Involvement of heme oxygenase-1 induction in the cytoprotective and immunomodulatory activities of 6,4′-dihydroxy-7-methoxyflavanone in murine hippocampal and microglia cells

European Journal of Pharmacology

Volumn 674, Issue 2-3, 2012, Pages 153-162

  Li, Bin ^a   Lee, Dong Sung ^a   Jeong, Gil Saeng ^b   Kim, Youn Chul ^a  

^a Wonkwang University   (South Korea)

^b Keimyung University   (South Korea)

Author keywords

BV2 microglia; DMF (6,4 Dihydroxy 7 methoxyflavanone); HO (Heme oxygenase) 1; HT22 cell; MAPK activation

Indexed keywords

6 4' DIHYDROXY 7 METHOXYFLAVANONE; FLAVANONE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME ACTIVITY; HIPPOCAMPUS; IMMUNOMODULATION; MICROGLIA; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; CELL LINE; CYTOKINES; CYTOPROTECTION; ENZYME INDUCTION; FLAVANONES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMIC ACID; HEME OXYGENASE-1; HIPPOCAMPUS; IMMUNOLOGIC FACTORS; LIPOPOLYSACCHARIDES; MAP KINASE SIGNALING SYSTEM; MICE; MICROGLIA; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES;

EID: 84855556681     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2011.11.016     Document Type: Article

References (72)

