Lipopolysaccharide induces cyclooxygenase-2 in intestinal epithelium via a noncanonical p38 MAPK pathway

Journal of Immunology

Volumn 176, Issue 1, 2006, Pages 580-588

  Grishin, Anatoly V ^a   Wang, Jin ^a   Potoka, Douglas A ^b   Hackam, David J ^b   Upperman, Jeffrey S ^b   Boyle, Patricia ^a   Zamora, Ruben ^b   Ford, Henri R ^a  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CELECOXIB; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BACTERIAL COLONIZATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME INDUCTION; HYPOXIA; INFLAMMATORY CELL; INTESTINE EPITHELIUM; INTESTINE MUCOSA; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPORTER GENE; TRANSCRIPTION REGULATION;

EID: 29644435432     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.1.580     Document Type: Article

References (53)

1. Noerr, B. 2003. Current controversies in the understanding of necrotizing enterocolitis. Adv. Neonatal Care 3: 107-120.
2. Ford, H. R., D. L. Sorrells, and A. S. Knisely. 1996. Inflammatory cytokines, nitric oxide, and necrotizing enterocolitis. Semin. Pediatr. Surg. 5: 155-159.
3. Guthrie, S. O., P. V. Gordon, V. Thomas, J. A. Thorp, J. Peabody, and R. H. Clark. 2003. Necrotizing enterocolitis among neonates in the United States. J. Perinatol. 23: 278-285.
4. Ohno, Y., J. Lee, R. D. Fusunyan, R. P. MacDermott, and I. R. Sanderson. 1997. Macrophage inflammatory protein-2: chromosomal regulation in rat small intestinal epithelial cells. Proc. Natl. Acad. Sci. USA 94: 10279-10284.
5. Longo, W. E., L. J. Damore, J. E. Mazuski, G. S. Smith, N. Panesar, and D. L. Kaminski. 1998. The role of cyclooxygenase-1 and cyclooxygenase-2 in lipopolysaccharide and interleukin-1-stimulated enterocyte prostanoid formation. Mediat. Inflamm. 7: 85-91.
6. Cario, E., G. Gerken, and D. K. Podolsky. 2002. "For whom the bell tolls!": innate defense mechanisms and survival strategies of the intestinal epithelium against lumenal pathogens. Z. Gastroenterol. 40: 983-990.
7. Longo, W. E., N. Panesar, J. Mazuski, and D. L. Kaminski. 1998. Contribution of cyclooxygenase-1 and cyclooxygenase-2 to prostanoid formation by human enterocytes stimulated by calcium ionophore and inflammatory agents. Prostaglandins Other Lipid Mediat. 56: 325-339.
8. Whittle, B. J. 2003. Gastrointestinal effects of nonsteroidal anti-inflammatory drugs. Fundam. Clin. Pharmacol. 17: 301-313.
9. Wallace, J. L. 2001. Prostaglandin biology in inflammatory bowel disease. Gastroenterol. Clin. North Am. 30: 971-980.
10. Subbaramaiah, K., K. Yoshimatsu, E. Scherl, K. M. Das, K. D. Glazier, D. Golijanin, R. A. Soslow, T. Tanabe, H. Naraba, and A. J. Dannenberg. 2004. Microsomal prostaglandin E synthase-1 is overexpressed in inflammatory bowel disease: evidence for involvement of the transcription factor Egr-1. J. Biol. Chem. 279: 12647-12658.
11. Kankuri, E., K. Vaali, R. Korpela, I. Paakkari, H. Vapaatalo, and E. Moilanen. 2001. Effects of a cyclooxygenase-2 preferential agent nimesulide on TNBS-induced acute inflammation in the gut. Inflammation 25: 301-310.
12. Loftin, C. D., H. F. Tiano, and R. Langenbach. 2002. Phenotypes of the cyclooxygenase-deficient mice indicate physiological and pathophysiological roles for cyclooxygenase-1 and cyclooxygenase-2. Prostaglandins Other Lipid Mediat. 68-69: 177-185.
13. Sigthorsson, G., R. J. Simpson, M. Walley, A. Anthony, R. Foster, C. Hotz-Behoftsitz, A. Palizban, J. Pombo, J. Watts, S. G. Morham, and I. Bjarnason. 2002. cyclooxygenase-1 and 2, intestinal integrity, and pathogenesis of nonsteroidal anti-inflammatory drug enteropathy in mice. Gastroenterology 122: 1913-1923.
14. Chung, D. H., R. T. Ethridge, S. Kim, S. Owens-Stowall, A. Hernandez, D. R. Kelly, and B. M. Evers. 2001. Molecular mechanisms contributing to necrotizing enterocolitis. Ann. Surg. 233: 835-842.
15. Tanabe, T., and N. Tohnai. 2002. Cox isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat. 68-69: 95-114.
16. Ramsay, R. G., D. Ciznadija, M. Vanevski, and T. Mantamadiotis. 2003. Transcriptional regulation of cyclooxygenase expression: three pillars of control. Int. J. Immunopathol. Pharmacol. 16: 59-67.
