Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen-activated protein kinases

Toxicological Sciences

Volumn 69, Issue 2, 2002, Pages 373-382

  Moon, Yuseok ^a,b   Pestka, James J ^b,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

COX 2 expression; Immunotoxins; Mycotoxins; Tricothecenes; Vomitoxin

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYCLOOXYGENASE 2; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROSTAGLANDIN E2; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRICHOTHECENE DERIVATIVE; VOMITOXIN;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; DATA ANALYSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXPOSURE; EXPRESSION VECTOR; GENE CONSTRUCT; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IMMUNOTOXICITY; MACROPHAGE; METABOLITE; MOUSE; NONHUMAN; PROMOTER REGION; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA STABILITY; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BETA-GALACTOSIDASE; BLOTTING, WESTERN; CELL LINE; CYCLOOXYGENASE 2; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ISOENZYMES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUCIFERASES; MACROPHAGES; MAP KINASE KINASE 4; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLASMIDS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; TRANSFECTION; TRICHOTHECENES;

ANIMALIA; MURINAE; VECTORS;

EID: 0036772512     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/69.2.373     Document Type: Article

References (76)

1. Abouzied, M. M., Azcona-Olivera, J. I., Braselton, W. E., and Pestka, J. J. (1991). Immunochemical assessment of mycotoxins in 1989 grain foods: Evidence for deoxynivalenol (vomitoxin) contamination. Appl. Environ. Microbiol. 57, 672-677.
2. Anderson, G. D., Hauser, S. D., McGarity, K. L., Bremer, M. E., Isakson, P. C., and Gregory, S. A. (1996). Selective inhibition of cyclooxygenase (COX)-2 reverses inflammation and expression of COX-2 and interleukin 6 in rat adjuvant arthritis. J. Clin. Invest. 97, 2672-2679.
3. Azcona-Olivera, J. I., Quyang, Y., Murtha, J., Chu, F. F., and Pestka, J. J. (1995a). Induction of cytokine mRNAs in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): Relationship to toxin distribution and protein synthesis inhibition. Toxicol. Appl. Pharmacol. 133, 109-120.
4. + cells. Food. Chem. Toxicol. 35, 433-441.
5. Betina, V. (1989). Trichothecenes. In Mycotoxins. (V. Betina, Ed.), pp. 192-241. Elsevior, New York.
6. Betz, M., and Fox, B. S. (1991). Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 146, 108-113.
7. Bhat, R., Beedu, S. R., Ramakrishna, Y., and Munshi, K. L. (1989). Outbreak of trichothecene mycotoxicosis associated with consumption of mould-damaged wheat production in Kashmir Valley, India. Lancet 1, 35-37.
8. Bondy, G. S., and Pestka, J. J. (2000). Immunomodulation by fungal toxins. J. Toxicol. Environ. Health B Crit. Rev. 3, 109-143.
9. Callejas, N. A., Castrillo, A., Bosca, L., and Martin-Sanz, P. (1999). Inhibition of prostaglandin synthesis upregulates cyclooxygenase-2 induced by lipopolysaccharide and peroxisomal proliferators. J. Pharmacol. Exp. Ther. 288, 1235-1241.
10. Chen, C., Chen, Y. H., and Lin, W. W. (1999). Involvement of p38 mitogen-activated protein kinase in lipopolysaccharide-induced iNOS and COX-2 expression in J774 macrophages. Immunology 97, 124-129.
