Repression of peroxisome proliferator-activated receptor γ by mucosal ribotoxic insult-activated CCAAT/enhancer-binding protein homologous protein

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5522-5530

  Park, Seong Hwan ^a   Choi, Hye Jin ^a   Yang, Hyun ^a   Do, Kee Hun ^a   Kim, Juil ^a   Moon, Yuseok ^a  

^a Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

15 ACETYLVOMITOXIN; ANISOMYCIN; CCAAT ENHANCER BINDING PROTEIN BETA; HUR PROTEIN; INTERLEUKIN 8; MESSENGER RNA; MYCOTOXIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG; VOMITOXIN; 15-ACETYLDEOXYNIVALENOL; DDIT3 PROTEIN, HUMAN; ELAV-LIKE PROTEIN 1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MEMBRANE ANTIGEN; PROTEIN SYNTHESIS INHIBITOR; RNA BINDING PROTEIN; TRICHOTHECENE DERIVATIVE;

ARTICLE; CHEMICAL STRESS; CYTOKINE PRODUCTION; EPITHELIUM CELL; GASTROINTESTINAL MUCOSA; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RECEPTOR BLOCKING; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; RIBOSOME; RNA STABILITY; BIOSYNTHESIS; CELL LINE; CONFOCAL MICROSCOPY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MUCOSAL IMMUNITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANISOMYCIN; ANTIGENS, SURFACE; BLOTTING, WESTERN; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, MUCOSAL; INTERLEUKIN-8; INTESTINAL MUCOSA; MICROSCOPY, CONFOCAL; PPAR GAMMA; PROTEIN SYNTHESIS INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; TRANSCRIPTION FACTOR CHOP; TRANSFECTION; TRICHOTHECENES;

EID: 78149487633     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001315     Document Type: Article

References (77)

1. Fornace, A. J., Jr., J. Jackman, M. C. Hollander, B. Hoffman-Liebermann, and D. A. Liebermann. 1992. Genotoxic-stress-response genes and growth-arrest genes: gadd, MyD, and other genes induced by treatments eliciting growth arrest. Ann. N. Y. Acad. Sci. 663:139-153.
2. Fornace, A. J., Jr., I. Alamo, Jr., and M. C. Hollander. 1988. DNA damageinducible transcripts in mammalian cells. Proc. Natl. Acad. Sci. USA 85:8800-8804.
3. Bruhat, A., C. Jousse, V. Carraro, A. M. Reimold, M. Ferrara, and P. Fafournoux. 2000. Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol. Cell. Biol. 20:7192-7204.
4. Bruhat, A., J. Averous, V. Carraro, C. Zhong, A. M. Reimold, M. S. Kilberg, and P. Fafournoux. 2002. Differences in the molecular mechanisms involved in the transcriptional activation of the CHOP and asparagine synthetase genes in response to amino acid deprivation or activation of the unfolded protein response. J. Biol. Chem. 277:48107-48114.
5. Shirakawa, K., S. Maeda, T. Gotoh, M. Hayashi, K. Shinomiya, S. Ehata, R. Nishimura, M. Mori, K. Onozaki, H. Hayashi, et al. 2006. CCAAT/enhancerbinding protein homologous protein (CHOP) regulates osteoblast differentiation. Mol. Cell. Biol. 26:6105-6116.
6. Ron, D., and J. F. Habener. 1992. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6:439-453.
7. Vij, N., M. O. Amoako, S. Mazur, and P. L. Zeitlin. 2008. CHOP transcription factor mediates IL-8 signaling in cystic fibrosis bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 38:176-184.
8. Tsutsumi, S., T. Gotoh, W. Tomisato, S. Mima, T. Hoshino, H. J. Hwang, H. Takenaka, T. Tsuchiya, M. Mori, and T. Mizushima. 2004. Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory druginduced apoptosis. Cell Death Differ. 11:1009-1016.