17. Guo, Y. S., M. R. Hellmich, X. D. Wen, and C. M. Townsend, Jr. 2001. Activator protein-1 transcription factor mediates bombesin-stimulated cyclooxygenase-2 expression in intestinal epithelial cells. J. Biol. Chem. 276: 22941-22947.
18. Tessner, T. G., F. Muhale, S. Schloemann, S. M. Cohn, A. Morrison, and W. F. Stenson. 2002. Basic fibroblast growth factor up-regulates cyclooxygenase-2 in 1407 cells through p38 MAP kinase. Am. J. Physiol. 284:G269-G279.
19. Arbabi, S., M. R. Rosengart, I. Garcia, S. Jelacic, and R. V. Maier. 2001. Epithelial cyclooxygenase-2 expression: a model for pathogenesis of colon cancer. J. Surg. Res. 97: 60-64.
20. Lee, J. Y., J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang. 2003. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatydylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J. Biol. Chem. 278: 37041-37051.
21. Yeo, S. J., D. Gravis, J. G. Yoon, and A. K. Yi. 2003. Myeloid differentiation factor 88-dependent transcriptional regulation of cyclooxygenase-2 expression by CpG DNA: role of NF-κB and p38. J. Biol. Chem. 278: 22563-22573.
22. Cheng, H. F., and R. C. Harris. 2002. cyclooxygenase-2 expression in cultured cortical thick ascending limb of Henle increases in response to decreased extracellular ionic content by both transcriptional and posttranscriptional mechanisms: role of p38-mediated pathways. J. Biol. Chem. 277: 45638-45643.
23. Deva, R., P. Shankaranarayanan, R. Ciccoli, and S. Nigam. 2003. Candida albicans induces selectively transcriptional activation of cyclooxygenase-2 in HeLa cells: pivotal roles of Toll-like receptors, p38 mitogen-activated protein kinase, and NF-κB. J. Immunol. 171: 3047-3055.
24. Caivano, M., B. Gorgoni, P. Cohen, and V. Poli. 2001. The induction of cyclooxygenase-2 mRNA in macrophages is biphasic and requires both CCAAT enhancer-binding protein β(C/EBP-β) and C/EBP-δ transcription factors. J. Biol. Chem. 276: 48693-48701.
25. Deng, W. G., Y. Zhu, and K. K. Wu. 2003. Role of p300 and PCAF in regulating cyclooxygenase-2 promoter activation by inflammatory mediators. Blood 103: 2135-2142.
26. 2 production by epidermal growth factor via mitogen-activated protein kinase in articular chondrocytes. J. Biol. Chem. 278: 9691-9697.
27. 2 release and cyclooxygenase-2 expression in a mouse macula densa cell line. J. Biol. Chem. 275: 37922-37929.
28. Yang, T., Y. Huang, L. E. Heasley, T. Berl, J. B. Schnermann, and J. P. Briggs. 2000. MAPK mediation of hypertonicity-stimulated cyclooxygenase-2 expression in renal medullary collecting duct cells. J. Biol. Chem. 275: 23281-23286.
29. Xu, K., A. M. Robida, and T. J. Murphy. 2000. Immediate-early MEK-1-dependent stabilization of rat smooth muscle cell cyclooxygenase-2 mRNA by Gα(q)-coupled receptor signaling. J. Biol. Chem. 275: 23012-23019.
30. Subbaramaiah, K., J. C. Hart, L. Noron, and A. J. Dannenberg. 2000. Microtubule-interfering agents stimulate the transcription of cyclooxygenase-2: evidence for involvement of ERK1/ERK2 and p38 mitogen-activated protein kinase pathways. J. Biol. Chem. 275: 14838-14845.
31. Lasa, M., S. M. Abraham, C. Boucheron, J. Saklatvala, and A. R. Clark. 2002. Dexamethasone causes sustained expression of MAPK phosphatase 1 and phosphatase-mediated inhibition of MAPK p38. Mol. Cell. Biol. 22: 7802-7811.
32. Kim, S. J., S. G. Hwang, I. C. Kim, and J. S. Chun. 2003. Actin cytoskeletal architecture regulates nitric oxide-induced apoptosis, dedifferentiation, and cyclooxygenase-2 expression in articular chondrocytes via mitogen-activated protein kinase and protein kinase C pathways. J. Biol. Chem. 278: 42448-42456.
33. Jang, B. C., T. Sanchez, H. J. Schaefers, O. C. Trifan, C. H. Liu, C. Cremion, C. K. Huang, and T. Hla. 2000. Serum withdrawal-induced posttranscriptional stabilization of cyclooxygenase-2 mRNA in MDA-MB-231 mammary carcinoma cells requires the activity of the p38 stress-activated protein kinase. J. Biol. Chem. 275: 39507-39515.
