Influence of deoxynivalenol on NF-κB activation and IL-8 secretion in human intestinal Caco-2 cells

Toxicology Letters

Volumn 177, Issue 3, 2008, Pages 205-214

  Van De Walle, Jacqueline ^a   Romier, Béatrice ^a   Larondelle, Yvan ^a   Schneider, Yves Jacques ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Caco 2 cells; Deoxynivalenol; Il 8 secretion; Intestinal inflammation; NF B I B pathway

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; VOMITOXIN;

ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DISEASE EXACERBATION; DOSE RESPONSE; ENTERITIS; HUMAN; HUMAN CELL; HYPOTHESIS; INTESTINE CELL; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; PRIORITY JOURNAL;

CACO-2 CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTERITIS; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-1BETA; INTERLEUKIN-8; NF-KAPPA B; PHOSPHORYLATION; TRICHOTHECENES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 40849116036     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2008.01.018     Document Type: Article

References (65)

1. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with image. J. Biophot. Int. 11 (2004) 36-42
2. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 75 (2004) 639-653
3. Azcona-Olivera J.I., Ouyang Y.L., Warner R.L., Linz J.E., and Pestka J.J. Effects of vomitoxin (deoxynivalenol) and cycloheximide on IL-2,4, 5 and 6 secretion and mRNA levels in murine CD4+ cells. Food Chem. Toxicol. 33 (1995) 433-441
4. Bony S., Carcelen M., Olivier L., and Devaux A. Genotoxicity assessment of deoxynivalenol in the Caco-2 cell line model using the Comet assay. Toxicol. Lett. 166 (2006) 67-76
5. Caradonna L., Amati L., Magrone T., Pellegrino N.M., Jirillo E., and Caccavo D. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J. Endotoxin Res. 6 (2000) 205-214
6. Dong W., Azcona-Olivera J.I., Brooks K.H., Linz J.E., and Pestka J.J. Elevated gene expression and production of interleukins 2,4, 5 and 6 during exposure to vomitoxin (deoxynivalenol) and cycloheximide in the EL-4 thymoma. Toxicol. Appl. Pharmacol. 127 (1994) 282-290
7. EC, 2003. Collection of Occurrence Data of Fusarium Toxins in Food and Assessment of Dietary Intake by the Population of EU Member States, European Commission: Health and Consumers Protection Directorate-General, Brussels, Belgium, pp. 1-606.
8. Fornelli F., Minervini F., and Mule G. Cytotoxicity induced by nivalenol, deoxynivalenol, and fumonisin B1 in the SF-9 insect cell line. In Vitro Cell Dev. Biol. Anim. 40 (2004) 166-171
9. Gouze M.E., Laffitte J., Rouimi P., Loiseau N., Oswald I.P., and Galtier P. Effect of various doses of deoxynivalenol on liver xenobiotic metabolizing enzymes in mice. Food Chem. Toxicol. 44 (2006) 476-483
10. Goyarts T., Dänicke S., Tiemann U., and Rothkötter H.J. Effect of the Fusarium toxin deoxynivalenol (DON) on IgA, IgM and IgG concentrations and proliferation of porcine blood lymphocytes. Toxicol. In Vitro 20 (2006) 858-867
11. Halleux C., and Schneider Y.J. Iron absorption by intestinal epithelial cells. 1. Caco-2 cells cultivated in serum-free medium, on polyethylene terephtalate microporous membranes, as an in vitro model. In Vitro Cell Dev. Biol. 27A (1991) 293-302
12. Hanai H. Positions of selective leukocytapheresis in the medical therapy of ulcerative colitis. World J. Gastroenterol. 12 (2006) 7568-7577
13. Hershko D.D., Robb B.W., Wray C.J., Luo G.J., and Hasselgren P.O. Superinduction of IL-6 by cycloheximide is associated with mRNA stabilization and sustained activation of p38 map kinase and NF-kappaB in cultured caco-2 cells. J. Cell Biochem. 91 (2004) 951-961
14. Hoffmann E., Dittrich-Breiholz O., Holtmann H., and Kracht M. Multiple control of interleukin-8 gene expression. J. Leukocyte Biol. 72 (2002) 847-855
15. Hollenbach E., Neumann M., Vieth M., Roessner A., Malfertheiner P., and Naumann M. Inhibition of p38 MAP kinase- and RICK/NF-kappaB-signaling suppresses inflammatory bowel disease. FASEB J. 18 (2004) 1550-1552
16. Instanes C., and Hetland G. Deoxynivalenol (DON) is toxic to human colonic, lung and monocytic cell lines, but does not increase the IgE response in a mouse model for allergy. Toxicology 204 (2004) 13-21