9. Oyadomari, S., A. Koizumi, K. Takeda, T. Gotoh, S. Akira, E. Araki, and M. Mori. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109:525-532.
10. Namba, T., K. Tanaka, Y. Ito, T. Ishihara, T. Hoshino, T. Gotoh, M. Endo, K. Sato, and T. Mizushima. 2009. Positive role of CCAAT/enhancer-binding protein homologous protein, a transcription factor involved in the endoplasmic reticulum stress response in the development of colitis. Am. J. Pathol. 174:1786-1798.
11. Milhavet, O., J. L. Martindale, S. Camandola, S. L. Chan, D. S. Gary, A. Cheng, N. J. Holbrook, and M. P. Mattson. 2002. Involvement of Gadd153 in the pathogenic action of presenilin-1 mutations. J. Neurochem. 83:673-681.
12. Endo, M., S. Oyadomari, M. Suga, M. Mori, and T. Gotoh. 2005. The ER stress pathway involving CHOP is activated in the lungs of LPS-treated mice. J. Biochem. 138:501-507.
13. Endo, M., M. Mori, S. Akira, and T. Gotoh. 2006. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 176:6245-6253.
14. Sansonetti, P. J. 2008. Host-bacteria homeostasis in the healthy and inflamed gut. Curr. Opin. Gastroenterol. 24:435-439.
15. Cario, E. 2008. Innate immune signalling at intestinal mucosal surfaces: a fine line between host protection and destruction. Curr. Opin. Gastroenterol. 24:725-732.
16. McCole, D. F., and K. E. Barrett. 2007. Varied role of the gut epithelium in mucosal homeostasis. Curr. Opin. Gastroenterol. 23:647-654.
17. Medvedev, A. E., K. M. Kopydlowski, and S. N. Vogel. 2000. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: dysregulation of cytokine, chemokine, and Toll-like receptor 2 and 4 gene expression. J. Immunol. 164:5564-5574.
18. Tsianos, E. V., and K. Katsanos. 2009. Do we really understand what the immunological disturbances in inflammatory bowel disease mean? World J. Gastroenterol. 15:521-525.
19. Srinivasan, M., and D. J. Summerlin. 2009. Modulation of the colonic epithelial cell responses and amelioration of inflammation by CD80 blockade in TNBS colitis. Clin. Immunol. 133:411-421.
20. Schölmerich, J. 2006. Inflammatory bowel disease: Pandora's box, present and future. Ann. N. Y. Acad. Sci. 1072:365-378.
21. Mansén, A., H. Guardiola-Diaz, J. Rafter, C. Branting, and J. A. Gustafsson. 1996. Expression of the peroxisome proliferator-activated receptor (PPAR) in the mouse colonic mucosa. Biochem. Biophys. Res. Commun. 222:844-851.
22. Jiang, C., A. T. Ting, and B. Seed. 1998. PPAR-γ agonists inhibit production of monocyte inflammatory cytokines. Nature 391:82-86.
23. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391:79-82.
24. Su, C. G., X. Wen, S. T. Bailey, W. Jiang, S. M. Rangwala, S. A. Keilbaugh, A. Flanigan, S. Murthy, M. A. Lazar, and G. D. Wu. 1999. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammatory response. J. Clin. Invest. 104:383-389.
25. Moon, Y., H. Yang, and S. H. Park. 2008. Hypo-responsiveness of interleukin-8 production in human embryonic epithelial intestine 407 cells independent of NF-κB pathway: new lessons from endotoxin and ribotoxic deoxynivalenol. Toxicol. Appl. Pharmacol. 231:94-102.
26. Yoder, J. M., R. U. Aslam, and N. J. Mantis. 2007. Evidence for widespread epithelial damage and coincident production of monocyte chemotactic protein 1 in a murine model of intestinal ricin intoxication. Infect. Immun. 75:1745-1750.
