Attenuation of inducible nitric oxide synthase gene expression by Δ9- tetrahydrocannabinol is mediated through the inhibition of nuclear factor- κB/Rel activation

Molecular Pharmacology

Volumn 50, Issue 2, 1996, Pages 334-341

  Jeon, Young J ^b   Yang, Kyu H ^b   Pulaski, Jim T ^a   Kaminski, Norbert E ^a,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TETRAHYDROCANNABINOL;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; FEMALE; GENE EXPRESSION; IMMUNE RESPONSE; MACROPHAGE ACTIVATION; MOUSE; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; STRUCTURE ACTIVITY RELATION;

ACTIVATING TRANSCRIPTION FACTOR 2; ANIMALS; BASE SEQUENCE; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; FORSKOLIN; GENE EXPRESSION REGULATION; INTERFERON TYPE II; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; NITRIC OXIDE SYNTHASE; NITRITES; TETRAHYDROCANNABINOL; TRANSCRIPTION FACTORS;

EID: 0029790065     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (36)

1. Herkenham, M., A. B. Lynn, M. D. Little, M. R. Johnson, L. S. Melvin, B. R. de Costa, and K. C. Rice. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. USA 87:1932-1936 (1990).
2. 9-THC-DMH. J. Pharmacol. Exp. Ther. 263:1383-1390 (1992).
3. Kaminski, N. E., M. E. Abood, F. K. Kessler, B. R. Martin, and A. R. Schatz. Identification of a functionally relevant cannabinoid receptor on mouse spleen cells that is involved in cannabinoid-mediated immune modulation. Mol. Pharmacol. 42:736-742 (1992).
4. Munro, S., K. L. Thomas, and M. Abu-Shaar. Molecular characterization of a peripheral receptor for cannabinoids. Nature (Lond.) 365:61-65 (1993).
5. Matsuda, L. A., S. J. Lolait, M. J. Brownstein, A. C. Young, and T. I. Bonner. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature (Lond.) 348:561-564 (1990).
6. Kaminski, N. E., W. S. Koh, M. Lee, K. H. Yang, and F. K. Kessler. Suppression of the humoral immune response by cannabinoids is partially mediated through inhibition of adenylate cyclase by a pertussis toxin-sensitive G-protein coupled mechanism. Biochem. Pharmacol. 48:1899-1908 (1994).
7. Bouaboula, M., M. Rinaldi, P. Carayon, C. Carillon, B. Delpech, D. Shire, G. Le Fur, and P. Casellas. Cannabinoid-receptor expression in human leukocytes. Eur. J. Biochem. 214:173-180 (1993).
8. Facci, L., R. Dal Toso, S. Romanello, A. Buriani, D. Skaper, and A. Leon. Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. Proc. Natl. Acad. Sci. USA 92:3376-3380 (1995).
9. Palmer, R. M. J., D. S. Ashton, and S. Moncada. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature (Lond.) 333:664-666 (1988).
10. Hibbs, J. B., R. R. Taintor, and Z. Vavrin. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science (Washington D. C.) 235:473-476 (1987).
11. Lowenstein, C. J., E. W. Alley, P. Raval, A. M. Snowman, S. H. Snyder, S. W. Russell, and W. J. Murphy. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by Interferon γ and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90:9730-9734 (1993).
12. Xie, Q., Y. Kashiwabara, and C. Nathan. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269:4705-4708 (1994).
13. Grilli, M., J.-S. Chiu, and M. Lenardo. NF-κB and Rel, participants in a multiform transcriptional regulatory system, in International Review of Cytology: A Survey of Cell Biology. Academic Press, San Diego, 1-62 (1993).
14. Shirakawa, F., and S. B. Mizel. In vitro activation and nuclear translocation of NF-κB catalyzed by cyclic AMP-dependent protein kinase and protein kinase C. Mol. Cell. Biol. 9:2424-2430 (1989).
15. Muroi, M., and T. Suzuki. Role of protein kinase A in LPS-induced activation of NK-κB proteins of a mouse macrophage-like cell-line, J774. Cell. Signalling 5:289-298 (1993).
