Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Inhibition of Nitric Oxide Production by Ethyl Digallates Isolated from Galla Rhois in RAW 264.7 Macrophages

  • Park, Pil-Hoon (College of Pharmacy, Yeungnam University) ;
  • Hur, Jin (Institute of Pharmaceutical Research and Development, Department of Pharmacy, Wonkwang University) ;
  • Lee, Dong-Sung (Standardized Material Bank for New Botanical Drugs, College of Pharmacy, Wonkwang University) ;
  • Kim, Youn-Chul (Standardized Material Bank for New Botanical Drugs, College of Pharmacy, Wonkwang University) ;
  • Jeong, Gil-Saeng (College of Pharmacy, Keimyung University) ;
  • Sohn, Dong-Hwan (Institute of Pharmaceutical Research and Development, Department of Pharmacy, Wonkwang University)
  • Received : 2011.07.29
  • Accepted : 2011.09.22
  • Published : 2011.10.30
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Abstract

Galla Rhois and its components are known to possess anti-infl ammatory properties. In the present study, we prepared equilibrium mixture of ethyl m-digallate and ethyl p-digallate isomers (EDG) from Galla Rhois and examined its effect on nitric oxide (NO) production in murine macrophage cell line. Treatment of RAW264.7 macrophages with EDG signifi cantly inhibited NO production and inducible nitric oxide synthase (iNOS) expression stimulated by LPS, as assessed by Western blot and quantitative RT-PCR analyses. We also demonstrated that EDG treatment led to an increase in heme oxygenase-1 (HO-1) mRNA and protein expression. EDG treatment also enhanced expression level of nuclear factor-erythroid 2-related factor 2 (Nrf2) in nucleus, which is critical for transcriptional induction of HO-1. Treatment with SnPP (tin protoporphyrin IX), a selective HO-1 inhibitor, reversed EDG-mediated inhibition of nitrite production, suggesting that HO-1 plays an important role in the suppression of NO production by EDG. Taken together, these results indicate that EDG isolated from Galla Rhois suppresses LPS-stimulated NO production in RAW 264.7 macrophages via HO-1 induction.

