Neuroprotective and anti-inflammatory effects of mollugin via up-regulation of heme oxygenase-1 in mouse hippocampal and microglial cells

European Journal of Pharmacology

Volumn 654, Issue 3, 2011, Pages 226-234

  Jeong, Gil Saeng ^a   Lee, Dong Sung ^a   Kim, Dong Chun ^b   Jahng, Yurngdong ^b   Son, Jong Keun ^b   Lee, Seung Ho ^b   Kim, Youn Chul ^a  

^a Wonkwang University   (South Korea)

^b Yeungnam University   (South Korea)

Author keywords

Anti inflammation; BV2; Heme oxygenase (HO) 1; HT22; Mollugin; Neuroprotection

Indexed keywords

ANTIINFLAMMATORY AGENT; CYCLOOXYGENASE 2; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; MOLLUGIN; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL PROTECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; MICROGLIA; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; CELL LINE; CELL NUCLEUS; CYTOKINES; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMIC ACID; HEME OXYGENASE-1; HIPPOCAMPUS; LIPOPOLYSACCHARIDES; MAP KINASE SIGNALING SYSTEM; MICE; MICROGLIA; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRANS; REACTIVE OXYGEN SPECIES; UP-REGULATION;

EID: 79951674708     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.12.027     Document Type: Article

References (62)