1. Ahn, S.C., Kim, G.Y., Kim, J.H., Baik, S.W., Han, M.K., Lee, H.J., Moon, D.O., Lee, C.M., Kang, J.H., Kim, B.H., Oh, Y.H., Park, Y.M., 2004. Epigallocatechin-3-gallate, constituent of green tea, suppresses the LPS-induced phenotypic and functional maturation of murine dendritic cells through inhibition of mitogen-activated protein kinases and NF-kappaB. Biochem. Biophys. Res. Commun. 313, 148-155.
2. An, R.B., Jeong, G.S., Kim, Y.C., 2008. Flavonoids fromthe heartwood of Dlabergia odorifera and their protective effect on glutamate-induced oxidative injury inHT22 cells. Chem. Pharm. Bull. 56, 1722-1724.
3. Banati, R.B., Rothe, G., Valet, G., Kreutzberg, G.W., 1991. Respiratory burst activity in brain macrophages: a flow cytometric study on cultured rat microglia. Neuropath. Appl. Neuro. 17, 223-230.
4. Block, M.L., Hong, J.S., 2005. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76, 77-98. (Pubitemid 41242883)
5. Chan, S.C., Chang, Y.S., Wang, J.P., Chen, S.C., Kuo, S.C., 1998. Three new flavonoids and antiallergic, anti-inflammatory constituents fromthe heartwood of Dalbergia odorifera. Planta Med. 64, 153-158.
6. Chao, C.C., Hu, S., Molitor, T.W., Shaskan, E.G., Peterson, P.K., 1992. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Neurosci. Res. 149, 2736-2741.
7. Choi, D.W., 1988. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
8. Choi, B.M., Kim, H.J., Oh, G.S., Pae, H.O., Oh, H.C., Jeong, S.J., Kwon, T.O., Kim, Y.M., Chung, H.T., 2002. 1,2,3,4,6-Penta-O-galloyl-beta-D-glucose protects rat neuronal cells (Neuro 2A) from hydrogen peroxide-mediated cell death via the induction of heme oxygenase-1. Neurosci. Lett. 328, 185-189.
9. Choi, B.M., Lim, D.W., Lee, J.A., Gao, S.S., Kwon, D.Y., Kim, B.R., 2008. Luteolin suppresses cisplatin-induced apoptosis in auditory cells: possible mediation through induction of heme oxygenase-1 expression. J. Med. Food 11, 230-236. (Pubitemid 351948178)
10. Chora, A.A., Fontoura, P., Cunha, A., Pais, T.F., Cardoso, S., Ho, P.P., Lee, L.Y., Sobel, R.A., Steinman, L., Soares, M.P., 2007. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J. Clin. Invest. 117, 438-447. (Pubitemid 46203972)
11. Coyle, J.T., Puttfarcken, P., 1993. Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695. (Pubitemid 23350687)
12. Das, S., Tosaki, A., Bagchi, D., Maulik, N., Das, D.K., 2006. Potentiation of a survival signal in the ischemic heart by resveratrol through p38 mitogen-activated protein kinase/mitogen- and stress-activated protein kinase 1/cAMP response elementbinding protein signaling. J. Pharmacol. Exp. Ther. 317, 980-988. (Pubitemid 43764100)
13. Dore, S., Takahashi, M., Ferris, C.D., Zakhary, R., Hester, L.D., Guastella, D., Snyder, S.H., 1999. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl. Acad. Sci. U.S.A. 96, 2445-2450. (Pubitemid 29117935)
14. Elbirt, K.K., Whitmarsh, A.J., Davis, R.J., Bonkovsky, H.L., 1998. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases. J. Biol. Chem. 273, 8922-8931. (Pubitemid 28176175)
15. Fagone, P., Mangano, K., Quattrocchi, C., Motterlini, R., Di Marco, R., Magro, G., Penacho, N., Romao, C.C., Nicoletti, F., 2010. Prevention of clinical and histological signs of proteolipid protein (PLP)-induced experimental allergic encephalomyelitis (EAE) in mice by the water-soluble carbon monoxide-releasing molecule (CORM)-A1. Clin. Exp. Immunol. 163, 368-374.
16. Gibson,G.E., Zhang, H., 2001. Abnormalities in oxidative processes in non-neuronal tissues from patients with Alzheimer's disease. J. Alzheimers Dis. 3, 329-338. (Pubitemid 32577637)
17. Giulian, D., Haverkamp, L.J., Yu, J.H., Karshin, W., Tom, D., Li, J., Kirkpatrick, J., Kuo, L.M., Roher, A.E., 1996. Specific domains of β-amyloid from Alzheimer plague elicit neuron killing in human microglia. J. Neurosci. 16, 6021-6037. (Pubitemid 26313978)