27. Thorpe, C. M., B. P. Hurley, L. L. Lincicome, M. S. Jacewicz, G. T. Keusch, and D. W. Acheson. 1999. Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect. Immun. 67:5985-5993.
28. Korcheva, V., J. Wong, C. Corless, M. Iordanov, and B. Magun. 2005. Administration of ricin induces a severe inflammatory response via nonredundant stimulation of ERK, JNK, and P38 MAPK and provides a mouse model of hemolytic uremic syndrome. Am. J. Pathol. 166:323-339.
29. Laskin, J. D., D. E. Heck, and D. L. Laskin. 2002. The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol. Sci. 69:289-291.
30. Shifrin, V. I., and P. Anderson. 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.
31. Barbacid, M., and D. Vazquez. 1975. Ribosome changes during translation. J. Mol. Biol. 93:449-463.
32. Bunyard, P., M. Handley, G. Pollara, K. Rutault, I. Wood, M. Chaudry, C. Alderman, J. Foreman, D. R. Katz, and B. M. Chain. 2003. Ribotoxic stress activates p38 and JNK kinases and modulates the antigen-presenting activity of dendritic cells. Mol. Immunol. 39:815-827.
33. Instanes, C., and G. Hetland. 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.
34. Smith, W. E., A. V. Kane, S. T. Campbell, D. W. Acheson, B. H. Cochran, and C. M. Thorpe. 2003. Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect. Immun. 71:1497-1504.
35. Rotter, B. A., D. B. Prelusky, and J. J. Pestka. 1996. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48:1-34.
36. Jackson, L. S., and L. B. Bullerman. 1999. Effect of processing on Fusarium mycotoxins. Adv. Exp. Med. Biol. 459:243-261.
37. Luo, Y., T. Yoshizawa, and T. Katayama. 1990. Comparative study on the natural occurrence of Fusarium mycotoxins (trichothecenes and zearalenone) in corn and wheat from high-and low-risk areas for human esophageal cancer in China. Appl. Environ. Microbiol. 56:3723-3726.
38. Li, F. Q., Y. W. Li, X. Y. Luo, and T. Yoshizawa. 2002. Fusarium toxins in wheat from an area in Henan Province, PR China, with a previous human red mould intoxication episode. Food Addit. Contam. 19:163-167.
39. Bhat, R. V., S. R. Beedu, Y. Ramakrishna, and K. L. Munshi. 1989. Outbreak of trichothecene mycotoxicosis associated with consumption of mould-damaged wheat production in Kashmir Valley, India. Lancet 333:35-37.
40. Pieters, M. N., J. Freijer, B. J. Baars, D. C. Fiolet, J. van Klaveren, and W. Slob. 2002. Risk assessment of deoxynivalenol in food: concentration limits, exposure and effects. Adv. Exp. Med. Biol. 504:235-248.
41. van Egmond, H. P., R. C. Schothorst, and M. A. Jonker. 2007. Regulations relating to mycotoxins in food: perspectives in a global and European context. Anal. Bioanal. Chem. 389:147-157.
42. Pestka, J. J., and A. T. Smolinski. 2005. Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 8:39-69.
43. Bouhet, S., and I. P. Oswald. 2005. The effects of mycotoxins, fungal food contaminants, on the intestinal epithelial cell-derived innate immune response. Vet. Immunol. Immunopathol. 108:199-209.
44. Calvert, T. W., K. E. Aidoo, A. G. Candlish, and A. R. Fuat. 2005. Comparison of in vitro cytotoxicity of Fusarium mycotoxins, deoxynivalenol, T-2 toxin and zearalenone on selected human epithelial cell lines. Mycopathologia 159:413-419.
45. Maresca, M., R. Mahfoud, N. Garmy, and J. Fantini. 2002. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 132:2723-2731.
46. Sergent, T., M. Parys, S. Garsou, L. Pussemier, Y. J. Schneider, and Y. Larondelle. 2006. Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol. Lett. 164:167-176.