1. J. Alam, and J.L. Cook How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am. J. Respir. Cell Mol. Biol. 36 2007 166 174 (Pubitemid 46233469)
2. E. Balogun, M. Hoque, P. Gong, E. Killeen, C.J. Green, R. Foresti, J. Alam, and R. Motterlini Curcumin activates the heme oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element Biochem. J. 371 2003 887 895 (Pubitemid 36578887)
3. S. Basu, A. Ghosh, and B. Hazra Evaluation of the antibacterial activity of Ventilago madraspatana Gaertn., Rubia cordifolia Linn. and Lantana camara Linn.: isolation of emodin and physcion as active antibacterial agents Phytother. Res. 19 2005 888 894 (Pubitemid 41665959)
4. N.R. Bhat, P. Zhang, J.C. Lee, and E.L. Hogan Extracellular signalregulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures J. Neurosci. 18 1998 1633 1641 (Pubitemid 28103071)
5. E. Blasi, R. Barluzzi, V. Bocchini, R. Mazzolla, and F. Bistoni Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus J. Neuroimmunol. 27 1990 229 237 (Pubitemid 20146292)
6. V. Bocchini, R. Mazzolla, R. Barluzzi, E. Blasi, P. Sick, and H. Kettenmann An immortalized cell line expresses properties of activated microglial cells J. Neurosci. Res. 31 1992 616 621
7. Y. Cai, M. Sun, J. Xing, and H. Corke Antioxidant phenolic constituents in roots of Rheum officinale and Rubia cordifolia: structure-radical scavenging activity relationships J. Agric. Food Chem. 52 2004 7884 7890 (Pubitemid 40053671)
8. B.M. Choi, H.J. Kim, G.S. Oh, H.O. Pae, H.C. Oh, S.J. Jeong, T.O. Kwon, Y.M. Kim, and H.T. Chung 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 2002 185 189
9. J.T. Coyle, and P. Puttfarcken Oxidative stress, glutamate, and neurodegenerative disorders Science 262 1993 689 695 (Pubitemid 23350687)
10. I.M. Copple, C.E. Goldring, N.R. Kitteringham, and B.K. Park The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity Toxicology 246 2008 24 33
11. E.O. Farombi, and Y.J. Surh Heme oxygenase-1 as a potential therapeutic target for hepatoprotection J. Biochem. Mol. Biol. 39 2006 479 491 (Pubitemid 44714527)
12. G.E. Gibson, and H. Zhang Abnormalities in oxidative processes in non-neuronal tissues from patients with Alzheimer's disease J. Alzheimers Dis. 3 2001 329 338 (Pubitemid 32577637)
13. D. Giulian, L.J. Haverkamp, J.H. Yu, W. Karshin, D. Tom, J. Li, J. Kirkpatrick, L.M. Kuo, and A.E. Roher Specific domains of beta-amyloid from Alzheimer plaque elicit neuron killing in human microglia J. Neurosci. 16 1996 6021 6037 (Pubitemid 26313978)
14. F. Gonzalez-Scarano, and G. Baltuch Microglia as mediators of inflammatory and degenerative diseases Annu. Rev. Neurosci. 22 1999 219 240 (Pubitemid 29144887)
15. V. Haridas, M. Hanausek, G. Nishimura, H. Soehnge, A. Gaikwad, M. Narog, E. Spears, R. Zoltaszek, Z. Walaszek, and J.U. Gutterman Triterpenoid electrophiles (avicins) activate the innate stress response by redox regulation of a gene battery J. Clin. Invest. 113 2004 65 73 (Pubitemid 38541633)
16. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
17. G.S. Jeong, R.B. An, H.O. Pae, H.T. Chung, K.H. Yoon, D.G. Kang, H.S. Lee, and Y.C. Kim Cudratricusxanthone A protects mouse hippocampal cells against glutamate-induced neurotoxicity via the induction of heme oxygenase-1 Planta Med. 74 2008 1368 1373
18. G.S. Jeong, D.S. Lee, and Y.C. Kim Cudratricusxanthone A from Cudrania tricuspidata suppresses pro-inflammatory mediators through expression of anti-inflammatory heme oxygenase-1 in RAW264.7 macrophages Int. Immunopharmacol. 9 2009 241 246
19. G.S. Jeong, D.S. Lee, B. Li, H.J. Lee, E.C. Kim, and Y.C. Kim Effects of sappanchalcone on the cytoprotection and anti-inflammation via heme oxygenase-1 in human pulp and periodontal ligament cells Eur. J. Pharmacol. 644 2010 230 237
