Attenuation of mycotoxin-induced IgA nephropathy by eicosapentaenoic acid in the mouse: dose response and relation to IL-6 expression

Journal of Nutritional Biochemistry

Volumn 17, Issue 10, 2006, Pages 697-706

  Shi, Yuhui ^a,b   Pestka, James J ^a,b,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

Deoxynivalenol (DON); Fish oil; IgA nephropathy; Interleukin 6; n 3 PUFA

Indexed keywords

ARACHIDONIC ACID; BIOLOGICAL MARKER; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN A; INTERLEUKIN 6; MESSENGER RNA; MYCOTOXIN; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; TRANSCRIPTION FACTOR AP 1; VOMITOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; BINDING AFFINITY; BIOACCUMULATION; CELL CULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DIET; DRUG EFFICACY; FEEDING; FEMALE; FOOD INTAKE; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN A NEPHROPATHY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; INHIBITION KINETICS; MEDICAL ASSESSMENT; MESANGIUM CELL; MOUSE; NONHUMAN; PEYER PATCH; SPLEEN; TREATMENT OUTCOME; WEIGHT GAIN;

ANIMALS; ARACHIDONIC ACID; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; EICOSAPENTAENOIC ACID; FATTY ACIDS, UNSATURATED; FEMALE; GENE EXPRESSION; GLOMERULAR MESANGIUM; GLOMERULONEPHRITIS, IGA; IMMUNOGLOBULIN A; INTERLEUKIN-6; MICE; PHOSPHOLIPIDS; RNA, MESSENGER; SPLEEN; TRICHOTHECENES;

EID: 33748627704     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2005.12.002     Document Type: Article

References (59)

