Dietary fish oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of inflammatory colitis

Cancer Research

Volumn 70, Issue 20, 2010, Pages 7960-7969

  Woodworth, Hillary L ^a   McCaskey, Sarah J ^a   Duriancik, David M ^a   Clinthorne, Jonathan F ^a   Langohr, Ingeborg M ^b   Gardner, Elizabeth M ^b   Fenton, Jenifer I ^a,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CORN OIL; DOCOSAHEXAENOIC ACID; FISH OIL; L SELECTIN; SAFFLOWER OIL; TRANSCRIPTION FACTOR FOXP3;

ADENOCARCINOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANCER RISK; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLITIS; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; DIET; DIET SUPPLEMENTATION; DIETARY INTAKE; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; FLOW CYTOMETRY; HELICOBACTER HEPATICUS; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COLITIS; COLON; COLONIC NEOPLASMS; CORN OIL; DIETARY FATS, UNSATURATED; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; FISH OILS; FLOW CYTOMETRY; INFLAMMATION; LECTINS, C-TYPE; MICE; MICE, KNOCKOUT; RECTUM; SMAD3 PROTEIN; T-LYMPHOCYTES;

EID: 78049287658     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1396     Document Type: Article

References (55)

1. Breynaert C, Vermeire S, Rutgeerts P, Van Assche G. Dysplasia and colorectal cancer in inflammatory bowel disease: a result of inflammation or an intrinsic risk? Acta Gastroenterol Belg 2008;71:367-72.
2. Xu Y, Pasche B. TGF-β signaling alterations and susceptibility to colorectal cancer. Hum Mol Genet 2007;16 Spec No 1:R14-20.
3. van Schaik FD, Offerhaus GJ, Schipper ME, Siersema PD, Vleggaar FP, Oldenburg B. Endoscopic and pathological aspects of colitis-associated dysplasia. Nat Rev Gastroenterol Hepatol 2009;6:671-8.
4. Tweedle EM, Chaudhri S, Azadeh B, Rooney PS. Small, flat colorectal cancers in the UK population: an analysis of resected specimens. Colorectal Dis 2007;9:641-6. (Pubitemid 47261831)
5. Nasir A, Boulware D, Kaiser HE, et al. Flat and polypoid adenocarcinomas of the colorectum: a comparative histomorphologic analysis of 47 cases. Hum Pathol 2004;35:604-11. (Pubitemid 38656946)
6. Hudert CA, Weylandt KH, Lu Y, et al. Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc Natl Acad Sci U S A 2006;103:11276-81. (Pubitemid 44156509)
7. Lee KM. Nutrition in inflammatory bowel disease. Korean J Gastroenterol 2008;52:1-8.
8. Meister D, Bode J, Shand A, Ghosh S. Anti-inflammatory effects of enteral diet components on Crohn's disease-affected tissues in vitro. Dig Liver Dis 2002;34:430-8. (Pubitemid 34679066)
9. Meister D, Ghosh S. Effect of fish oil enriched enteral diet on inflammatory bowel disease tissues in organ culture: differential effects on ulcerative colitis and Crohn's disease. World J Gastroenterol 2005;11:7466-72. (Pubitemid 43126028)
10. Nowak J, Weylandt KH, Habbel P, et al. Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n-3 fatty acids. Carcinogenesis 2007;28:1991-5. (Pubitemid 47500613)
11. Gibney MJ, Hunter B. The effects of short- and long-term supplementation with fish oil on the incorporation of n-3 polyunsaturated fatty acids into cells of the immune system in healthy volunteers. Eur J Clin Nutr 1993;47:255-9. (Pubitemid 23111664)
12. Endres S, Ghorbani R, Kelley VE, et al. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med 1989;320:265-71. (Pubitemid 19045549)
13. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ. The effect on human tumor necrosis factor α and interleukin 1β production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 1996;63:116-22. (Pubitemid 26005735)
14. Chapkin RS, Kim W, Lupton JR, McMurray DN. Dietary docosahexaenoic and eicosapentaenoic acid: emerging mediators of inflammation. Prostaglandins Leukot Essent Fatty Acids 2009;81:187-91.
15. Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 2003;126:1-27. (Pubitemid 37297962)
16. Kundu JK, Surh YJ. Inflammation: gearing the journey to cancer. Mutat Res 2008;659:15-30.
17. Engle SJ, Ormsby I, Pawlowski S, et al. Elimination of colon cancer in germ-free transforming growth factor β1-deficient mice. Cancer Res 2002;62:6362-6. (Pubitemid 35364086)
18. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-β in homeostasis and cancer. Nat Rev Cancer 2003;3:807-21.
19. Massague J. TGF-β signal transduction. Annu Rev Biochem 1998;67:753-91.
20. Lin Y, Martin J, Gruendler C, et al. A novel link between the proteasome pathway and the signal transduction pathway of the bone morphogenetic proteins (BMPs). BMC Cell Biol 2002;3:15. (Pubitemid 38597745)
21. Maggio-Price L, Treuting P, Zeng W, Tsang M, Bielefeldt-Ohmann H, Iritani BM. Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res 2006;66:828-38. (Pubitemid 43165948)
22. Becker C, Fantini MC, Neurath MF. TGF-β as a T cell regulator in colitis and colon cancer. Cytokine Growth Factor Rev 2006;17:97-106. (Pubitemid 43117519)
23. Sijben JW, Calder PC. Differential immunomodulation with long-chain n-3PUFAin health and chronic disease. ProcNutrSoc 2007;66:237-59.
24. Berquin IM, Edwards IJ, Chen YQ. Multi-targeted therapy of cancer by omega-3 fatty acids. Cancer Lett 2008;269:363-77.
25. Figler M, Gasztonyi B, Cseh J, et al. Association of n-3 and n-6 longchain polyunsaturated fatty acids in plasma lipid classes with inflammatory bowel diseases. Br J Nutr 2007;97:1154-61. (Pubitemid 46925368)
26. O'Sullivan M, O'Morain C. Nutrition in inflammatory bowel disease. Best Pract Res Clin Gastroenterol 2006;20:561-73.
27. Turner D, Zlotkin SH, Shah PS, Griffiths AM. Omega 3 fatty acids (fish oil) for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev 2007:CD006320.
28. Turner D, Zlotkin SH, Shah PS, Griffiths AM. Omega 3 fatty acids (fish oil) for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev 2009:CD006320.
29. Yessoufou A, Ple A, Moutairou K, Hichami A, Khan NA. Docosahexaenoic acid reduces suppressive and migratory functions of CD4+CD25+ regulatory T-cells. J Lipid Res 2009;50:2377-88.
30. Reeves PG. Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 1997;127:838-41S.
31. Shi Y, Pestka JJ. Mechanisms for suppression of interleukin-6 expression in peritoneal macrophages from docosahexaenoic acidfed mice. J Nutr Biochem 2009;20:358-68.
32. Jia Q, Zhou HR, Shi Y, Pestka JJ. Docosahexaenoic acid consumption inhibits deoxynivalenol-induced CREB/ATF1 activation and IL-6 gene transcription in mouse macrophages. J Nutr 2006;136:366-72. (Pubitemid 43228287)
33. Hasler CM, Trosko JE, Bennink MR. Incorporation of n-3 fatty acids into WB-F344 cell phospholipids inhibits gap junctional intercellular communication. Lipids 1991;26:788-92.
34. Jia Q, Shi Y, Bennink MB, Pestka JJ. Docosahexaenoic acid and eicosapentaenoic acid, but not α-linolenic acid, suppress deoxynivalenol-induced experimental IgA nephropathy in mice. J Nutr 2004;134:1353-61. (Pubitemid 38720706)
