NF-κB activation via MyD88-dependent Toll-like receptor signaling is inhibited by trichothecene mycotoxin deoxynivalenol

Journal of Toxicological Sciences

Volumn 41, Issue 2, 2016, Pages 273-279

  Sugiyama, Kei Ichi ^a   Muroi, Masashi ^b   Kinoshita, Mawo ^a,c   Hamada, Osamu ^a,c   Minai, Yuji ^c   Sugita Konishi, Yoshiko ^d   Kamata, Yoichi ^e   Tanamoto, Ken Ichi ^b  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b MUSASHINO UNIVERSITY   (Japan)

^c TAMAGAWA UNIVERSITY   (Japan)

^d AZABU UNIVERSITY   (Japan)

^e IWATE UNIVERSITY   (Japan)

Author keywords

Deoxynivalenol; Macrophage; MyD88; Toll like receptor

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TRICHOTHECENE DERIVATIVE; TRICHOTHECENE MYCOTOXIN DEOXYNIVALENOL; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE; MYCOTOXIN; VOMITOXIN;

ANIMAL CELL; CELL FUNCTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; LETTER; MACROPHAGE ACTIVATION; MACROPHAGE CULTURE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ASSAY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; AGONISTS; ANIMAL; CELL CULTURE; CHEMICAL PHENOMENA; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MACROPHAGE; METABOLISM; MONOCYTE; PHYSIOLOGY; RAW 264.7 CELL LINE;

ANIMALS; CELLS, CULTURED; CYTOKINES; DEPRESSION, CHEMICAL; DOWN-REGULATION; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MONOCYTES; MYCOTOXINS; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; RAW 264.7 CELLS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRICHOTHECENES;

EID: 84960347927     PISSN: 03881350     EISSN: 18803989     Source Type: Journal    
DOI: 10.2131/jts.41.273     Document Type: Letter

References (42)