1. Feehally J. IgA nephropathy - a disorder of IgA production?. QJM 90 (1997) 387-390
2. Hunley T.E., and Kon V. IgA nephropathy. Curr Opin Pediatr 11 (1999) 152-157
3. Emancipator S.N., and Lamm M.E. IgA nephropathy: pathogenesis of the most common form of glomerulonephritis. Lab Invest 60 (1989) 168-183
4. Hellegers D. IgA nephropathy. Partn Prev (1993) 10
5. Donadio Jr. J.V., Grande J.P., Bergstralh E.J., Dart R.A., Larson T.S., and Spencer D.C. The long-term outcome of patients with IgA nephropathy treated with fish oil in a controlled trial. Mayo Nephrology Collaborative Group. J Am Soc Nephrol 10 (1999) 1772-1777
6. Harper S.J., Allen A.C., Pringle J.H., and Feehally J. Increased dimeric IgA producing B cells in the bone marrow in IgA nephropathy determined by in situ hybridisation for J chain mRNA. J Clin Pathol 49 (1996) 38-42
7. Montinaro V., Gesualdo L., and Schena F.P. The relevance of experimental models in the pathogenetic investigation of primary IgA nephropathy. Ann Med Interne (Paris) 150 (1999) 99-107
8. Calder P.C. N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38 (2003) 343-352
9. Gil A. Polyunsaturated fatty acids and inflammatory diseases. Biomed Pharmacother 56 (2002) 388-396
10. Calder P.C. Polyunsaturated fatty acids and inflammation. Biochem Soc Trans 33 (2005) 423-427
11. Wakai K., Kawamura T., Matsuo S., Hotta N., and Ohno Y. Risk factors for IgA nephropathy: a case-control study in Japan. Am J Kidney Dis 33 (1999) 738-745
12. Wakai K., Nakai S., Matsuo S., Kawamura T., Hotta N., Maeda K., et al. Risk factors for IgA nephropathy: a case-control study with incident cases in Japan. Nephron 90 (2002) 16-23
13. Holman R.T., Johnson S.B., Bibus D., Spencer D.C., and Donadio Jr. J.V. Essential fatty acid deficiency profiles in idiopathic immunoglobulin A nephropathy. Am J Kidney Dis 23 (1994) 648-654
14. Donadio J.V., and Grande J.P. The role of fish oil/omega-3 fatty acids in the treatment of IgA nephropathy. Semin Nephrol 24 (2004) 225-243
15. Pestka J.J., and Smolinski A.T. Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health B Crit Rev 8 (2005) 39-69
16. Pestka J.J., Moorman M.A., and Warner R.L. Dysregulation of IgA production and IgA nephropathy induced by the trichothecene vomitoxin. Food Chem Toxicol 27 (1989) 361-368
17. Dong W., and Pestka J.J. Persistent dysregulation of IgA production and IgA nephropathy in the B6C3F1 mouse following withdrawal of dietary vomitoxin (deoxynivalenol). Fundam Appl Toxicol 20 (1993) 38-47
18. Dong W., Sell J.E., and Pestka J.J. Quantitative assessment of mesangial immunoglobulin A (IgA) accumulation, elevated circulating IgA immune complexes, and hematuria during vomitoxin-induced IgA nephropathy. Fundam Appl Toxicol 17 (1991) 197-207
19. Beagley K.W., Eldridge J.H., Lee F., Kiyono H., Everson M.P., Koopman W.J., et al. Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J Exp Med 169 (1989) 2133-2148
20. Yan D., Zhou H.R., Brooks K.H., and Pestka J.J. Role of macrophages in elevated IgA and IL-6 production by Peyer's patch cultures following acute oral vomitoxin exposure. Toxicol Appl Pharmacol 148 (1998) 261-273
21. Yan D., Zhou H.R., Brooks K.H., and Pestka J.J. Potential role for IL-5 and IL-6 in enhanced IgA secretion by Peyer's patch cells isolated from mice acutely exposed to vomitoxin. Toxicology 122 (1997) 145-158
22. Pestka J.J., and Zhou H.R. Interleukin-6-deficient mice refractory to IgA dysregulation but not anorexia induction by vomitoxin (deoxynivalenol) ingestion. Food Chem Toxicol 38 (2000) 565-575
23. Pestka J.J., Zhou H.R., Jia Q., and Timmer A.M. Dietary fish oil suppresses experimental immunoglobulin a nephropathy in mice. J Nutr 132 (2002) 261-269
24. Jia Q., Shi Y., Bennink M.B., and Pestka J.J. Docosahexaenoic acid and eicosapentaenoic acid, but not alpha-linolenic acid, suppress deoxynivalenol-induced experimental IgA nephropathy in mice. J Nutr 134 (2004) 1353-1361
25. Jia Q., Zhou H.R., Bennink M., and Pestka J.J. Docosahexaenoic acid attenuates mycotoxin-induced immunoglobulin a nephropathy, interleukin-6 transcription, and mitogen-activated protein kinase phosphorylation in mice. J Nutr 134 (2004) 3343-3349
26. Seo T., Blaner W.S., and Deckelbaum R.J. Omega-3 fatty acids: molecular approaches to optimal biological outcomes. Curr Opin Lipidol 16 (2005) 11-18
27. Yusufi A.N., Cheng J., Thompson M.A., Walker H.J., Gray C.E., Warner G.M., et al. Differential effects of low-dose docosahexaenoic acid and eicosapentaenoic acid on the regulation of mitogenic signaling pathways in mesangial cells. J Lab Clin Med 141 (2003) 318-329
28. Obajimi O., Black K.D., Macdonald D.J., Boyle R.M., Glen I., and Ross B.M. Differential effects of eicosapentaenoic and docosahexaenoic acids upon oxidant-stimulated release and uptake of arachidonic acid in human lymphoma U937 cells. Pharmacol Res 52 (2005) 183-191
29. Egashira Y., Murotani G., Tanabe A., Saito K., Uehara K., Morise A., et al. Differential effects of dietary fatty acids on rat liver alpha-amino-beta-carboxymuconate-epsilon-semialdehyde decarboxylase activity and gene expression. Biochim Biophys Acta 1686 (2004) 118-124
30. Woodman R.J., Mori T.A., Burke V., Puddey I.B., Barden A., Watts G.F., et al. Effects of purified eicosapentaenoic acid and docosahexaenoic acid on platelet, fibrinolytic and vascular function in hypertensive type 2 diabetic patients. Atherosclerosis 166 (2003) 85-93