17. Islam Z., and Pestka J.J. LPS priming potentiates and prolongs proinflammatory cytokine response to the trichothecene deoxynivalenol in the mouse. Toxicol. Appl. Pharmacol. 211 (2006) 53-63
18. Islam Z., Gray J.S., and Pestka J.J. p38 Mitogen-activated protein kinase mediates IL-8 induction by the ribotoxin deoxynivalenol in human monocytes. Toxicol. Appl. Pharmacol. 213 (2006) 235-244
19. Jackson L.S., and Bullerman L.B. Effect of processing on Fusarium mycotoxins. Adv. Exp. Med. Biol. 459 (1999) 243-261
20. Ji G.E., Park S.Y., Wong S.S., and Pestka J.J. Modulation of nitric oxide, hydrogen peroxide and cytokine production in a clonal macrophage model by the trichothecene vomitoxin (deoxynivalenol). Toxicology 125 (1998) 203-214
21. Kasuga F., Hara-Kudo Y., Saito N., Kumagai S., and Sugita-Konishi Y. In vitro effect of deoxynivalenol on the differentiation of human colonic cell lines Caco-2 and T84. Mycopathologia 142 (1998) 161-167
22. Lakatos P.L. Recent trends in the epidemiology of inflammatory bowel diseases: up or down?. World J. Gastroenterol. 12 (2006) 6102-6108
23. Larsen J.C., Hunt J., Perrin I., and Ruckenbauer P. Workshop on trichothecenes with a focus on DON: summary report. Toxicol. Lett. 153 (2004) 1-22
24. Laskin J.D., Heck D.E., and Laskin D.L. The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol. Sci. 69 (2002) 289-291
25. Li S., Ouyang Y., Yang G.H., and Pestka J.J. Modulation of transcription factor AP-1 activity in murine EL-4 thymoma cells by vomitoxin (deoxynivalenol). Toxicol. Appl. Pharmacol. 163 (2000) 17-25
26. Liu S.F., and Malik A.B. NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am. J. Physiol. Lung Cell Mol. Physiol. 290 (2006) 622-645
27. Malamut G., Cabane C., Dubuquoy L., Malapel M., Dérijard B., Gay J., Tamboli C., Colombel J.F., and Desreumaux P. No evidence for an involvement of the p38 and JNK mitogen-activated protein in inflammatory bowel diseases. Dig. Dis. Sci. 51 (2006) 1443-1453
28. Maresca M., Mahfoud R., Garmy N., and Fantini J. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 132 (2002) 2723-2731
29. Matis C., Chomez P., Picard J., and Rezsohazy R. Differential and opposed transcriptional effects of protein fusions containing the VP16 activation domain. FEBS Lett. 499 (2001) 92-96
30. Meky F.A., Hardie L.J., Evans S.W., and Wild C.P. Deoxynivalenol-induced immunomodulation of human lymphocyte proliferation and cytokine production. Food Chem. Toxicol. 39 (2001) 827-836
31. Mitchell T., and Sudgen B. Stimulation of NF-κB-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J. Virol. 69 (1995) 2968-2976
32. Moon Y., Yang H., and Lee S.H. Modulation of early growth response gene 1 and interleukin-8 expression by ribotoxin deoxynivalenol (vomitoxin) via ERK1/2 in human epithelial intestine 407 cells. Biochem. Biophys. Res. Commun. 362 (2007) 256-262
33. Neuman M.G. Immune dysfunction in inflammatory bowel disease. Transl. Res. 149 (2007) 173-186
34. Ouyang Y.L., Azcona-Olivera J.I., Murtha J., and Pestka J.J. Vomitoxin-mediated IL-2, IL-4, and IL-5 superinduction in murine CD4+ T cells stimulated with phorbol ester calcium ionophore: relation to kinetics of proliferation. Toxicol. Appl. Pharmacol. 138 (1996) 324-334
35. Ouyang Y.L., Li S., and Pestka J.J. Effects of vomitoxin (deoxynivalenol) on transcription factor NF-kappa B/Rel binding activity in murine EL-4 thymoma and primary CD4+ T cells. Toxicol. Appl. Pharmacol. 140 (1996) 328-336
36. Panja A., Goldberg S., Eckmann L., Krishen P., and Mayer L. The regulation and functional consequence of proinflammatory cytokine binding on human intestinal epithelial cells. J. Immunol. 161 (1998) 3675-3684
37. 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
38. Prelusky D.B. A study on the effect of deoxynivalenol on serotonin receptor binding in pig brain membranes. J. Environ. Sci. Health B 31 (1996) 1103-1117
39. Reimund J.M., Wittersheim C., Dumont S., Muller C.D., Baumann R., Poindron P., and Duclos B. Mucosal inflammatory cytokine production by intestinal biopsies in patients with ulcerative colitis and Crohn's disease. J. Clin. Immunol. 16 (1996) 144-150
40. Romier, B., Van De Walle, J., During, A., Larondelle, Y., Schneider, Y.J., in press. Modulation of signaling NF-κB activation pathway by polyphenols in human intestinal Caco-2 cells. Br. J. Nutr.