20. D.Q. Jin, C.S. Lim, J.K. Hwang, I. Ha, and J.S. Han 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 2005 1264 1269 (Pubitemid 40692493)
21. T. Kietzmann, A. Samoylenko, and S. Immenschuh 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 2003 17927 17936 (Pubitemid 36799399)
22. T. Koppal, T.V. Petrova, and L.J. Van Eldik Cyclopentenone prostaglandin 15-deoxy-delta(12, 14)-prostaglandin J(2) acts as a general inhibitor of inflammatory responses in activated BV-2 microglial cells Brain Res. 867 2000 115 121 (Pubitemid 30317387)
23. G.W. Kreutzberg Microglia: a sensor for pathological events in the CNS Trends Neurosci. 19 1996 312 318 (Pubitemid 26349059)
24. R.K. Kutty, G. Kutty, B. Wiggert, G.J. Chader, R.M. Darrow, and D.T. Organisciak Induction of heme oxygenase 1 in the retina by intense visible light: suppression by the antioxidant dimethylthiaurea Proc. Natl Acad. Sci. USA 92 1995 1177 1181
25. S.R. Lee, and K.H. Suk Heme oxygenase-1 mediates cytoprotective effects of immunostimulation in microglia Biochem. Pharmacol. 74 2007 723 729
26. B. Li, G.S. Jeong, D.G. Kang, H.S. Lee, and Y.C. Kim Cytoprotective effects of lindenenyl acetate isolated from Lindera strychnifolia on mouse hippocampal HT22 cells Eur. J. Pharmacol. 614 2009 58 65
27. W. Li, T.O. Khor, C. Xu, G. Shen, JWS, S. Yu, and A.N. Kong Activation of Nrf2-antioxidant signaling attenuates NF-kappaB-inflammatory response and elicits apoptosis Biochem. Pharmacol. 76 2008 1485 1489
28. C.S. Lim, D.Q. Jin, H. Mol, S.J. Oh, J.U. Lee, and J.K. Hwang Antioxidant and anti-inflammatory activities of xanthorrhizol in hippocampal neurons and primary cultured microglia J. Neurosci. Res. 82 2005 831 838 (Pubitemid 41746496)
29. M.T. Lin, and M.F. Beal Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795 (Pubitemid 44622683)
30. Y. Liu, E.G. Shepherd, and L.D. Nelin MAPK phosphatases - regulating the immune response Nat. Rev. Immunol. 7 2007 202 212
31. P. Maher, and D. Schubert Signaling by reactive oxygen species in the nervous system Cell. Mol. Life Sci. 57 2000 1287 1305 (Pubitemid 30663484)
32. M.D. Maines Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J. 2 1988 2557 2568
33. P. Matz, C. Turner, P.R. Weinstein, S.M. Massa, S.S. Panter, and F.R. Sharp Hemeoxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage Mol. Brain Res. 713 1996 211 222 (Pubitemid 26114842)
34. W.K. McCoubrey Jr., J.F. Ewing, and M.D. Maines Human heme oxygenase-2: characterization and expression of a fulllength cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal Arch. Biochem. Biophys. 295 1992 13 20
35. L. Meda, M.A. Cassatella, G.I. Szendrei, L. Otvos Jr., P. Baron, M. Villalba, D. Ferrari, and F. Rossi Activation of microglial cells by beta-amyloid protein and interferon-gamma Nature 374 1995 647 650
36. K.J. Min, I. Jou, and E. Joe Plasminogen-induced IL-1beta and TNFalpha production in microglia is regulated by reactive oxygen species Biochem. Biophys. Res. Commun. 312 2003 969 974 (Pubitemid 37490910)
37. K.J. Min, H.K. Pyo, M.S. Yang, K.A. Ji, I. Jou, and E.H. Joe Gangliosides activate microglia via protein kinase C, NADPH oxidase Glia 48 2004 197 206 (Pubitemid 39545935)
38. K.J. Min, M.S. Yang, S.U. Kim, I. Jou, and E.H. Joe Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation J. Neurosci. 26 2006 1880 1887 (Pubitemid 43237001)
39. T.H. Murphy, M. Miyamoto, A. Sastre, R.L. Schnaar, and J.T. Coyl Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress Neuron 2 1989 1547 1558
40. G.S. Oh, H.O. Pae, B.S. Lee, B.N. Kim, J.M. Kim, H.R. Kim, S.B. Jeon, W.K. Jeon, H.J. Chae, and H.T. Chung 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. Méd. 41 2006 106 119 (Pubitemid 43884782)
41. L.E. Otterbein, F.H. Bach, J. Alam, M. Soares, H. Tao Lu, M. Wysk, R.J. Davis, R.A. Flavell, and A.M. Choi Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat. Med. 6 2000 422 428 (Pubitemid 30208159)