18. Goda, Y., Kiuchi, F., Shibuya, M., Sankawa, U., 1992. Inhibitors of prostaglandin biosynthesis from Dalbergia odorifera. Chem. Pharm. Bull. 40, 2452-2457.
19. Gonzalez-Scarano, F., Baltuch, G., 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240. (Pubitemid 29144887)
20. Gueler, F., Park, J.K., Rong, S., Kirsch, T., Lindschau, C., Zheng, W., Elger, M., Fiebeler, A., Fliser, D., Luft, F.C., Haller, H., 2007. Statins attenuate ischemia-reperfusion injury by inducing heme oxygenase-1 in infiltrating macrophages. Am. J. Pathol. 170, 1192-1199. (Pubitemid 47339327)
21. Ha, S.K., Lee, P., Park, J.A., Oh, H.R., Lee, S.Y., Park, J.H., Lee, E.H., Ryu, J.H., Lee, K.R., Kim, S.Y., 2008. Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem. Int. 52, 878-886.
22. Iles, K.E., Dickinson, D.A., Wigley, A.F., Welty, N.E., Blank, V., Forman, H.J., 2005. HNE increases HO-1 through activation of the ERK pathway in pulmonary epithelial cells. Free Radic. Biol. Med. 39, 355-364. (Pubitemid 40910192)
23. Jeong, G.S., An, R.B., Pae, H.O., Chung, H.T., Yoon, K.H., Kang, D.G., Lee, H.S., Kim, Y.C., 2008. Cudratricusxanthone A protectsmouse hippocampal cells against glutamate-induced neurotoxicity via the induction of heme oxygenase-1. Planta Med. 74, 1368-1373.
24. Jeong, G.S., Lee, D.S., Kim, Y.C., 2009. Cudratricusxanthone A from Cudrania tricuspidata suppresses pro-inflammatory mediators through expression of anti-inflammatory heme oxygenase-1 in RAW264.7 macrophages. Int. Immunopharmacol. 9, 241-246.
25. Jin, D.Q., Lim, C.S., Hwang, J.K., Ha, I., Han, J.S., 2005. Anti-oxidant and anti-inflammatory activities of macelignan in murine hippocampal cell line and primary culture of rat microglial cells. Biochem. Biophys. Res. Commun. 331, 1264-1269. (Pubitemid 40692493)
26. Kang, T.H., Tian, Y.H., Kim, Y.C., 2005. Isoliquiritigenin: a competitive tyrosinase inhibitor from the heartwood of Dalbergia odorifera. J. Appl. Pharmacol. 13, 32-34.
27. Kietzmann, T., Samoylenko, A., Immenschuh, S., 2003. Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J. Biol. Chem. 278, 17927-1736.
28. Kreutzberg, G.W., 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318. (Pubitemid 26349059)
29. Lee, D.S., Jeong, G.S., Li, B., Park, H., Kim, Y.C., 2010. Anti-inflammatory effects of sulfuretin from Rhus verniciflua Stokes via the induction of heme oxygenase-1 expression in murine macrophages. Int. Immunopharmacol. 10, 855-858.
30. Li, B., Jeong, G.S., Kang, D.G., Lee, H.S., Kim, Y.C., 2009. Cytoprotective effects of lindenenyl acetate isolated from Lindera strychnifolia on mouse hippocampal HT22 cells. Eur. J. Pharmacol. 614, 58-65.
31. Lim, C.S., Jin, D.Q., Mol, H., Oh, S.J., Lee, J.U., Hwang, J.K., Ha, I., Han, J.S., 2005. Antioxidant and anti-inflammatory activities of xanthorrhizol in hippocampal neurons and primary cultured microglia. J. Neurosci. Res. 82, 831-838. (Pubitemid 41746496)
32. Lipton, S.A., 2007. Pathologically activated therapeutics for neuroprotection. Nat. Rev. Neurosci. 8, 803-808. (Pubitemid 47462118)
33. Liu, Y., Shepherd, E.G., Nelin, L.D., 2007. MAPK phosphatases - regulating the immune response. Nat. Rev. Immunol. 7, 202-212.
34. Maher, P., Davis, J.B., 1996. The role of monoamine metabolism in oxidative glutamate toxicity. J. Neurosci. 16, 6394-6401. (Pubitemid 26337363)
35. Mattson, M.P., 2001. Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Biol. 120-129.
36. McGeer, P.L., Kawamata, T., Walker, D.G., Akiyama, H., Tooyama, I., McGeer, E.G., 1993. Microglia in degenerative neurological disease. Glia 7, 84-92.
37. Meda, L., Cassatella, M.A., Szendrei, G.I., Otvos Jr., L., Baron, P., Villalba, M., Ferrari, D., Rossi, F., 1995. Activation of microglial cells by β-amyloid protein and interferon-γ. Nature 374, 647-650.
