the colon and liver of the immunodeficient (SCID) mouse by 2-amino-3-methylimidazo 4,5-f quinoline (IQ) - modulation by long-chain fatty acids. Carcinogenesis 2002, 23:1519-1529.
59. Torzsas T.L., Kendall C.W.C., Sugano M., Iwamoto Y., Rao A.V. The influence of high and low molecular weight chitosan on colonic cell proliferation and aberrant crypt foci development in CF1 mice. Food Chem Toxicol 1996, 34:73-77.
60. Lee D.Y.K., Lupton J.R., Aukema H.M., Chapkin R.S. Dietary fat and fiber alter rat colonic mucosal lipid mediators and cell proliferation. J Nutr 1993, 123:1808-1817.
61. Reuter B.K., Asfaha S., Buret A., Sharkey K.A., Wallace J.L. Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2. J Clin Invest 1996, 98:2076-2085.
62. Morteau O., Morham S.G., Sellon R., Dieleman L.A., Langenbach R., Smithies O., et al. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J Clin Invest 2000, 105:469-478.
63. Guslandi M. Exacerbation of inflammatory bowel disease by nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 inhibitors: fact or fiction?. World J Gastroenterol 2006, 12:1509-1510.
64. 2 and cysteinyl leukotriene concentrations in sputum: association with asthma severity and eosinophilic inflammation. Clin Exp Allergy 2010, 40:85-93.
65. 2 on allergen-induced airway responses and airway inflammation. Am J Resp Crit Care 1999, 159:31-36.
66. Kawamori T., Rao C.V., Seibert K., Reddy B.S. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res 1998, 58:409-412.