Phenethyl isothiocyanate suppresses nitric oxide production via inhibition of phosphoinositide 3-kinase/Akt-induced IFN-γ secretion in LPS-activated peritoneal macrophages

Molecular Nutrition and Food Research

Volumn 54, Issue 9, 2010, Pages 1351-1360

  Okubo, Toru ^a   Washida, Kazuto ^b   Murakami, Akira ^a  

^a KYOTO UNIVERSITY   (Japan)

^b The Nara Prefectural Agricultural Experiment Station   (Japan)

Author keywords

Inflammation; Interferon ; LPS; Nitric oxide; Phenethyl isothiocyanate

Indexed keywords

GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; ISOTHIOCYANIC ACID DERIVATIVE; LIPOPOLYSACCHARIDE; MESSENGER RNA; NEUTRALIZING ANTIBODY; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; NOS2 PROTEIN, MOUSE; PHENETHYL ISOTHIOCYANATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR;

ANIMAL; ARTICLE; BLOOD; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MACROPHAGE ACTIVATION; MALE; METABOLISM; MOUSE; ORAL DRUG ADMINISTRATION; PERITONEUM MACROPHAGE; SECRETION; SIGNAL TRANSDUCTION;

ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIBODIES, NEUTRALIZING; CELLS, CULTURED; GENE EXPRESSION REGULATION; INTERFERON-GAMMA; INTERLEUKIN-12; ISOTHIOCYANATES; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED ICR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION;

MUS;

EID: 77957059129     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200900318     Document Type: Article

References (49)