11. Davis, S., Vanhoutte, P., Pages, C., Caboche, J., and Laroche, S. (2000). The MAPK/ERK cascade targets both Elk-1 and cAMP. response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci. 20, 4563-4572.
12. Dean, J. L., Brook, M., Clark, A. R., and Saklatvala, J. (1999). The p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J. Biol. Chem. 274, 264-269.
13. Dixon, D. A., Kaplan, C. D., McIntyre, T. M., Zimmerman, G. A., and Prescott, S. M. (2000). Post-transcriptional control of cyclooxygenase-2 gene expression: The role of the 3′-untranslated region. J. Biol. Chem. 275, 11750-11757.
14. Dixon, D. A., Tolley, N. D., King, P. H., Nabors, L. B., McIntyre, T. M., Zimmerman, G. A., and Prescott, S. M. (2001). Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108, 1657-1665.
15. Dong, W., Sell, J. E., and Pestka, J. J. (1991). Quantitative assessment of mesangial immunoglobulin A (IgA) accumulation, elevated circulating IgA immune complexes, and hematuria during vomitoxin-induced IgA nephropathy. Fundam. Appl. Toxicol. 17, 197-207.
16. Fiebich, B. L., Mueksch, B., Boehringer, M., and Hull, M. (2000). Interleukin-1β induces cyclooxygenase-2 and prostaglandin E(2) synthesis in human neuroblastoma cells: Involvement of p38 mitogen-activated protein kinase and nuclear factor-κB. J. Neurochem. 75, 2020-2028.
17. Fletcher, B. S., Kujubu, D. A., Perrin, D. M., and Herschman, H. R. (1992). Structure of the mitogenic-inducible TIS10 gene and demonstration that the TIS10-encoded protein is a functional prostaglandin G/H synthase. J. Biol. Chem. 267, 4338-4344.
18. Guan, Z., Buckman, S. Y., Miller, B. W., Springer, L. D., Morrison, A. R. (1998). Interleukin 1β-induced cyclooxygenase-2 expression requires activation of both c-Jun NH2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J. Biol. Chem. 273, 28670-28676.
19. Hall, L. L., Bicknell, G. R., Primrose, L., Pringle, J. H., Shaw, J. A., and Furness, P. N. (1998). Reproducibility in the quantification of mRNA levels by RT-PCR- ELISA and RT competitive-PCR ELISA. Biotechniques 24, 652-658.
20. Hu, J., Roy, S. K., Shapiro, P. S., Rodig, S. R., Reddy, S. P., Platanias, L. C., Schreiber, R. D., and Kalvakolanu, D. V. (2001). ERK1 and ERK2 activate CCAAAT/enhancer-binding protein-beta-dependent gene transcription in response to interferon-gamma. J. Biol. Chem. 276, 287-297.
21. Iordanov, M. S., Pribnow, D., Magun, J. L., Dinh, T. H., Pearson, J. A., Chen, S. L., and Magun, B. E. (1997). Ribotoxic stress response: Activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the α-sarcin/ricin loop in the 28S rRNA. Mol. Cell Biol. 17, 3373-3381.
22. Islam, Z., Moon, Y. S., Zhou, H. R., King, L. E., Fraker, P. J., and Pestka, J. J. (2002). Endotoxin potentiation of trichothecene-induced lymphocyte apoptosis is mediated by up-regulation of glucocorticoids. Toxicol. Appl. Pharmacol. 180, 43-55.
23. Ji, G. E., Park, S. Y., Wong, S. S., and Pestka, J. J. (1998). Modulation of nitric oxide, hydrogen peroxide, and cytokine production in a clonal macrophage model by the trichothecene vomitoxin (deoxynivalenol). Toxicology 125, 203-214.
24. Kalinski, P., Vieira, P. L., Schuitemaker, J. H., de Jong, E. C., and Kapsenberg, M. L. (2001). Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 97, 3466-3469.
25. Kotsonis, F. N., Buedock, G. A., and Flamm, W. G. (1996). Food toxicology. In Casarett & Dull's Toxicology, The Basic Science of Poisons. (C. D. Klaassen, Ed.), pp. 909-949. McGraw-Hill, New York.