42. W. Paschen, A. Uto, B. Djuricic, and J. Schmitt Heme oxygenase expression after reversible ischemia of rat brain Neurosci. Lett. 180 1994 5 8 (Pubitemid 24314867)
43. M. Pertusa, S. Garcia-Matas, E. Rodriguez-Farre, C. Sanfeliu, and R. Cristofol Astrocytes aged in vitro show a decreased neuroprotective capacity J. Neurochem. 101 2007 794 805 (Pubitemid 46633314)
44. O.G. Rossler, I. Bauer, H.Y. Chung, and G. Thiel 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 2004 253 257 (Pubitemid 38648953)
45. S.W. Ryter, L.E. Otterbein, D. Morse, and A.M. Choi Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance Mol. Cell. Biochem. 234/235 2002 249 263 (Pubitemid 34777864)
46. S.K. Sadhu, E. Okuyama, H. Fujimoto, and M. Ishibashi Separation of Leucas aspera, a medicinal plant of Bangladesh, guided by prostaglandin inhibitory and antioxidant activities Chem. Pharm. Bull. 51 2003 595 598 (Pubitemid 41656816)
47. T. Satoh, M. Baba, D. Nakatsuka, Y. Ishikawa, H. Aburatani, K. Furuta, T. Ishikawa, H. Hatanaka, M. Suzuki, and Y. Watanabe Role of heme oxygenase-1 protein in the neuroprotective effects of cyclopentenone prostaglandin derivatives under oxidative stress Eur. J. Neurosci. 17 2003 2249 2255 (Pubitemid 36793734)
48. T. Satoh, D. Nakatsuka, Y. Watanabe, I. Nagata, H. Kikuchi, and S. Namura Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons Neurosci. Lett. 288 2000 163 166 (Pubitemid 30392436)
49. H.H. Schmidt, and U. Walter NO at work Cell 78 1994 919 925 (Pubitemid 24292320)
50. S. Shibahara, R.M. Muller, and H. Taguchi Transcriptional control of rat heme oxygenase by heat shock J. Biol. Chem. 262 1987 12889 12892
51. L.S. Simon Role and regulation of cycloxygenase-2 during inflammation Am. J. Med. 106 1999 37 42
52. J.K. Son, S.J. Jung, J.H. Jung, Z. Fang, C.S. Lee, C.S. Seo, D.C. Moon, B.S. Min, M.R. Kim, and M.H. Woo Anticancer constituents from the roots of Rubia cordifolia L Chem. Pharm. Bull. 56 2008 213 216 (Pubitemid 351206651)
53. G.Y. Suh, Y. Jin, A.K. Yi, X.M. Wang, and A.M. Choi CCAAT/enhancer- binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2 Am. J. Respir. Cell Mol. Biol. 35 2006 220 226 (Pubitemid 44175322)
54. H.W. Suh, S. Kang, and K.S. Kwon Curcumin attenuates glutamate-induced HT22 cell death by suppressing MAP kinases signaling Mol. Cell. Biochem. 298 2007 187 194 (Pubitemid 46605296)
55. P.J. Syapin Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders Br. J. Pharmacol. 155 2008 623 640
56. R. Tenhunen, H.S. Marver, and R. Schmid The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin J. Lab. Clin. Med. 75 1970 410 421
57. Y. Tezuka, S. Irikawa, T. Kaneko, A.H. Banskota, T. Nagaoka, Q. Xiong, K. Hase, and S. Kadota Screening of Chinese herbal drug extracts for inhibitory activity on nitric oxide production and identification of an active compound of Zanthoxylum bungeanum J. Ethnopharmacol. 77 2001 209 217 (Pubitemid 32776623)
58. K.K. Tha, Y. Okuma, H. Miyazaki, T. Murayama, T. Uehara, and R. Hatakeyama Changes in expressions of proinflammatory cytokines IL-1β, TNF-α and IL-6 in the brain of senescence accelerated mouse (SAM) P8 Brain Res. 885 2000 25 31
59. The Ministry of Public Health Pharmacopoeia of the People's Republic of China 2001 Chemical Industry Press Beijing
60. A. Verma, D.J. Hirsch, C.E. Glatt, G.V. Ronnett, and S.H. Snyder Carbon monoxide: a putative neural messenger Science 259 1993 381 384 (Pubitemid 23055683)
61. P. Wiesel, L.C. Foster, A. Pellacani, M.D. Layne, S.M. Hsieh, and G.S. Huggins Thioredoxin facilitates the induction of heme oxygenase-1 in response to inflammatory mediators J. Biol. Chem. 275 2000 24840 24846 (Pubitemid 30626588)
62. J. Zielasek, and H.P. Hartung Molecular mechanisms of microglial activation Adv. Neuroimmunol. 6 1996 191 222 (Pubitemid 26279977)