41. Rotter B.A., Prelusky D.B., and Pestka J.J. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48 (1996) 1-34
42. Russel M.G. Changes in the incidence of inflammatory bowel disease: what does it mean?. Eur. J. Intern. Med. 11 (2000) 191-196
43. Schneider Y.J. Optimisation of hybridoma cell growth and monoclonal antibody secretion in a chemically defined serum- and protein-free culture medium. J. Immunol. Methods 116 (1989) 65-77
44. Schreiber S. Experimental immunomodulatory therapy of inflammatory bowel disease. Neth. J. Med. 53 (1998) 24-31
45. Sergent T., Parys M., Garsou S., Pussemier L., Schneider Y.J., and Larondelle Y. Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol. Lett. 164 (2006) 167-176
46. Shifrin V.I., and Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem. 274 (1999) 13985-13992
47. Sudakin D.L. Trichothecenes in the environment: relevance to human health. Toxicol. Lett. 20 (2003) 97-107
48. Sugita-Konishi Y., and Pestka J.J. Differential upregulation of TNF-alpha, IL-6, and IL-8 production by deoxynivalenol (vomitoxin) and other 8-ketotrichothecenes in a humanmacrophage model. J. Toxicol. Environ. Health A 64 (2001) 619-636
49. Sun S.C., Ganchi P.A., Ballard D.W., and Greene W.C. NF-κB expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 25 (1993) 1912-1915
50. Ten Hove T., van den Blink B., Pronk I., Drillenburg P., Peppelenbosch M.P., and van Deventer S.J. Dichotomal role of inhibition of p38 MAPK with SB 203580 in experimental colitis. Gut 50 (2002) 507-512
51. Tsatsanis C., Androulidaki A., Venihaki M., and Margioris A.N. Signalling networks regulating cyclooxygenase-2. Int. J. Biochem. Cell Biol. 38 (2006) 1654-1661
52. Turner, P.C., Burley, V.J., Rothwell, J.A., White, K.L.M., Cade, J.E., Wild, C.P., 2007. Dietary wheat reduction decreases the level of urinary deoxynivalenol in UK adults. J. Expos. Sci. Environ. Epidemiol., doi:10.1038/sj.jes.7500611.
53. Ueno Y. The toxicology of mycotoxins. Crit. Rev. Toxicol. 14 (1985) 99-132
54. Van Den Blink B., Ten Hove T., Van Den Brink G.R., Peppelenbosch M.P., and Van Deventer S.J. From extracellular to intracellular targets, inhibiting MAP kinases in treatment of Crohn's disease. Ann. NY Acad. Sci. 973 (2002) 349-358
55. Viatour P., Merville M.P., Bours V., and Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30 (2005) 43-52
56. Waetzig G.H., Seegert D., Rosenstiel P., Nikolaus S., and Schreiber S. p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J. Immunol. 168 (2002) 5342-5351
57. Warhurst A.C., Hopkins S.J., and Warhurst G. Interferon γinduces differential upregulation of α and β chemokine secretion in colonic epithelial cell lines. Gut 42 (1998) 208-213
58. Warner R.L., Brooks K., and Pestka J.J. In vitro effects of vomitoxin (deoxynivalenol) on T-cell interleukin production and IgA secretion. Food Chem. Toxicol. 32 (1994) 617-625
59. Wild G.E., Drozdowski L., Tartaglia C., Clandinin M.T., and Thomson A.B. Nutritional modulation of the inflammatory response in inflammatory bowel disease-from the molecular to the integrative to the clinical. World J. Gastroenterol. 13 (2007) 1-7
60. 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
61. Wong S., Schwartz R.C., and Pestka J.J. Superinduction of TNF-alpha and IL-6 in macrophages by vomitoxin (deoxynivalenol) modulated by mRNA stabilization. Toxicology 161 (2001) 139-149
62. Wong S.S., Zhou H.R., and Pestka J.J. Effects of vomitoxin (deoxynivalenol) on the binding of transcription factors AP-1, NF-kappaB, and NF-IL6 in raw 264.7 macrophage cells. J. Toxicol. Environ. Health A 65 (2002) 1161-1180
63. Zhou H.R., Yan D., and Pestka J.J. Induction of cytokine gene expression in mice after repeated and subchronic oral exposure to vomitoxin (Deoxynivalenol): differential toxin-induced hyporesponsiveness and recovery. Toxicol. Appl. Pharmacol. 151 (1998) 347-358
64. Zhou H.R., Harkema J.R., Yan D., and Pestka J.J. Amplified proinflammatory cytokine expression and toxicity in mice coexposed to lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol). J. Toxicol. Environ. Health A 57 (1999) 115-136
65. 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