26. Langenbach, R., Loftin, C., Lee, C., and Tiano, H. (1999). Cyclooxygenase knockout mice: Models for elucidating isoform-specific functions. Biochem. Pharmacol. 58, 1237-1246.
27. Lasa, M., Mahtani, K. R., Finch A., Brewer, G., Saklatvala, J., and Clark, A. R. (2000). Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated, protein kinase p38 signaling cascade. Mol. Cell. Biol. 20, 4265-4274.
28. Mestre, J. R., Mackrell, P. J., Rivadeneira, D. E., Stapleton, P.P., Tanabe, T., and Daly, J. M. (2001). Redundancy in the signaling pathways and promoter elements regulating cyclooxygenase-2 gene expression in endotoxin-treated macrophage/monocytic cells. J. Biol. Chem. 276, 3977-3982.
29. Morteau, O. (1999). COX-2: promoting tolerance. Nat Med. 5, 867-868.
30. Morteau, O., Morham, S. G., Sellon, R., Dieleman, L. A., Langenbach, R., Smithies, O., and Sartor, R. B. (2000). Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J. Clin. Invest. 105, 469-478.
31. Myers, L. K., Kang, A. H., Postlethwaite, A. E., Rosloniec, E. F., Morham, S. G., Shlopov, B. V., Goorha, S., and Ballou, L. R. (2000). The genetic ablation of cyclooxygenase 2 prevents the development of autoimmune arthritis. Arthritis Rheum. 43, 2687-2693.
32. Nabors, L. B., Gillespie, G. Y., Harkins, L., and King, P. H. (2001). HuR, an RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res. 61, 2154-2161.
33. Naseem, S. M., Hines, H. B., and Creasia, D. A. (1989). Effect of toxins on arachidonic acid metabolism in rat cultured pulmonary alveolar macrophages. Biochem Int. 19, 583-592.
34. Newberry, R. D., Stenson, W. F., and Lorenz, R. G. (1999). Cyclooxygenase-2-dependent arachidonic acid metabolites are essential modulators of the intestinal immune response to dietary antigen. Nat. Med. 5, 900-906.
35. Newton, R., Seybold, J., Liu, S. F., and Barnes, P.J. (1997a). Alternate COX-2 transcripts are differentially regulated: Implications for post-transcriptional control. Biochem. Biophys. Res. Commun. 234, 85-89.
36. Newton, R., Stevens, D. A., Hart, L. A., Lindsay, M., Adcock, I. M., and Barnes, P. J. (1997b). Superinduction of COX-2 mRNA by cycloheximide and interleukin-1β involves increased transcription and correlates with increased NF-κB and JNK activation. FEBS Lett. 418, 135-138.
37. Pang, L. (2001). COX-2 expression in asthmatic airways: the story so far. Thorax 56, 335-336.
38. Pang, L., and Hoult, J. R. (1996). Induction of cyclooxygenase and nitric oxide synthase in endotoxin-activated J774 macrophages is differentially regulated by indomethacin: Enhanced cyclooxygenase-2 protein expression but reduction of inducible nitric oxide synthase. Eur. J. Pharmacol. 317, 151-155.
39. Paul, A., Cuenda, A., Bryant, C. E., Murray, J., Chilvers, E. R., Cohen, P., Gould, G. W., and Plevin, R. (1999). Involvement of mitogen-activated protein kinase homologues in the regulation of lipopolysaccharide-mediated induction of cyclo oxygenase-2, but not nitric oxide synthase, in RAW 264.7 macrophages. Cell Signal. 11, 491-497.
40. Peraica, M., Radic, B., Lucic, A., and Pavlovic, M. (1999). Toxic effects of mycotoxins in humans. Bull. World Health Organ. 77, 754-766.
41. Pestka, J. J., and Bondy, G. S. (1994). Mycotoxin-induced immunomodulation. In Immunotoxicology and Immunopharmacology. (J. H. Dean., M. I. Luster., A. E. Munson., and I. Kimber, Eds.), pp. 163-182. Raven Press, New York.