35. + regulatory T cell migration requires L-selectin expression: L-selectin transcriptional regulation balances constitutive receptor turnover. J Immunol 2007;178:291-300.
36. Leid JG, Jutila MA. Impact of polyunsaturated fatty acids on cytoskeletal linkage of L-selectin. Cell Immunol 2004;228:91-8.
37. Grailer JJ, Kodera M, Steeber DA. L-selectin: role in regulating homeostasis and cutaneous inflammation. J Dermatol Sci 2009;56:141-7.
38. Cruz-Chamorro L, Puertollano MA, Puertollano E, Alvarez de Cienfuegos G, de Pablo MA. Examination of host immune resistance against Listeria monocytogenes infection in cyclophosphamide-treated mice after dietary lipid administration. Clin Nutr 2007;26:631-9. (Pubitemid 47618328)
39. Bonilla DL, Fan YY, Chapkin RS, McMurray DN. Transgenic mice enriched in omega-3 fatty acids are more susceptible to pulmonary tuberculosis: impaired resistance to tuberculosis in fat-1 mice. J Infect Dis 201:399-408.
40. Schwerbrock NM, Karlsson EA, Shi Q, Sheridan PA, Beck MA. Fish oil-fed mice have impaired resistance to influenza infection. J Nutr 2009;139:1588-94.
41. Wendel M, Heller AR. Anticancer actions of omega-3 fatty acids - current state and future perspectives. Anticancer Agents Med Chem 2009;9:457-70.
42. Hegazi RA, Saad RS, Mady H, Matarese LE, O'Keefe S, Kandil HM. Dietary fatty acids modulate chronic colitis, colitis-associated colon neoplasia and COX-2 expression in IL-10 knockout mice. Nutrition 2006;22:275-82. (Pubitemid 43261525)
43. Chapkin RS, Davidson LA, Ly L, Weeks BR, Lupton JR, McMurray DN. Immunomodulatory effects of (n-3) fatty acids: putative link to inflammation and colon cancer. J Nutr 2007;137:200-4S.
44. Gil A. Polyunsaturated fatty acids and inflammatory diseases. Biomed Pharmacother 2002;56:388-96. (Pubitemid 35232741)
45. Matsunaga H, Hokari R, Kurihara C, et al. Omega-3 fatty acids exacerbate DSS-induced colitis through decreased adiponectin in colonic subepithelial myofibroblasts. Inflamm Bowel Dis 2008;14:1348-57.
46. + regulatory T-cells. J Lipid Res 2009;50:2377-88.
47. Gounaris E, Blatner NR, Dennis K, et al. T-regulatory cells shift from a protective anti-inflammatory to a cancer-promoting proinflammatory phenotype in polyposis. Cancer Res 2009;69:5490-7.
48. Erdman SE, Poutahidis T. Roles for inflammation and regulatory T cells in colon cancer. Toxicol Pathol 2009;38:76-87.
49. Kew S, Mesa MD, Tricon S, Buckley R, Minihane AM, Yaqoob P. Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am J Clin Nutr 2004;79:674-81. (Pubitemid 41103914)
50. Pratt JS, Sachen KL, Wood HD, Eaton KA, Young VB. Modulation of host immune responses by the cytolethal distending toxin of Helicobacter hepaticus. Infect Immun 2006;74:4496-504.
51. Smith JL, Bayles DO. The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol 2006;32:227-48.
52. Ohara M, Hayashi T, Kusunoki Y, Miyauchi M, Takata T, Sugai M. Caspase-2 and caspase-7 are involved in cytolethal distending toxin-induced apoptosis in Jurkat and MOLT-4 T-cell lines. Infect Immun 2004;72:871-9. (Pubitemid 38166666)
53. + T cells. Microbes Infect 2004;6:1171-81.
54. Zhang P, Smith R, Chapkin RS, McMurray DN. Dietary (n-3) polyunsaturated fatty acids modulate murine Th1/Th2 balance toward the Th2 pole by suppression of Th1 development. J Nutr 2005;135:1745-51. (Pubitemid 40980728)
55. Harris WS, Mozaffarian D, Lefevre M, et al. Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J Nutr 2009;139:804-19S.