34. Matsuura, H., M. Sakaue, K. Subbaramaiah, H. Kamitani, T. E. Eling, A. J. Dannenberg, T. Tanabe, H. Inoue, J. Arata, and A. M. Jetten. 1999. Regulation of cyclooxygenase-2 by interferon γ and transforming growth factor α in normal human epidermal keratinocytes and squamous carcinoma cells: role of mitogen-activated protein kinases. J. Biol. Chem. 247: 29138-29148.
35. Barry, O. P., M. G. Kazanietz, D. Pratico, and G. A. FitzGerald. 1999. Arachidonic acid in platelet microparticles up-regulates cyclooxygenase-2- dependent prostaglandin formation via a protein kinase C/mitogen-activated protein kinase-dependent pathway. J. Biol. Chem. 274: 7545-7556.
36. Brewer, J. A., B. Khor, S. K. Vogt, L. M. Muglia, H. Fujiwara, K. E. Haegele, B. P. Sleckman, and L. J. Muglia. 2003. T cell glucocorticoid receptor is required to suppress cyclooxygenase-2-mediated lethal immune activation. Nat. Med. 9: 1318-1322.
37. Guan, Z., S. Y. Buckman, A. P. Pentland, D. J. Templeton, and A. R. Morrison. 1998. Induction of cyclooxygenase-2 by the activated MEKK1→SEK1/MKK4→p38 mitogen-activated protein kinase pathway. J. Biol. Chem. 273: 12901-12908.
38. Hendrickx, N., C. Volanti, U. Moens, O. M. Seternes, P. de Witte, J. R. Vandenheede, J. Piette, and P. Agostinis. 2003. Up-regulation of cyclooxygenase-2 and apoptosis resistance by p38 MAPK in hypericin-mediated photodynamic therapy of human cancer cells. J. Biol. Chem. 278: 52231-52239.
39. Beutler, B., K. Hoebe, X. Du, and R. J. Ulevitch. 2003. How we detect microbes and respond to them: the Toll-like receptors and their transducers. J. Leukocyte Biol. 74: 479-485.
40. Fusunyan, R. D., N. N. Nanthakumar, M. E. Baldeon, and W. A. Walker. 2001. Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr. Res. 49: 589-593.
41. De Plaen, I. G., X. W. Qu, H. Wang, X. D. Tan, L. Wang, X. B. Han, R. A. Rozenfeld, and W. Hsueh. 2002. Endotoxin, but not platelet-activating factor, activates nuclear factor-κB and increases 1κBα and 1κBβ turnover in enterocytes. Immunology 106: 577-583.
42. Ruemelle, F. M., J. F. Beaulieu, S. Dionne, E. Levy, E. G. Seidman, N. Cerf-Bensussan, and M. J. Lentze. 2002. Lipopolysaccharide modulation of normal enterocyte turnover by Toll-like receptors is mediated by endogenously produced tumor necrosis factor α. Gut 51: 842-848.
43. Nanthakumar, N. N., R. D. Fusunyan, I. Sanderson, and W. A. Walker. 2000. Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis. Proc. Natl. Acad. Sci. USA 97: 6043-6048.
44. Grishin, A., J. Wang, D. Hackam, F. Qureshi, J. Upperman, R. Zamora, and H. R. Ford. 2004. p38 MAP kinase mediates endotoxin-induced expression of cyclooxygenase-2 in enterocytes. Surgery 136: 329-335.
45. Nadler, E. P., E. Dickinson, A. Knisely, X. R. Zhang, P. Boyle, D. Beer-Stolz, S. C. Watkins, and H. R. Ford. 2000. Expression of inducible nitric oxide synthase and interleukin-12 in experimental necrotizing enterocolitis. J. Surg. Res. 92: 71-77.
46. Ge, B., H. Gram, F. Di Padova, B. Huang, R. J. Ulevitch, Y. Luo, and J. Han. 2002. MAPKK-independent activation of p38α mediated by TAB1-dependent autophosphorylation of p38α. Science 295: 1291-1294.
47. Livingstone, C., G. Patel, and N. Jones. 1995. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14: 1785-1797.
48. Cetin, S., H. R. Ford, L. R. Sysko, C. Agrawal, J. Wang, M. D. Neal, C. Baty, G. Apodaca, and D. J. Hackam. 2004. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J. Biol. Chem. 279: 24592-24600.
49. Otte, J. M., E. Cario, and D. K. Podolsky. 2004. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126: 1054-1070.
50. 2. Arch. Surg. 129: 1290-1294.
51. Rakoff-Nahum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
52. Faour, W. H., A. Mancini, Q. W. He, and J. A. Di Battista. 2003. T cell-derived interleukin-17 regulates the level and stability of cyclooxygenase-2 mRNA through restricted activation of the p38 mitogen-activated protein kinase cascade: role of distal sequences in the 3′-untranslated region of cyclooxygenase-2 mRNA. J. Biol. Chem. 278: 26897-26907.
53. Dean, J. L., M. Brook, A. R. Clark, and J. Saklatvala. 1999. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J. Biol. Chem. 274: 264-269.