42. Pestka, J. J., and Zhou, H. R. (2000). Interleukin-6-deficient mice refractory to IgA dysregulation but not anorexia induction by vomitoxin (deoxynivalenol) ingestion. Food Chem. Toxicol. 38, 565-575.
43. Rasooly, L., Abouzied, M. M., Brooks, K. H., and Pestka, J. J. (1994). 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, 337-348.
44. Rasooly, L., and Pestka, J. J. (1994). Polyclonal autoreactive IgA increase and mesangial deposition during vomitoxin-induced IgA nephropathy in the BALB/c mouse. Food Chem. Toxicol. 32, 329-336.
45. Ridley, S. H., Dean, J. L., Sarsfield, S. J., Brook, M., Clark, A. R., and Saklatvala, J. (1998). A p38 MAP kinase inhibitor regulates stability of interleukin-1-induced cyclooxygenase-2 mRNA. FEBS Lett. 439, 75-80.
46. Riedy, M. C., Timm, E. A., Jr., and Stewart, C. C. (1995). Quantitative RT-PCR for measuring gene expression. Biotechniques 18, 70-76.
47. Rizzo, A. F., Atroshi, F., Ahotupa, M., Sankari, S., and Elovaara, E. (1994). Protective effect of antioxidants against free radical-mediated lipid peroxidation induced by DON or T-2 toxin. Zentralbl. Veterinarmed. A 41, 81-90.
48. Rizzo, A. F., Atroshi, F., Hirvi, T., and Saloniemi, H. (1992). The hemolytic activity of deoxynivalenol and T-2 toxin. Nat. Toxins 1, 106-110.
49. Rotter, B. A., Prelusky, D. B., and Pestka, J. J. (1996) Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48, 1-34.
50. Samad, T. A., Moore, K. A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J. V., and Woolf, C. J. (2001). Interleukin 1β-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410, 471-475.
51. Scherle, P. A., Jones, E. A., Favata, M. F., Daulerio, A. J., Covington, M. B., Nurnberg, S. A., Magolda, R. L., and Trzaskos, J. M. (1998). Inhibition of MAP kinase kinase prevents cytokine and prostaglandin E2 production in lipopolysaccharide-stimulated monocytes. J. Immunol. 161, 5681-5686.
52. Scott, P. M. (1990). Trichothecenes; in grains. Cereal Foods World 35, 661-666.
53. Sheng, H., Shao, J., and Dubois, R. N. (2001). K-Ras-mediated increase in cyclooxygenase 2 mRNA stability involves activation of the protein kinase B1. Cancer Res. 61, 2670-2675.
54. Shifrin, V. I., and Anderson, P. (1999). 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, 13985-13992.
55. Shohami, E., and Feuerstein, G. (1986). T-2 toxemia and brain prostaglandins. Prostaglandins 31, 307-319.
56. Shohami, E., Wisotsky, B., Kempski, O., and Feuerstein, G. (1987). Therapeutic effect of dexamethasone in T-2 toxicosis. Pharm. Res. 4, 527-530.
57. Sirenko, O. I., Lofquist, A. K., DeMaria, C. T., Morris, J. S., Brower, G., and Haskill, J. S. (1997). Adhesion-dependent regulation of an A + U-rich element-binding activity associated with AUF1 Mol. Cell. Biol. 17, 3898-3906.
58. Smith., W. L., DeWitt, D. L., and Garavito, R. M. (2000). Cyclooxygenases: Structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182.
59. Snijdewint, F. G., Kalinski, P., Wierenga, E. A., Bos, J. D., and Kapsenberg, M. L. (1993). Prostaglandin E2 differentially modulates cytokine secretion profiles of human T helper lymphocytes. J. Immunol. 150, 5321-5329.
60. Strober, W. (1991). Trypan blue exclusion test for cell viability. In Current Protocols in Immunology.. (J. E. Coligan, A. M. Kruisbeek, D. H. Marguiles, E. M. Shevach, and W. Strober, Eds.), pp. A.3.3-4. Wiley, New York.