31. Leigh-Firbank E.C., Minihane A.M., Leake D.S., Wright J.W., Murphy M.C., Griffin B.A., et al. Eicosapentaenoic acid and docosahexaenoic acid from fish oils: differential associations with lipid responses. Br J Nutr 87 (2002) 435-445
32. Clifford L.J., Jia Q., and Pestka J.J. An improved method for the purification of the trichothecene deoxynivalenol (vomitoxin) from Fusarium graminearum culture. J Agric Food Chem 51 (2003) 521-523
33. Thompson W.L., and Wannemacher Jr. R.W. Structure-function relationships of 12,13-epoxytrichothecene mycotoxins in cell culture: comparison to whole animal lethality. Toxicon 24 (1986) 985-994
34. Reeves P.G., Nielsen F.H., and Fahey Jr. G.C. 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 (1993) 1939-1951
35. Pestka J.J. Deoxynivalenol-induced IgA production and IgA nephropathy-aberrant mucosal immune response with systemic repercussions. Toxicol Lett 140-1 (2003) 287-295
36. Zhou H.R., Jia Q., and Pestka J.J. Ribotoxic stress response to the trichothecene deoxynivalenol in the macrophage involves the SRC family kinase Hck. Toxicol Sci 85 (2005) 916-926
37. Hasler C.M., Trosko J.E., and Bennink M.R. Incorporation of n-3 fatty acids into WB-F344 cell phospholipids inhibits gap junctional intercellular communication. Lipids 26 (1991) 788-792
38. Zhou H.R., Islam Z., and Pestka J.J. Rapid, sequential activation of mitogen-activated protein kinases and transcription factors precedes proinflammatory cytokine mRNA expression in spleens of mice exposed to the trichothecene vomitoxin. Toxicol Sci 72 (2003) 130-142
39. Barratt J., Feehally J., and Smith A.C. Pathogenesis of IgA nephropathy. Semin Nephrol 24 (2004) 197-217
40. Fyfe D.J., and Abbey M. Effects of n-3 fatty acids on growth and survival of J774 macrophages. Prostaglandins Leukot Essent Fatty Acids 62 (2000) 201-207
41. Kanayasu-Toyoda T., Morita I., Hibino H., Nakao-Hayashi J., Ito H., and Murota S. Eicosapentaenoic acid abolishes the proatherogenic effects of cholesterol: effects on migration of bovine smooth muscle and endothelial cells in vitro. Prostaglandins Leukot Essent Fatty Acids 48 (1993) 463-468
42. Rasooly L., and Pestka J.J. Polyclonal autoreactive IgA increase and mesangial deposition during vomitoxin-induced IgA nephropathy in the BALB/c mouse. Food Chem Toxicol 32 (1994) 329-336
43. Rasooly L., Abouzied M.M., Brooks K.H., and Pestka J.J. Polyspecific and autoreactive IgA secreted by hybridomas derived from Peyer's patches of vomitoxin-fed mice: characterization and possible pathogenic role in IgA nephropathy. Food Chem Toxicol 32 (1994) 337-348
44. Zhou H.R., Yan D., and Pestka J.J. Differential cytokine mRNA expression in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): dose response and time course. Toxicol Appl Pharmacol 144 (1997) 294-305
45. Wong S.S., Zhou H.R., Marin-Martinez M.L., Brooks K., and Pestka J.J. Modulation of IL-1beta, IL-6 and TNF-alpha secretion and mRNA expression by the trichothecene vomitoxin in the RAW 264.7 murine macrophage cell line. Food Chem Toxicol 36 (1998) 409-419
46. Kanda T., and Takahashi T. Interleukin-6 and cardiovascular diseases. Jpn Heart J 45 (2004) 183-193
47. Elferink C.J., and Reiners Jr. J.J. Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 20 (1996) 470-477
48. Dendorfer U., Oettgen P., and Libermann T.A. Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol Cell Biol 14 (1994) 4443-4454
49. Tokunou T., Ichiki T., Takeda K., Funakoshi Y., Iino N., Shimokawa H., et al. Thrombin induces interleukin-6 expression through the cAMP response element in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 21 (2001) 1759-1763
50. Moon Y., Uzarski R., and Pestka J.J. Relationship of trichothecene structure to COX-2 induction in the macrophage: selective action of type B (8-keto) trichothecenes. J Toxicol Environ Health A 66 (2003) 1967-1983
51. Moon Y., and Pestka J.J. Cyclooxygenase-2 mediates interleukin-6 upregulation by vomitoxin (deoxynivalenol) in vitro and in vivo. Toxicol Appl Pharmacol 187 (2003) 80-88
52. Moon Y., and Pestka J.J. Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen-activated protein kinases. Toxicol Sci 69 (2002) 373-382
53. Moyad M.A. An introduction to dietary/supplemental omega-3 fatty acids for general health and prevention: Part II. Urol Oncol 23 (2005) 36-48
54. Moon Y., and Pestka J.J. Deoxynivalenol-induced mitogen-activated protein kinase phosphorylation and IL-6 expression in mice suppressed by fish oil. J Nutr Biochem 14 (2003) 717-726
55. Trebble T., Arden N.K., Stroud M.A., Wootton S.A., Burdge G.C., Miles E.A., et al. Inhibition of tumour necrosis factor-alpha and interleukin 6 production by mononuclear cells following dietary fish-oil supplementation in healthy men and response to antioxidant co-supplementation. Br J Nutr 90 (2003) 405-412
56. Wallace F.A., Miles E.A., and Calder P.C. Comparison of the effects of linseed oil and different doses of fish oil on mononuclear cell function in healthy human subjects. Br J Nutr 89 (2003) 679-689
57. Taniguchi Y., Yorioka N., Oda H., and Yamakido M. Platelet-derived growth factor, interleukin (IL)-1 beta, IL-6R and tumor necrosis factor-alpha in IgA nephropathy. An immunohistochemical study. Nephron 74 (1996) 652-660
58. Bagheri N., Chintalacharuvu S.R., and Emancipator S.N. Proinflammatory cytokines regulate Fc alphaR expression by human mesangial cells in vitro. Clin Exp Immunol 107 (1997) 404-409
59. Donadio J.V., and Grande J.P. IgA nephropathy. N Engl J Med 347 (2002) 738-748