16. Novotney, M., Z.-L. Chang, H. Uchiyama, and T. Suzuki. Protein kinase C in tumoricidal activation of mouse macrophage cell lines. Biochemistry 30:5597-5604 (1991).
17. Koide, M., Y. Kawahara, I. Nakayama, T. Tsuda, and M. Yokoyama. Cyclic AMP-elevating agents induce an inducible type of nitric oxide synthase in cultured vascular smooth muscle cells. J. Biol. Chem. 268:24959-24966 (1993).
18. Alonso, A., J. Carvalho, S. Alonso-Torre, L. Nunez, L. Bosca, and M. Crespo. Nitric oxide synthesis in rat peritoneal macrophages is induced by IgE/DNP complexes and cyclic AMP analogues: evidence in favor of a common signaling mechanism. J. Immunol. 154:6475-6483 (1995).
19. 15N]nitrate in biological fluids. Anal. Biochem. 128:131-138 (1982).
20. Vanden Heuvel, J., G. Clark, M. Kohn, A. Tritscher, W. Greenlee, G. Lucier, and D. Bell. Dioxin-responsive genes: examination of dose-response relationships using quantitative reverse transcriptase-polymerase chain reaction. Cancer Res. 54:62-68 (1994).
21. Vanden Heuvel, J., F. Tyson, and D. Bell. Construction of recombinant RNA templates for use as internal standards in quantitative RT-PCR. Biotechniques 14:395-398 (1993).
22. Chomczynski, P., and K. Mackey. Substitution of chloroform by bromochloropropane in the single-strip method of RNA isolation. Anal. Biochem. 225:163-164 (1995).
23. Gilliland, G., K. Perrin, K. Blanchard, and H. Bunn. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc. Natl. Acad. Sci. USA 87:2725-2729 (1990).
24. Gilliland, G., S. Perrin, and H. Bunn. Competitive PCR for quantitation of mRNA, in PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, 60-66 (1990).
25. Xie, H., T. C. Chiles, and T. L. Rothstein. Induction of CREB activity via the surface Ig receptor of B cells. J. Immunol. 151:880-889 (1993).
26. Montminy, M. R., K. A. Sevarino, J. A. Wagner, and G. Mandel. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl. Acad. Sci. USA 83:6682-6686 (1986).
27. Pierce, J. W., M. Lenardo, and D. Baltimore. Oligonucleotide that binds nuclear factor NF-κB acts as a lymphoid-specific and inducible enhancer element. Proc. Natl. Acad. Sci. USA 85:1482-1486 (1988).
28. Lee, H. J., E. S. Masuda, N. Arai, K. Arai, and T. Yokota. Definition of cis-regulatory elements of the mouse interleukin-5 gene promoter. J. Biol. Chem. 270:17541-17550 (1995).
29. Dunnett, C. W. A multiple comparison procedure for comparing several treatments with a control. J. Am. Statistics Assoc. 50:1096-1121 (1955).
30. Schreck, R., B. Meier, D. N., Mannel, W. Droge, and P. A. Bauerle. Dithiocarbamates as potent inhibitors of NF-κB activation in intact cells. J. Exp. Med. 175:1181-1194 (1992).
31. Lynn, A. B., and M. Herkenham. Localization of cannabinoid receptors and nonsaturable high-density cannabinoid binding sites in peripheral tissues of the rat: implications for receptor-mediated immune modulation by cannabinoids. J. Pharmacol. Exp. Ther. 268:1612-1623 (1994).
32. Howlett, A. C. Cannabinoid inhibition of adenylate cyclase: biochemistry of the response in neuroblastoma cell membranes. Mol. Pharmacol. 27: 429-436 (1985).
33. 9-tetrahydrocannabinol in mouse spleen cells: a potential mechanism for cannabinoid-mediated immunosuppression. Life Sci. 51: 25-30 (1992).
34. Shirakawa, F., M. Chedid, J. Suttles, B. A. Pollok, and S. B. Mizel. Interleukin-1 and cyclic AMP induce K immunoglobulin light-chain expression via activation of an NF-κB-like DNA-binding protein. Mol. Cell. Biol. 9:959-964 (1989).
35. Ghosh, S., and D. Baltimore. Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature (Lond.) 344:678-682 (1990).
36. Condie, R., A. Herring, W. S. Koh, M. Lee, and N. E. Kaminski. Cannabinoid inhibition of adenylate cyclase-mediated signal transduction and IL-2 expression in the murine T-cell line. EL4-IL-2. J. Biol. Chem. 271:13175-13183 (1996).