1. Davis, K., Martin, E., Turko, I., Murad, F., Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 2001, 41, 203-236.
2. Kröncke, K., Fehsel, K., Kolb-Bachofen, V., Inducible nitric oxide synthase in human diseases. Clin. Exp. Immunol. 1998, 113, 147-156.
3. Kleinert, H., Pautz, A., Linker, K., Schwarz, P., Regulation of the expression of inducible nitric oxide synthase. Eur. J. Pharmacol. 2004, 500, 255-266.
4. Xie, Q., Kashiwabara, Y., Nathan, C., Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 1994, 269, 4705-4708.
5. Gao, J., Morrison, D., Parmely, T., Russell, S., Murphy, W., 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. 1997, 272, 1226-1230.
6. Xie, Q., Whisnant, R., Nathan, C., Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 1993, 177, 1779-1784.
7. Mancuso, G., Midiri, A., Biondo, C., Beninati, C. et al., Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J. Immunol. 2007, 178, 3126-3133.
8. Matsuura, M., Saito, S., Hirai, Y., Okamura, H., A pathway through interferon-gamma is the main pathway for induction of nitric oxide upon stimulation with bacterial lipopolysaccharide in mouse peritoneal cells. Eur. J. Biochem. 2003, 270, 4016-4025.
9. Schwacha, M., Eisenstein, T., Interleukin-12 is critical for induction of nitric oxide-mediated immunosuppression following vaccination of mice with attenuated Salmonella typhimurium. Infect. Immun. 1997, 65, 4897-4903.
10. Clemons-Miller, A., Cox, G., Suttles, J., Stout, R., LPS stimulation of TNF-receptor deficient macrophages: a differential role for TNF-alpha autocrine signaling in the induction of cytokine and nitric oxide production. Immunobiology 2000, 202, 477-492.
11. Park, S., Lee, S., Hong, S., Kim, H., Degradation of Ikappa-Balpha in activated RAW264.7 cells is blocked by the phosphatidylinositol 3-kinase inhibitor LY294002. Cell Biol. Toxicol. 2002, 18, 121-130.
12. Ojaniemi, M., Glumoff, V., Harju, K., Liljeroos, M. et al., Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 2003, 33, 597-605.
13. Jung, Y., Kim, M., Lee, K., Kang, I. et al., 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002) inhibits nitric oxide production in cultured murine astrocytes. Pharmacol. Res. 1999, 40, 423-427.
14. Weinstein, S., Finn, A., Davé, S., Meng, F. et al., Phosphatidylinositol 3-kinase and mTOR mediate lipopolysaccharide-stimulated nitric oxide production in macrophages via interferon-beta. J. Leukoc. Biol. 2000, 67, 405-414.
15. Palaniswamy, U., McAvoy, R., Bible, B., Stuart, J., Ontogenic variations of ascorbic acid and phenethyl isothiocyanate concentrations in watercress (Nasturtium officinale R.Br.) leaves. J. Agric. Food. Chem. 2003, 51, 5504-5509.
16. Uematsu, Y., Hirata, K., Suzuki, K., Iida, K. et al., Determination of isothiocyanates and related compounds in mustard extract and horseradish extract used as natural food additives. Shokuhin Eiseigaku Zasshi 2002, 43, 10-17.
17. Xu, C., Yuan, X., Pan, Z., Shen, G. et al., Mechanism of action of isothiocyanates: the induction of ARE-regulated genes is associated with activation of ERK and JNK and the phosphorylation and nuclear translocation of Nrf2. Mol. Cancer Ther. 2006, 5, 1918-1926.
18. Rose, P., Whiteman, M., Huang, S., Halliwell, B., Ong, C., Beta-phenylethyl isothiocyanate-mediated apoptosis in hepatoma HepG2 cells. Cell Mol. Life Sci. 2003, 60, 1489-1503.
19. Xiao, D., Singh, S., Phenethyl isothiocyanate inhibits angiogenesis in vitro and ex vivo. Cancer Res. 2007, 67, 2239-2246.
20. Rose, P., Won, Y., Ong, C., Whiteman, M., Beta-phenylethyl and 8-methylsulphinyloctyl isothiocyanates, constituents of watercress, suppress LPS induced production of nitric oxide and prostaglandin E2 in RAW 264.7 macrophages. Nitric Oxide 2005, 12, 237-243.
21. Dey, M., Ribnicky, D., Kurmukov, A., Raskin, I., In vitro and in vivo anti-inflammatory activity of a seed preparation containing phenethylisothiocyanate. J. Pharmacol. Exp. Ther. 2006, 317, 326-333.
22. Barillari, J., Gueyrard, D., Rollin, P., Iori, R., Barbarea verna as a source of 2-phenylethyl glucosinolate, precursor of cancer chemopreventive phenylethyl isothiocyanate. Fitoterapia 2001, 72, 760-764.
23. Okugawa, S., Ota, Y., Kitazawa, T., Nakayama, K. et al., Janus kinase 2 is involved in lipopolysaccharide-induced activation of macrophages. Am. J. Physiol. Cell Physiol. 2003, 285, C399-C408.
24. Samten, B., Townsend, J., Weis, S., Bhoumik, A. et al., CREB, ATF, and AP-1 transcription factors regulate IFNgamma secretion by human T cells in response to mycobacterial antigen. J. Immunol. 2008, 181, 2056-2064.