38. Min, K.J., Yang, M.S., Kim, S.U., Jou, I., Joe, E.H., 2006. Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J. Neurosci. 26, 1880-1887. (Pubitemid 43237001)
39. Min, Y.D., Choi, C.H., Bark, H., Son, H.Y., Park, H.H., Lee, S., Park, J.W., Park, E.K., Shin, H.I., Kim, S.H., 2007. Quercetin inhibits expression of inflammatory cytokines through attenuation of NF-kappaB and p38 MAPK in HMC-1 human mast cell line. Inflamm. Res. 56, 210-215. (Pubitemid 46985839)
40. Min, K.J., Kim, J.H., Jou, I., Jeo, E.H., 2008. Adenosine induces hemeoxygenase-1 expression in microglia through the activation of phosphatidylinositol 3-kinase and nuclear factor E2-related factor 2. Glia 56, 1028-1037.
41. Minghetti, L., Levi, G., 1995. Induction of prostanoid biosynthesis by bacterial lipopolysaccharide and isoproterenol in rat microglial cultures. J. Neurochem. 65, 2690-2698.
42. Montellano, P.R., 2000. The mechanism of heme oxygenase. Curr. Opin. Chem. Biol. 4, 221-227. (Pubitemid 30189315)
43. Motterlini, R., Foresti, R., Intaglietta, M., Winslow, R.M., 1996. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am. J. Physiol. 270, H107-H114.
44. Nakamura, Y., Si, Q.S., Kataoka, K., 1999. Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci. Res. 35, 95-100. (Pubitemid 29518400)
45. Nguyen, T.H., Mustafa, F.B., Pervaiz, S., Ng, F.S., Lim, L.H., 2008. ERK1/2 activation is required for resveratrol-induced apoptosis in MDA-MB-231 cells. Int. J. Oncol. 33, 81-92.
46. Noh, H.J., Sung, E.G., Kim, J.Y., Lee, T.J., Song, I.H., 2010. Suppression of phorbol-12-myristate-13-acetate-induced tumor cell invasion by apigenin via the inhibition of p38 mitogen-activated protein kinase-dependent matrix metalloproteinase-9 expression. Oncol. Rep. 24, 277-283.
47. Oh, G.S., Pae, H.O., Lee, B.S., Kim, B.N., Kim, J.M., Kim, H.R., Jeon, S.B., Jeon, W.K., Chae, H.J., Chung, H.T., 2006. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic. Biol. Med. 41, 106-119. (Pubitemid 43884782)
48. Otterbein, L.E., Bach, F.H., Alam, J., Soares, M., Tao, Lu.H., Wysk, M., Davis, R.J., Flavell, R.A., Choi, A.M., 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6, 422-428. (Pubitemid 30208159)
49. Park, J.D., Lee, Y.H., Baek, N.I., Kim, S.I., Ahn, B.Z., 1995. Isolation of antitumor agent from the heartwood of Dalbergia odorifera. Kororan J. Pharmacogn. 26, 323-326. (Pubitemid 26120505)
50. Popko, B., Corbin, J.G., Baerwald, K.D., Dupree, J., Garcia, A.M., 1997. The effects of interferon-γ on the central nervous system. Mol. Neurobiol. 14, 19-35. (Pubitemid 127720195)
51. Romero, L.I., Tatro, J.B., Field, J.A., Reichlin, S., 1996. Roles of IL-1 and TNF-α in endotoxin-induced activation of nitric oxide synthase in cultured rat brain cells. Am. J. Physiol. 270, 326-332.
52. Ro{combining double acute accent}ssler, O.G., Bauer, I., Chung, H.Y., Thiel, G., 2004. Glutamate-induced cell death of immortalized murine hippocampal neurons: neuroprotective activity of heme oxygenase-1, heat shock protein 70, and sodium selenite. Neurosci. Lett. 362, 253-257.
53. Ryter, S.W., Otterbein, L.E., Morse, D., Choi, A.M.K., 2002. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234-235, 249-263. (Pubitemid 34777864)
54. Satoh, T., Lipton, S.A., 2007. Redox regulation of neuronal survival mediated by electrophilic compounds. Trends Neurosci. 30, 37-45. (Pubitemid 44960491)
55. Satoh, T., Enokido, Y., Kubo, K., Yamada, M., Hatanaka, H., 1999. Oxygen toxicity induces apoptosis in neuronal cells. Cell. Mol. Neurobiol. 18, 6496-66.
56. Satoh, T., Baba, M., Nakatsuka, D., Ishikawa, Y., Aburatani, H., Furuta, K., Ishikawa, T., Hatanaka, H., Suzuki, M., Watanabe, Y., 2003. Role of heme oxygenase-1 protein in the neuroprotective effets of cyclopentenone prostaglandin derivatives under oxidative stress. Eur. J. Neurosic. 17, 2249-2255. (Pubitemid 36793734)