47. Azcona-Olivera, J. I., Y. Ouyang, J. Murtha, F. S. Chu, and J. J. Pestka. 1995. 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.
48. Chung, Y. J., G. H. Yang, Z. Islam, and J. J. Pestka. 2003. Up-regulation of macrophage inflammatory protein-2 and complement 3A receptor by the trichothecenes deoxynivalenol and satratoxin G. Toxicology 186:51-65.
49. Moon, Y., and J. J. Pestka. 2002. Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen-activated protein kinases. Toxicol. Sci. 69:373-382.
50. Zhou, H.-R., J. R. Harkema, D. Yan, and J. J. Pestka. 1999. Amplified proinflammatory cytokine expression and toxicity in mice coexposed to lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol). J. Toxicol. Environ. Health A 57:115-136.
51. Gotoh, T., S. Oyadomari, K. Mori, and M. Mori. 2002. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J. Biol. Chem. 277:12343-12350.
52. Chen, Y. J., B. C. Tan, Y. Y. Cheng, J. S. Chen, and S. C. Lee. 2010. Differential regulation of CHOP translation by phosphorylated eIF4E under stress conditions. Nucleic Acids Res. 38:764-777.
53. Alcantara Warren, C., R. V. Destura, J. E. Sevilleja, L. F. Barroso, H. Carvalho, L. J. Barrett, A. D. O'Brien, and R. L. Guerrant. 2008. Detection of epithelialcell injury, and quantification of infection, in the HCT-8 organoid model of cryptosporidiosis. J. Infect. Dis. 198:143-149.
54. Sifuentes, L. Y., and G. D. Di Giovanni. 2007. Aged HCT-8 cell monolayers support Cryptosporidium parvum infection. Appl. Environ. Microbiol. 73:7548-7551.
55. Thébault, S., N. Deniel, R. Marion, R. Charlionet, F. Tron, D. Cosquer, J. Leprince, H. Vaudry, P. Ducrotté, and P. Déchelotte. 2006. Proteomic analysis of glutamine-treated human intestinal epithelial HCT-8 cells under basal and inflammatory conditions. Proteomics 6:3926-3937.
56. Avantaggiato, G., R. Havenaar, and A. Visconti. 2004. Evaluation of the intestinal absorption of deoxynivalenol and nivalenol by an in vitro gastrointestinal model, and the binding efficacy of activated carbon and other adsorbent materials. Food Chem. Toxicol. 42:817-824.
57. Obremski, K., L. Zielonka, M. Gajecka, E. Jakimiuk, T. Bakula, M. Baranowski, and M. Gajecki. 2008. Histological estimation of the small intestine wall after administration of feed containing deoxynivalenol, T-2 toxin and zearalenone in the pig. Pol. J. Vet. Sci. 11:339-345.
58. Moon, Y., H. Yang, and S. H. Lee. 2007. 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. 362:256-262.
59. Choi, H. J., H. Yang, S. H. Park, and Y. Moon. 2009. HuR/ELAVL1 RNA binding protein modulates interleukin-8 induction by muco-active ribotoxin deoxynivalenol. Toxicol. Appl. Pharmacol. 240:46-54.
60. Yang, H., S. H. Park, H. J. Choi, and Y. Moon. 2009. Epithelial cell survival by activating transcription factor 3 (ATF3) in response to chemical ribosomeinactivating stress. Biochem. Pharmacol. 77:1105-1115.
61. Yang, H., H. J. Choi, S. H. Park, J. S. Kim, and Y. Moon. 2009. Macrophage inhibitory cytokine-1 (MIC-1) and subsequent urokinase-type plasminogen activator mediate cell death responses by ribotoxic anisomycin in HCT-116 colon cancer cells. Biochem. Pharmacol. 78:1205-1213.
62. Kelly, D., J. I. Campbell, T. P. King, G. Grant, E. A. Jansson, A. G. Coutts, S. Pettersson, and S. Conway. 2004. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-γ and RelA. Nat. Immunol. 5:104-112.