61. Subbaramaiah, K., Chung, W. J., and Dannenberg, A. J. (1998). Ceramide regulates the transcription of cyclooxygenase-2: Evidence for involvement of extracellular signal-regulated kinase/c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase pathways. J. Biol. Chem. 273, 32943-32949.
62. Tavakoli, S., Cowan, M. J., Benfield, T., Logun, C., and Shelhamer, J. H. (2001). Prostaglandin E(2)-induced interleukin-6 release by a human airway epithelial cell line. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L127-133.
63. Ueno, Y. (1983). General toxicology. In Trichothecenes: Chemical, Biological, and Toxicological Aspects. (Y. Ueno, Ed.), pp 135-1446. Elsevier, New York.
64. Vane, J. R., Bakhle, Y. S., and Botting. R. M. (1998). Cyclooxygenases 1 and 2. Annu. Rev. Pharmacol. Toxicol. 38, 97-120.
65. Vogel, C. (2000). Prostaglandin H synthases and their importance in chemical toxicity. Curr. Drug Metab. 1, 391-404.
66. Wadleigh, D. J., Reddy, S. T., Kopp, E., Ghosh, S., and Herschman, H. R. (2000). Transcriptional activation of the cyclooxygenase-2 gene in endotoxin-treated RAW 264.7 macrophages. J. Biol. Chem. 275, 6259-6266.
67. Wong, S. S., Zhou, H. R., Marin-Martinez, M. L., Brooks, K., and Pestka, J. J. (1998). Modulation of IL-1β, IL-6, and TNF-α secretion and mRNA expression by the trichothecene vomitoxin in the RAW 264.7 murine macrophage cell line. Food Chem. Toxicol. 36, 409-419.
68. Wong, S. S. Zhou, H.-R., and Pestka, J. J. (2002). Effects of vomitoxin (deoxynivalenol) on the binding of transcription factors AP-1, NF-κB and NF-IL6 in RAW 264.7 macrophage cells. J. Toxicol. Environ. Health (in press).
69. Xie, W., and Herschman, H. R. (1995). V-src induces prostaglandin synthase-2 gene expression by activation of the c-Jun N-terminal kinase and the c-Jun transcription factor. J. Biol. Chem. 270, 27622-27628.
70. Yan, Z., Subbaramaiah, K., Camilli, T., Zhang, F., Tanabe, T., McCaffrey, T. A., Dannenberg, A. J., and Weksler, B. B. (2000). Benzo[a]pyrene induces the transcription of cyclooxygenase-2 in vascular smooth-muscle cells. Evidence for the involvement of extracellular signal-regulated kinase and NF-κB. J. Biol. Chem. 275, 4949-4955.
71. Yang, G. H., Jarvis, B. B., Chung, Y. J., and Pestka, J. J. (2000). Apoptosis induction by the satratoxins and other trichothecene mycotoxins: Relationship to ERK, p38 MAPK, and SAPK/JNK activation. Toxicol. Appl. Pharmacol. 164, 149-160.
72. Zhang, Z., Sheng, H., Shao, J., Beauchamp, R. D., and DuBois, R. N. (2000). Posttranscriptional regulation of cyclooxygenase-2 in rat intestinal epithelial cells. Neoplasia 2, 523-530,
73. Zhou, H. R., Harkema, J. R., Yan, D., and Pestka, J. J. (1999). Amplified proinflammatory cytokine gene expression and toxicity in mice coexposed to lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol). J. Toxicol. Environ. Health A 56, 115-136.
74. Zhou, H. R., Yan, D., and Pestka, J. J. (1997). Differential cytokine mRNA expression in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): Dose response and time course. Toxicol. Appl. Pharmacol. 144, 294-305.
75. Zhou, H. R., Yan, D., and Pestka, J. J. (1998). 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, 347-358.
76. Zhu, W., Brauchle, M. A., Di Padova, F., Gram, H., New, L., Ono, K., Downey, J. S., and Han, J. (2001). Gene suppression by tristetraprolin and release by the p38 pathway. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L499-508.