Cytokine induction of NO synthase II in human DLD-1 cells: Roles of the JAK-STAT, AP-1 and NF-κB-signaling pathways

British Journal of Pharmacology

Volumn 125, Issue 1, 1998, Pages 193-201

  Kleinert, Hartmut ^a   Wallerath, Thomas ^a   Fritz, Gerhard ^a   Ihrig Biedert, Irmgard ^a   Rodriguez Pascual, Fernando ^a   Geller, David A ^b   Förstermann, Ulrich ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

AP 1; Janus kinase 2; NF B; Nitric oxide synthase II; STAT1

Indexed keywords

ANISOMYCIN; ARSENOSOBENZENE; CALYCULIN A; CELL EXTRACT; CYTOKINE; DEXAMETHASONE; DNA FRAGMENT; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; NITRIC OXIDE SYNTHASE; NITRITE; OKADAIC ACID; PROTEIN KINASE; PYRROLIDINE DITHIOCARBAMATE; STAT1 PROTEIN; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; TYRPHOSTIN;

ARTICLE; DNA FLANKING REGION; ENZYME INDUCTION; EPITHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; ONCOGENE C FOS; ONCOGENE C JUN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CYTOKINES; DNA; ENZYME INDUCTION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTERFERON TYPE II; INTERFERON-STIMULATED GENE FACTOR 3; INTERLEUKIN-1; JANUS KINASE 2; NF-KAPPA B; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; OKADAIC ACID; OXAZOLES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PLASMIDS; PROMOTER REGIONS (GENETICS); PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; TYRPHOSTINS;

EID: 0031679445     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0702039     Document Type: Article

References (43)