25. Lin, Y., Brown, K., Siebenlist, U., Activation of NF-kappa B requires proteolysis of the inhibitor I kappa B-alpha: signalinduced phosphorylation of I kappa B-alpha alone does not release active NF-kappa B. Proc. Natl. Acad. Sci. USA 1995, 92, 552-556.
26. Uto, T., Fujii, M., Hou, D., 6-(Methylsulfinyl)hexyl isothiocyanate suppresses inducible nitric oxide synthase expression through the inhibition of Janus kinase 2-mediated JNK pathway in lipopolysaccharide-activated murine macrophages. Biochem. Pharmacol. 2005, 70, 1211-1221.
27. Dell'Albani, P., Santangelo, R., Torrisi, L., Nicoletti, V. et al., JAK/STAT signaling pathway mediates cytokine-induced iNOS expression in primary astroglial cell cultures. J. Neurosci. Res. 2001, 65, 417-424.
28. Frucht, D., Fukao, T., Bogdan, C., Schindler, H. et al., IFNgamma production by antigen-presenting cells: mechanisms emerge. Trends Immunol. 2001, 22, 556-560.
29. Fultz, M., Barber, S., Dieffenbach, C., Vogel, S., Induction of IFN-gamma in macrophages by lipopolysaccharide. Int. Immunol. 1993, 5, 1383-1392.
30. Salins, S., Newton, C., Widen, R., Klein, T., Friedman, H., Differential induction of gamma interferon in Legionella pneumophila-infected macrophages from BALB/c and A/J mice. Infect. Immun. 2001, 69, 3605-3610.
31. Freudenberg, M., Merlin, T., Kalis, C., Chvatchko, Y. et al., Cutting edge: a murine, IL-12-independent pathway of IFNgamma induction by gram-negative bacteria based on STAT4 activation by Type I IFN and IL-18 signaling. J. Immunol. 2002, 169, 1665-1668.
32. Stefanová, I., Corcoran, M., Horak, E., Wahl, L. et al., Lipopolysaccharide induces activation of CD14-associated protein tyrosine kinase p53/56lyn. J. Biol. Chem. 1993, 268, 20725-20728.
33. Herrera-Velit, P., Reiner, N., Bacterial lipopolysaccharide induces the association and coordinate activation of p53/56lyn and phosphatidylinositol 3-kinase in human monocytes. J. Immunol. 1996, 156, 1157-1165.
34. Penix, L., Sweetser, M., Weaver, W., Hoeffler, J. et al., The proximal regulatory element of the interferon-gamma promoter mediates selective expression in T cells. J. Biol. Chem. 1996, 271, 31964-31972.
35. Sica, A., Dorman, L., Viggiano, V., Cippitelli, M. et al., Interaction of NF-kappaB and NFAT with the interferongamma promoter. J. Biol. Chem. 1997, 272, 30412-30420.
36. Kiani, A., García-Cózar, F., Habermann, I., Laforsch, S. et al., Regulation of interferon-gamma gene expression by nuclear factor of activated T cells. Blood 2001, 98, 1480-1488.
37. Nguyen, K., Watford, W., Salomon, R., Hofmann, S. et al., Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 2002, 297, 2063-2066.
38. Szabo, S., Sullivan, B., Stemmann, C., Satoskar, A. et al., Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002, 295, 338-342.
39. Lin, W., Wu, R., Wu, T., Khor, T. et al., Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem. Pharmacol. 2008, 76, 967-973.
40. Xue, B., Wu, Y., Yin, Z., Zhang, H. et al., Regulation of lipopolysaccharide-induced inflammatory response by glutathione S-transferase P1 in RAW264.7 cells. FEBS Lett. 2005, 579, 4081-4087.
41. Wang, T., Arifoglu, P., Ronai, Z., Tew, K., Glutathione S-transferase P1-1 (GSTP1-1) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus. J. Biol. Chem. 2001, 276, 20999-21003.
42. Wu, Y., Fan, Y., Xue, B., Luo, L. et al., Human glutathione Stransferase P1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals. Oncogene 2006, 25, 5787-5800.
43. Luo, L., Wang, Y., Feng, Q., Zhang, H. et al., Recombinant protein glutathione S-transferases P1 attenuates inflammation in mice. Mol. Immunol. 2008.
44. Hayes, J., Kelleher, M., Eggleston, I., The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur. J. Nutr. 2008, 47, 73-88.
45. Nakamura, Y., Morimitsu, Y., Uzu, T., Ohigashi, H. et al., A glutathione S-transferase inducer from papaya: rapid screening, identification and structure-activity relationship of isothiocyanates. Cancer Lett. 2000, 157, 193-200.
46. Ku, K., Huang, Y., Huang, Y., Chiou, W., Miyabenol A inhibits LPS-induced NO production via IKK/IkappaB inactivation in RAW 264.7 macrophages: possible involvement of the p38 and PI3K pathways. J. Agric. Food Chem. 2008, 56, 8911-8918.
47. Verhoeven, D., Goldbohm, R., van Poppel, G., Verhagen, H., van den Brandt, P., Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiol. Biomarkers Prev. 1996, 5, 733-748.
48. Ohshima, H., Bartsch, H., Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat. Res. 1994, 305, 253-264.
49. Elfoul, L., Rabot, S., Khelifa, N., Quinsac, A. et al., Formation f allyl isothiocyanate from sinigrin in the digestive tract of rats monoassociated with a human colonic strain of Bacteroides thetaiotaomicron. FEMS Microbiol. Lett. 2001, 197, 99-103.