57. Satoh, T., Okamoto, S., Cui, J., Watanabe, Y., Furuta, K., Suzuki, M., Tohyama, K., Lipton, S.A., 2006. Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc. Natl. Acad. Sci. U.S.A. 103, 768-773. (Pubitemid 43153100)
58. Schroeter, H., Spencer, J.P., Rice-Evans, C., Williams, R.J., 2001. Flavonoids protect neurons from oxidized low-density-lipoprotein-induced apoptosis involving c-Jun Nterminal kinase (JNK), c-Jun and caspase-3. Biochem. J. 358, 547-557. (Pubitemid 32896942)
59. Shukla, S., Gupta, S., 2007. Apigenin-induced cell cycle arrest is mediated by modulation of MAPK, PI3K-Akt, and loss of cyclin D1 associated retinoblastoma dephosphorylation in human prostate cancer cells. Cell Cycle 6, 1102-1114. (Pubitemid 46708584)
60. Stanciu, M., Wang, Y., Kentor, R., Burke, N., Watkins, S., Kress, G., Reynolds, I., Klann, E., Angiolieri, M.R., Johnson, J.W., DeFranco, D.B., 2000. Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem. 275, 12200-12206. (Pubitemid 30237798)
61. Suh, G.Y., Jin, Y., Yi, A.K., Wang, X.M., Choi, A.M., 2006. CCAAT/enhancer-binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2. Am. J. Respir. Cell Mol. Biol. 35, 220-226. (Pubitemid 44175322)
62. Suh, H.W., Kang, S., Kwon, K.S., 2007. Curcumin attenuates glutamate-induced HT22 cell death by suppressing MAP kinases signaling. Mol. Cell. Biochem. 298, 187-194. (Pubitemid 46605296)
63. Syapin, P.J., 2008. Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders. Br. J. Pharmacol. 155, 623-640.
64. Vane, J.R., Mitchell, J.A., Appleton, I., Tomlinson, A., Bishop-Bailey, D., Croxtall, J., Willoughby, D.A., 1994. Inducible isoforms of cyclooxygenase and nitric-oxide synthase in inflammation. Proc. Natl. Acad. Sci. U.S.A. 91, 2046-2050. (Pubitemid 24092039)
65. Vila,M., Jackson-Lewis, V.,Guegan,C.,Wu,D.C., Teismann, P., Choi,D.K., Tieu, K., Przedborski, S., 2001. The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 14, 483-489. (Pubitemid 32703541)
66. Wang, M.J., Lin, W.W., Chen, H.L., Chang, Y.H., Ou, H.C., Kuo, J.S., Hong, J.S., Jeng, K.C., 2002. Silymarin protects dopaminergic neurons against lipopolysaccharide-induced neurotoxicity by inhibiting microglia activation. Eur. J. Neurosci. 16, 2103-2112.
67. Wiesel, P., Foster, L.C., Pellacani, A., Layne, M.D., Hsieh, S.M., Huggins, G.S., Strauss, P., Yet, S.F., Perrella, M.A., 2000. Thioredoxin facilitates the induction of heme oxygenase-1 in response to inflammatory mediators. J. Biol. Chem. 275, 24840-24846. (Pubitemid 30626588)
68. Yachie, A., Toma, T.,Mizuno, K., Okamoto, H., Shimura, S., Ohta, K., Kasahara, Y., Koizumi, S., 2003. Heme oxygenase-1 production by peripheral blood monocytes during acute inflammatory illnesses of children. Exp. Biol. Med. 228, 550-556. (Pubitemid 37203676)
69. Yahara, S., Ogata, T., Saijo, R., Konishi, R., Yamahara, J., Miyahara, K., Nohara, T., 1989. Isoflavan and related compounds from Dalbergia odorifera. Chem. Pharm. Bull. 37, 979-987.
70. Yu, X., Wang, W., Yang, M., 2007. Antioxidant activities of compounds isolated from Dalbergia odorifera T. Chen and their inhibition effects on the decrease of glutathione level of rat lens induced by UV irradiation. Food Chem. 104, 715-720. (Pubitemid 46661075)
71. Zampetaki, A., Minamino, T., Mitsialis, S.A., Kourembanas, S., 2003. Effect of heme oxygenase-1 overexpression in two models of lung inflammation. Exp. Biol. Med. 228, 442-446. (Pubitemid 37203657)
72. Zhang, T., Yang, D., Fan, Y., Xie, P., Li, H., 2009. Epigallocatechin-3- gallate enhances ischemia/reperfusion-induced apoptosis in human umbilical vein endothelial cells via AKT and MAPK pathways. Apoptosis 14, 1245-1254.