1. ALBRITTON, L.M., BOWCOCK, A.M., EDDY, R.L., MORTON, C.C., TSENG, L., FARRER, L.A., CAVALLI SFORZA, L.L., SHOWS, T.B. & CUNNINGHAM, J.M. (1992). The human cationic amino acid transporter (ATRC1): physical and genetic mapping to 13q13-q14. Genomics, 12, 430-434.
2. CHARLES, I.G., PALMER, R.M.J., HICKERY, M.S., BAYLISS, M.T., CHUBB, A.P., HALL, V.S., MOSS, D.W. & MONCADA, S. (1993). Cloning, characterization, and expression of a cDNA encoding an inducible nitric oxide synthase from the human chondrocyte. Proc. Natl. Acad. Sci. U.S.A., 90, 11419-11423.
3. CHOMCZYNSKI, P. & SACCHI, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
4. DE VERA, M.E., SHAPIRO, R.A., NÜSSLER, A.K., MUDGETT, J.S., SIMMONS, R.L., MORRIS, JR. S.M., BILLIAR, T.R. & GELLER, D.A. (1996). Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. U.S.A., 93, 1054-1059.
5. DONG, Z.Y., YANG, X.L., XIE, K.P., JUANG, S.H., LLANSA, N. & FIDLER, I.J. (1995). Activation of inducible nitric oxide synthase gene in murine macrophages requires protein phosphatases 1 and 2A activities. J. Leukocyte Biol., 58, 725-732.
6. ERKLE, G., ANKE, T. & STERNER, O. (1996). Inhibition of NF-κB activation by panepoxydone. Biochem. Biophys. Res. Commun., 226, 214-221.
7. GAO, J., MORRISON, D.C., PARMELY, T.J., RUSSELL, S.W. & MURPHY, W.J. (1997). An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopolysaccharide. J. Biol. Chem., 272, 1226-1230.
8. GARCIA, M.P., MINAMI, Y., LUONG, E., KLAUSNER, R.D. & SAMELSON, L.E. (1990). Tyrosine phosphorylation in T cells is regulated by phosphatase activity: studies with phenylarsine oxide. Proc. Natl. Acad. Sci. U.S.A., 87, 9255-9259.
9. GELLER, D.A., DE VERA, M.E., RUSSELL, D.A., SHAPIRO, R.A., NUSSLER, A.K., SIMMONS, R.L. & BILLIAR, T.R. (1995). A central role for IL-1 beta in the in vitro and in vivo regulation of hepatic inducible nitric oxide synthase. IL-1 beta induces hepatic nitric oxide synthesis. J. Immunol., 155, 4890-4898.
10. GELLER, D.A., MELLOTT, J., TAYLOR, B.S., NICK, H.S., BILLIAR, T.R. & CHESROW, S.E. (1997). Transcriptional regulation of the human inducible nitric oxide synthase (iNOS) gene. Jap. J. Pharmacol., 75 (suppl 1), 6P.
11. GREEN, L.C., WAGNER, D.A., GLOGOWSKI, J., SKIPPER, P.L., WISHNOK, J.S. & TANNENBAUM, S.R. (1992). Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem., 126, 131-138.
12. HABY, C., AUNIS, D. & ZWILLER, J. (1994). Okadaic acid induces activator protein 1 activity and immediate early gene transcription in rat pheochromocytoma cells. Mechanism of action. Biochem. Pharmacol., 418, 819-825.
13. HATTORI, K., ANGEL, P., LE BEAU, M.M. & KARIN, M. (1988). Structure and chromosomal localizatioan of the functional intronless human JUN protooncogene. Proc. Natl. Acad. Sci. U.S.A., 85, 9148-9152.
14. HATTORI, M., TUGORES, A., WESTWICK, J.K., VELOZ, L., LEFFERT, H.L., KARIN, M. & BRENNER, D.A. (1993). Activation of activating protein 1 during hepatic acute phase response. Am. J. Physiol., 264, G95-G103.
15. HELDIN, C.H., (1995). Dimerizatiaon of cell surface receptors in signal transduction. Cell, 80, 213-223.
16. JAATTELA, M., MOURITZEN, H., ELLING, F. & BASTHOLM, L. (1996). A20 zinc finger protein inhibits TNF and IL-1 signaling. J. Immunol., 156, 1166-1173.
17. JIN, Y., HECK, D.E., DEGEORGE, G., TIAN, Y. & LASKIN, J.D. (1996). 5-fluorouracil suppresses nitric oxide biosynthesis in colon carcinoma cells. Cancer Res., 56, 1978-1982.
18. KITAMURA, Y., TAKAHASHI, H., NOMURA, Y. & TANIGUCHI, T. (1996). Possible involvement of Janus kinase Jak2 in interferon-gamma induction of nitric oxide synthasein rat glial cells. Eur. J. Pharmacol., 306, 297-306.
19. KLEINERT, H., EUCHENHOFER, C., FRITZ, G., IHRIG-BIEDERT, I. & FÖRSTERMANN, U. (1989). Involvement of protein kinases in the induction of NO synthase II in human DLD-1 cells. Brit. J. Pharmacol., 123, 1716-1722.
20. KLEINERT, H., EUCHENHOFER, C., IHRIG-BEIDERT, I. & FÖRSTERMANN, U. (1996a). Glucocorticoids inhibit the induction of nitric oxide synthase II by down-regulating cytokine-induced activity of transcription factor nuclear factor-κB. Mol. Pharmacol., 49, 15-21.
21. KLEINERT, H., EUCHENHOFER, C., IHRIG-BIEDERT, I. & FÖRSTERMANN, U. (1996b). In murine 3T3 fibroblasts, different second messenger pathways resulting in the induction of NO synthase II (iNOS) converge in the activation of transcription factor NF-κB. J. Biol. Chem., 271, 6039-6045.