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References

  1. Alcaraz, M. J., Vicente, A. M., Araico A., Dominguez J. N., Terencio M.C. and Ferrandiz, M. L. (2004) Role of nuclear factor-kappaB and heme oxygenase-1 in the mechanism of action of an anti-infl ammatory chalcone derivative in RAW 264.7 cells. Br. J. Pharmacol. 142, 1191-1199. https://doi.org/10.1038/sj.bjp.0705821
  2. An, R. B., Oh, H. and Kim, Y. C. (2005) Phenolic constituents of galla Rhois with hepatoprotective effects on tacrine- and nitrofurantoininduced cytotoxicity in Hep G2 cells. Biol. Pharm. Bull. 28, 2155-2157. https://doi.org/10.1248/bpb.28.2155
  3. Ata, N., Oku, T., Hattori, M., Fujii, H., Nakajima, M. and Saiki, I. (1996) Inhibition by galloylglucose (GG6-10) of tumor invasion through extracellular matrix and gelatinase-mediated degradation of type IV collagens by metastatic tumor cells. Oncol. Res. 8, 503-511.
  4. Colasanti, M. and Suzuki, H. (2000) The dual personality of NO. Trends. Pharmacol. Sci. 21, 249-252. https://doi.org/10.1016/S0165-6147(00)01499-1
  5. Deaciuc, I. V., Doherty, D. E., Burikhanov, R., Lee, E. Y., Stromberg, A. J., Peng, X. and de Villiers, W. J. (2004) Large-scale gene profi ling of the liver in a mouse model of chronic, intragastric ethanol infusion. J. Hepatol. 40, 219-227. https://doi.org/10.1016/j.jhep.2003.10.021
  6. Dijkstra, G., Blokzijl, H., Bok, L., Homan, M., van Goor, H., Faber, K. N., Jansen, P. L. and Moshage, H. (2004) Opposite effect of oxidative stress on inducible nitric oxide synthase and haem oxygenase-1 expression in intestinal infl ammation: anti-infl ammatory effect of carbon monoxide. J. Pathol. 204, 296-303. https://doi.org/10.1002/path.1656
  7. Hsu, H. Y., Chu, L. C., Hua, K. F. and Chao, L. K. (2008) Heme oxygenase- 1 mediates the anti-infl ammatory effect of Curcumin within LPS-stimulated human monocytes. J. Cell. Physiol. 215, 603-612. https://doi.org/10.1002/jcp.21206
  8. Jung, H. J., Kim, S. J., Jeon, W. K., Kim, B. C., Ahn, K., Kim, K., Kim, Y. M., Park, E. H. and Lim, C. J. (2010) Anti-infl ammatory Activity of n-Propyl Gallate Through Down-regulation of NF-kappaB and JNK Pathways. Infl ammation. 34, 352-361.
  9. Kang, M. S., Oh, J. S., Kang, I. C., Hong, S. J. and Choi, C. H. (2008) Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J. Microbiol. 46, 744-750. https://doi.org/10.1007/s12275-008-0235-7
  10. Kroncke, K. D., Fehsel, K. and Kolb-Bachofen, V. (1997) Nitric oxide: cytotoxicity versus cytoprotection--how, why, when, and where? Nitric. Oxide. 1, 107-120. https://doi.org/10.1006/niox.1997.0118
  11. Kwak, M. K., Itoh, K., Yamamoto, M. and Kensler, T. W. (2002) Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell Biol. 22, 2883-2892. https://doi.org/10.1128/MCB.22.9.2883-2892.2002
  12. Lee, S. H., Kim, J. Y., Seo, G. S., Kim, Y. C. and Sohn, D. H. (2009) Isoliquiritigenin, from Dalbergia odorifera, up-regulates anti-infl ammatory heme oxygenase-1 expression in RAW264.7 macrophages. Infl amm. Res. 58: 257-262. https://doi.org/10.1007/s00011-008-8183-6
  13. Lee, S. H., Seo, G. S. and Sohn, D. H. (2004) Inhibition of lipopolysaccharide- induced expression of inducible nitric oxide synthase by butein in RAW 264.7 cells. Biochem. Biophys. Res. Commun. 323, 125-132. https://doi.org/10.1016/j.bbrc.2004.08.063
  14. Lin, Y. L. and Lin, J. K. (1997) (-)-Epigallocatechin-3-gallate blocks the induction of nitric oxide synthase by down-regulating lipopolysaccharide- induced activity of transcription factor nuclear factor-kappaB. Mol. Pharmacol. 52, 465-472.
  15. Lowenstein, C. J., Dinerman, J. L. and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger. Ann. Intern. Med. 120, 227-237. https://doi.org/10.7326/0003-4819-120-3-199402010-00009
  16. Maines, M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554. https://doi.org/10.1146/annurev.pharmtox.37.1.517
  17. Mashimo, H. and Goyal, R. K. (1999) Lessons from genetically engineered animal models. IV. Nitric oxide synthase gene knockout mice. Am. J. Physiol. 277, G745-G750.
  18. Melgarejo, E., Medina, M. A., Sanchez-Jimenez, F. and Urdiales, J. L. (2010) Targeting of histamine producing cells by EGCG: a green dart against infl ammation? J. Physiol. Biochem. 66, 265-270. https://doi.org/10.1007/s13105-010-0033-7
  19. Murase, T., Kume, N., Hase, T., Shibuya, Y., Nishizawa, Y., Tokimitsu, I. and Kita, T. (1999) Gallates inhibit cytokine-induced nuclear translocation of NF-kappaB and expression of leukocyte adhesion molecules in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 19, 1412-1420. https://doi.org/10.1161/01.ATV.19.6.1412
  20. Nguyen, T., Sherratt, P. J., Huang, H. C., Yang, C. S. and Pickett, C. B. (2003) Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J. Biol. Chem. 278, 4536-4541. https://doi.org/10.1074/jbc.M207293200
  21. Otterbein, L. E., Soares, M. P., Yamashita, K. and Bach, F. H. (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24, 449-455. https://doi.org/10.1016/S1471-4906(03)00181-9
  22. Paine, A., Eiz-Vesper, B., Blasczyk, R. and Immenschuh, S. (2010) Signaling to heme oxygenase-1 and its anti-infl ammatory therapeutic potential. Biochem. Pharmacol. 80, 1895-1903. https://doi.org/10.1016/j.bcp.2010.07.014
  23. Prawan, A., Kundu, J. K. and Surh, Y. J. (2005) Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxid. Redox. Signal 7, 1688-1703. https://doi.org/10.1089/ars.2005.7.1688
  24. Radtke, O. A., Kiderlen, A. F., Kayser, O. and Kolodziej, H. (2004) Gene expression profi les of inducible nitric oxide synthase and cytokines in Leishmania major-infected macrophage-like RAW 264.7 cells treated with gallic acid. Planta. Med. 70, 924-928. https://doi.org/10.1055/s-2004-832618
  25. Ruan, R. S. (2002) Possible roles of nitric oxide in the physiology and pathophysiology of the mammalian cochlea. Ann. N. Y. Acad. Sci. 962, 260-274. https://doi.org/10.1111/j.1749-6632.2002.tb04073.x
  26. Ryter, S. W. and Tyrrell, R. M. (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28, 289-309. https://doi.org/10.1016/S0891-5849(99)00223-3
  27. Sawle, P., Foresti, R., Mann, B. E., Johnson, T. R., Green, C. J. and Motterlini, R. (2005) Carbon monoxide-releasing molecules (CORMs) attenuate the infl ammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages. Br. J. Pharmacol. 145, 800-810. https://doi.org/10.1038/sj.bjp.0706241
  28. Son, E., Jeong, J., Lee, J., Jung, D. Y., Cho, G. J., Choi, W. S., Lee, M. S., Kim, S. H., Kim, I. K. and Suk, K. (2005) Sequential induction of heme oxygenase-1 and manganese superoxide dismutase protects cultured astrocytes against nitric oxide. Biochem. Pharmacol. 70, 590-597. https://doi.org/10.1016/j.bcp.2005.05.027
  29. Stewart, D., Killeen, E., Naquin, R., Alam, S. and Alam, J. (2003) Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 278, 2396-2402. https://doi.org/10.1074/jbc.M209195200
  30. Tipoe, G. L., Leung, T. M., Liong, E. C., Lau, T. Y., Fung, M. L. and Nanji, A. A. (2010) Epigallocatechin-3-gallate (EGCG) reduces liver infl ammation, oxidative stress and fi brosis in carbon tetrachloride (CCl4)-induced liver injury in mice. Toxicology 273, 45-52. https://doi.org/10.1016/j.tox.2010.04.014

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