1. Akira, S., Uematsu, S. and Takeuchi, O. (2006): Pathogen recognition and innate immunity. Cell, 124, 783-801
2. Bennett, J.W. and Klich, M. (2003): Mycotoxins. Clin. Microbiol. Rev., 16, 497-516
3. Beutler, B.A. (2009): TLRs and innate immunity. Blood, 113, 1399-1407
4. Boockvar, K.S., Granger, D.L., Poston, R.M., Maybodi, M., Washington, M.K., Hibbs, J.B.Jr. and Kurlander, R.L. (1994): Nitric oxide produced during murine listeriosis is protective. Infect. Immun., 62, 1089-1100
5. Chen, Z., Hagler, J., Palombella, V.J., Melandri, F., Scherer, D., Ballard, D. and Maniatis, T. (1995): Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev., 9, 1586-1597.
6. DiDonato, J., Mercurio, F., Rosette, C., Wu-Li, J., Suyang, H., Ghosh, S. and Karin, M. (1996): Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol., 16, 1295-1304
7. Dirks, W., Mittnacht, S., Rentrop, M. and Hauser, H. (1989): Isolation and functional characterization of the murine interferon-β1 promoter. J. Interferon. Res., 9, 125-133.
8. El Kasmi, K.C., Qualls, J.E., Pesce, J.T., Smith, A.M., Thompson, R.W., Henao-Tamayo, M., Basaraba, R.J., König, T., Schleicher, U., Koo, M.S., Kaplan, G., Fitzgerald, K.A., Tuomanen, E.I., Orme, I.M., Kanneganti, T.D., Bogdan, C., Wynn, T.A. and Murray, P.J. (2008): Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol., 9, 1399-1406
9. Hiscott, J., Alper, D., Cohen, L., Leblanc, J., Sportza, L., Wong, A. and Xanthoudakis, S. (1989): Induction of human interferon gene expression is associated with a nuclear factor that interacts with the NF-kappa B site of the human immunodeficiency virus enhancer. J. Virol., 63, 2557-2566
10. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S.O., Goode, J., Lin, P., Mann, N., Mudd, S., Crozat, K., Sovath, S., Han, J. and Beutler, B. (2003): Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature, 424, 743-748
11. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, H., Takeda, Y., Takeda, K. and Akira, S. (1999): Cutting edge: Tolllike receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol., 162, 3749-3752
12. Igarashi, A., Ohtsu, S., Muroi, M. and Tanamoto, K. (2006): Effects of possible endocrine disrupting chemicals on bacterial component-induced activation of NF-κB. Biol. Pharm. Bull., 29, 2120-2122
13. Instanes, C. and Hetland, G. (2004): 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, 13-21
14. Jacobs, A.T. and Ignarro, L.J. (2001): Lipopolysaccharide-induced expression of interferon-β mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J. Biol. Chem., 276, 47950-47957
15. Janssens, S. and Beyaert, R. (2003): Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell, 11, 293-302
16. Kawai, T. and Akira, S. (2009): The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol., 21, 317-337
17. Kawai, T. and Akira, S. (2010): The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol., 11, 373-384
18. Kim, Y.M., Lee, B.S., Yi, K.Y. and Paik, S.G. (1997): Upstream NF-κB site is required for the maximal expression of mouse inducible nitric oxide synthase gene in interferon-γ plus lipopolysaccharide-induced RAW 264.7 macrophages. Biochem. Biophys. Res. Commun., 236, 655-660
19. Laemmli, U.K. (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685
20. Lenardo, M.J., Fan, C.M., Maniatis, T. and Baltimore, D. (1989): The involvement of NF-κB in β-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell, 57, 287-294
21. Li, M., Harkema, J.R., Cuff, C.F. and Pestka, J.J. (2007): Deoxynivalenol exacerbates viral bronchopneumonia induced by respiratory reovirus infection. Toxicol. Sci., 95, 412-426
22. Li, S., Strelow, A., Fontana, E.J. and Wesche, H. (2002): IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. USA, 99, 5567-5572
23. Muroi, M. and Tanamoto, K. (2008): TRAF6 distinctively mediates MyD88-and IRAK-1-induced activation of NF-κB. J. Leukoc. Biol., 83, 702-707
24. Muroi, M., Ohnishi, T. and Tanamoto, K. (2002): Regions of the mouse CD14 molecule required for Toll-like receptor 2-and 4-mediated activation of NF-κB. J. Biol. Chem., 277, 42372-42379
25. Murphy, W.J., Muroi, M., Zhang, C.X., Suzuki, T. and Russell, S.W. (1996): Both basal and enhancer κB elements are required for full induction of the mouse inducible nitric oxide synthase gene. J. Endotoxin. Res., 3, 381-393
26. Pestka, J.J. (2008): Mechanisms of deoxynivalenol-induced gene expression and apoptosis. Food Addit. Contam., 25, 1128-1140
27. Pestka, J.J. and Smolinski, A.T. (2005): Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev., 8, 39-69
28. Poltorak, A., He, X., Smirnova, I., Liu, M.Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B. and Beutler, B. (1998): Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science, 282, 2085-2088
29. Rocha, O., Ansari, K. and Doohan, F. (2005): Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit. Contam., 22, 369-378
30. Rotter, B.A. (1996): Invited review: Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health A, 48, 1-34.
31. Shimomura-Shimizu, M., Sugiyama, K., Muroi, M. and Tanamoto, K. (2005): Alachlor and carbaryl suppress lipopolysaccharide-induced iNOS expression by differentially inhibiting NF-κB activation. Biochem. Biophys. Res. Commun., 332, 793-799
32. Sugiyama, K., Kawakami, H., Kamata, Y. and Sugita-Konishi, Y. (2011): Effect of a combination of deoxynivalenol and nivalenol on lipopolisaccharide-induced nitric oxide production by mouse macrophages. Mycotoxin. Res., 27, 57-62
33. Sugiyama, K., Muroi, M. and Tanamoto, K. (2008): A novel TLR4-binding peptide that inhibits LPS-induced activation of NF-κB and in vivo toxicity. Eur. J. Pharmacol., 594, 152-156
34. Sugiyama, K., Muroi, M., Tanamoto, K., Nishijima, M. and Sugita-Konishi, Y. (2010): Deoxynivalenol and nivalenol inhibit lipopolysaccharide-induced nitric oxide production by mouse macrophage cells. Toxicol. Lett., 192, 150-154
35. Tai, J.-H. and Pestka, J.J. (1990): T-2 toxin impairment of murine response to Salmonella typhimurium: a histopathologic assessment. Mycopathologia, 109, 149-155
36. Tryphonas, H., Iverson, F., So, Y., Nera, E.A., McGuire, P.F., O'grady, L., Clayson, D.B. and Scott, P.M. (1986): Effects of deoxynivalenol (vomitoxin) on the humoral and cellular immunity of mice. Toxicol. Lett., 30, 137-150
37. Tsutsuki, H., Yahiro, K., Suzuki, K., Suto, A., Ogura, K., Nagasawa, S., Ihara, H., Shimizu, T., Nakajima, H., Moss, J. and Noda, M. (2012): Subtilase cytotoxin enhances escherichia coli survival in macrophages by suppression of nitric oxide production through the inhibition of NF-κB activation. Infect. Immun., 80, 3939-3951
38. Visvanathan, K.V. and Goodbourn, S. (1989): Double-stranded RNA activates binding of NF-κB to an inducible element in the human beta-interferon promoter. EMBO J., 8, 1129-1138.
39. von Bernuth, H., Picard, C., Jin, Z., Pankla, R., Xiao, H., Ku, C.L., Chrabieh, M., Mustapha, I.B., Ghandil, P., Camcioglu, Y., Vasconcelos, J., Sirvent, N., Guedes, M., Vitor, A.B., Herrero-Mata, M.J., Aróstegui, J.I., Rodrigo, C., Alsina, L., Ruiz-Ortiz, E., Juan, M., Fortuny, C., Yagüe, J., Antón, J., Pascal, M., Chang, H.H., Janniere, L., Rose, Y., Garty, B.Z., Chapel, H., Issekutz, A., Maródi, L., Rodriguez-Gallego, C., Banchereau, J., Abel, L., Li, X., Chaussabel, D., Puel, A. and Casanova, J.L. (2008): Pyogenic bacterial infections in humans with MyD88 deficiency. Science, 321, 691-696
40. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., and Akira, S. (2003): Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science, 301, 640-643
41. Yazar, S. and Omurtag, G.Z. (2008): Fumonisins, trichothecenes and zearalenone in cereals. Int. J. Mol. Sci., 9, 2062-2090
42. Ziprin, R.L. and Elissalde, M.H. (1990): Effect of T-2 toxin on resistance to systemic Salmonella typhimurium infection of newly hatched chickens. Am. J. Vet. Res., 51, 1869-1872.