22. KRÖNCKE, K.D., FEHSEL, K. & BOLB-BACHOFEN, V. (1995). Inducible nitric oxide synthase and its product nitric oxide, a small molecule with complex biological activities. Biol. Chem. Hoppe Seyler, 376, 327-343.
23. LINN, S.C., MORELLI, P.J., EDRY, I., COTTONGIM, S.E., SZABO, C. & SALZMAN, A.L. (1997). Transcriptional regulation of human inducible nitric oxide synthase gene in an intestinal epithelial cell line. Am. J. Physiol., 272, G1499-G1508.
24. LOWENSTEIN, C.J., ALLEY, E.W., RAVAL, P., SNOWMAN, A.M., SNYDER, S.H., RUSSEL, S.W. & MURPHY, W.J. (1993). Macrophage nitric oxide synthase gene two upstream regions mediate induction by interferon-gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. U.S.A., 90, 9730-9734.
25. MENON, S.D., GUY, G.R. & TAN, Y.H. (1995). Involvement of a putative protein-tyrosine phosphatase and I kappa B-alpha serine phosphorylation in nuclear factor kappa B activation by tumor necrosis factor. J. Biol. Chem., 270, 18881-18887.
26. MESSINA, J.L. (1990). Insulin's regulation of c-fos gene transcription in hepatoma cells. J. Biol. Chem., 265, 11700-11705.
27. MEYDAN, N., GRUNBERGER, T., DADI, H., SHAHAR, M., ARPAIA, E., LAPIDOT, Z., LEEDER, J.S., FREEDMAN, M., COHEN, A., GAZIT, A., LEVITZKI, A. & ROIFMAN, C.M. (1996). Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature, 379, 645-648.
28. NATARAJAN, K., SINGH, S., BURKE, JR. T.R., GRUNBERGER, D. & AGGARWAL, B.B. (1996). Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc. Natl. Acad. Sci. U.S.A., 93, 9090-9095.
29. NISHIYA, T., UEHARA, T., EDAMATSU, H., KAZIRO, Y., ITOH, H. & NOMURA, Y. (1997). Activation of Statl and subsequent transcription of inducible nitric oxide synthase gene in C6 glioma cells is independent of interferon-gamma-induced MAPK activation that is mediated by p21ras. FEBS Lett., 408, 33-38.
30. NISHIYA, T., UEHARA, T. & NOMURA, Y. (1995). Herbimycin a suppresses NF-κB activation and tyrosine phosphorylation of JAK2 and the subsequent induction of nitric oxide synthase in c6 glioma cells. FEBS Lett., 371, 333-336.
31. NORDEEN, S.K. (1988). Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques, 6, 454-458.
32. NUNOKAWA, Y., OIKAWA, S. & TANAKA, S. (1996). Human inducible nitric oxide synthase gene is transcriptionally regulated by nuclear factor-κB dependent mechanism. Biochem. Biophys. Res. Commun., 223, 347-352.
33. OGUCHI, S., WEISZ, A. & ESUMI, H. (1994). Enhancement of Inducible-type NO synthase gene transcription by protein synthesis inhibitors activation of an intracellular signal transduction pathway by low concentrations of cycloheximide. FEBS Lett., 338, 326-330.
34. OSBORN, L., KUNKEL, S. & NABEL, G.J. (1989). Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc. Natl. Acad. Sci. U.S.A., 86, 2336-2340.
35. PARK, K., CHUNG, M. & KIM, S.J. (1992). Inhibition of myogenesis by okadaic acid, an inhibitor of protein phosphatases, 1 and 2A, correlates with the induction of API. J. Biol. Chem., 267, 10810-10815.
36. SCHINDLER, C. & DARNELL, J.E. (1995). Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem., 64, 621-651.
37. SHERMAN, P.A., LAUBACH, V.E., REEP, B.R. & WOOD, E.R. (1993). Purification and cDNA sequence of an inducible nitric oxide synthase from a human tumor cell line. Biochemistry, 32, 11600-11605.
38. SINGER, I.I., KAWKA, D.W., SCOTT, S., WEIDNER, J.R., MUMFORD, R.A., RIEHL, T.E. & STENSON, W.F. (1996). Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology, 111, 871-885.
39. SINGH, K., BALLINGAND, J.L., FISCHER, T.A., SMITH, T.W. & KELLY, R.A. (1996). Regulation of cytokine-inducible nitric oxide synthase in cardiac myocytes and microvascular endothelial cells - role of extracellular signal-regulated kinases 1 and 2 (ERK1/ERK2) and STAT1 alpha. J. Biol. Chem., 271, 1111-1117.
40. SPITSIN, S.V., KOPROWSKI, H. & MICHAELS, F.H. (1996). Characterization and functional analysis of the human inducible nitric oxide synthase gene promoter. Mol. Medicine, 2, 226-235.
41. THANOS, D. & MANIATIS, T. (1995). NF-kappa B: a lesson in family values. Cell, 80, 529-532.
42. VAN STRAATEN, F., MULLER, R., CURRAN, T., VAN BEVEREN, C. & VERMA, I.M. (1983). Complete nucleotide sequence of a human c-onc gene: deduced amino acid sequence of the human c-fos protein. Proc. Natl. Acad. Sci. U.S.A., 80, 3183-3187.
43. XIE, Q.W., KASHIWABARA, Y. & NATHAN, C. (1994). Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem., 269, 4705-4708.