63. Subbaramaiah, K., T. P. Marmo, D. A. Dixon, and A. J. Dannenberg. 2003. Regulation of cyclooxgenase-2 mRNA stability by taxanes: evidence for involvement of p38, MAPKAPK-2, and HuR. J. Biol. Chem. 278:37637-37647.
64. Doller, A., A. Huwiler, R. Müller, H. H. Radeke, J. Pfeilschifter, and W. Eberhardt. 2007. Protein kinase Ca-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell 18:2137-2148.
65. Doller, A., el-S. Akool, A. Huwiler, R. Müller, H. H. Radeke, J. Pfeilschifter, and W. Eberhardt. 2008. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cd elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol. Cell. Biol. 28:2608-2625.
66. Foster, G. H., C. S. Armstrong, R. Sakiri, and V. L. Tesh. 2000. Shiga toxininduced tumor necrosis factor a expression: requirement for toxin enzymatic activity and monocyte protein kinase C and protein tyrosine kinases. Infect. Immun. 68:5183-5189.
67. Torgersen, M. L., S. Wälchli, S. Grimmer, S. S. Skånland, and K. Sandvig. 2007. Protein kinase Cd is activated by Shiga toxin and regulates its transport. J. Biol. Chem. 282:16317-16328.
68. Harhaj, N. S., and D. A. Antonetti. 2004. Regulation of tight junctions and loss of barrier function in pathophysiology. Int. J. Biochem. Cell Biol. 36:1206-1237.
69. Zhou, H. R., Q. Jia, and J. J. Pestka. 2005. Ribotoxic stress response to the trichothecene deoxynivalenol in the macrophage involves the SRC family kinase Hck. Toxicol. Sci. 85:916-926.
70. von Knethen, A., M. Soller, N. Tzieply, A. Weigert, A. M. Johann, C. Jennewein, R. Köhl, and B. Brüne. 2007. PPARγ1 attenuates cytosol to membrane translocation of PKCα to desensitize monocytes/macrophages. J. Cell Biol. 176:681-694.
71. Lee, S. Y., M. S. Lee, R. P. Cherla, and V. L. Tesh. 2008. Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell. Microbiol. 10:770-780.
72. Shi, Y., K. Porter, N. Parameswaran, H. K. Bae, and J. J. Pestka. 2009. Role of GRP78/BiP degradation and ER stress in deoxynivalenol-induced interleukin-6 upregulation in the macrophage. Toxicol. Sci. 109:247-255.
73. Wolfson, J. J., K. L. May, C. M. Thorpe, D. M. Jandhyala, J. C. Paton, and A. W. Paton. 2008. Subtilase cytotoxin activates PERK, IRE1 and ATF6 endoplasmic reticulum stress-signalling pathways. Cell. Microbiol. 10:1775-1786.
74. Wu, Z., N. L. Bucher, and S. R. Farmer. 1996. Induction of peroxisome proliferator-activated receptor γ during the conversion of 3T3 fibroblasts into adipocytes is mediated by C/EBPβ, C/EBPδ, and glucocorticoids. Mol. Cell. Biol. 16:4128-4136.
75. Hamm, J. K., B. H. Park, and S. R. Farmer. 2001. A role for C/EBPb in regulating peroxisome proliferator-activated receptor γ activity during adipogenesis in 3T3-L1 preadipocytes. J. Biol. Chem. 276:18464-18471.
76. Pereira, R. C., A. M. Delany, and E. Canalis. 2004. CCAAT/enhancer binding protein homologous protein (DDIT3) induces osteoblastic cell differentiation. Endocrinology 145:1952-1960.
77. Yang, H., D. H. Chung, Y. B. Kim, Y. H. Choi, and Y. Moon. 2008. Ribotoxic mycotoxin deoxynivalenol induces G2/M cell cycle arrest via p21Cip/WAF1 mRNA stabilization in human epithelial cells. Toxicology 243:145-154.