Berberine induces heme oxygenase-1 up-regulation through phosphatidylinositol 3-kinase/AKT and NF-E2-related factor-2 signaling pathway in astrocytes

International Immunopharmacology

Volumn 12, Issue 1, 2012, Pages 94-100

  Chen, Jia Hong ^a   Huang, Ssu Ming ^a,b   Tan, Tzu Wei ^c   Lin, Hsiao Yun ^b   Chen, Pei Yi ^c   Yeh, Wei Lan ^d   Chou, Shao Chun ^e   Tsai, Cheng Fang ^f   Wei, I Hua ^c   Lu, Dah Yuu ^c  

^a BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL MUSEUM OF NATURAL SCIENCE   (Taiwan)

^e CARDINAL TIEN HOSPITAL   (Taiwan)

^f ASIA UNIVERSITY   (Taiwan)

Author keywords

Astrocytes; Berberine; Chinese herb; Heme oxygenase 1; Nrf2

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BERBERINE; COPTIS RHIZOME EXTRACT; HEME OXYGENASE 1; LUCIFERASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B INHIBITOR; PROTEIN P85; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; WORTMANNIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN; CELL DAMAGE; CELL NUCLEUS; CHINESE HERB; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; HOMEOSTASIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ASTROCYTES; BERBERINE; CELL LINE; CELLS, CULTURED; HEME OXYGENASE-1; NF-E2-RELATED FACTOR 2; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION;

EID: 84856110886     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2011.10.019     Document Type: Article

References (54)

1. M.D. Maines Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J 2 1988 2557 2568
2. P. Ponka Cell biology of heme Am J Med Sci 318 1999 241 256 (Pubitemid 30349676)
3. S.W. Ryter, and R.M. Tyrrell The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties Free Radic Biol Med 28 2000 289 309 (Pubitemid 30084022)
4. V.S. Chopra, L.E. Chalifour, and H.M. Schipper Differential effects of cysteamine on heat shock protein induction and cytoplasmic granulation in astrocytes and glioma cells Brain Res Mol Brain Res 31 1995 173 184
5. W.D. Le, W.J. Xie, and S.H. Appel Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury J Neurosci Res 56 1999 652 658 (Pubitemid 29246847)
6. J.L. Platt, and K.A. Nath Heme oxygenase: protective gene or Trojan horse Nat Med 4 1998 1364 1365 (Pubitemid 28553454)
7. L.E. Otterbein, and A.M. Choi Heme oxygenase: colors of defense against cellular stress Am J Physiol Lung Cell Mol Physiol 279 2000 L1029 L1037
8. M.D. Maines The heme oxygenase system: a regulator of second messenger gases Annu Rev Pharmacol Toxicol 37 1997 517 554 (Pubitemid 27238886)
9. C.M. Terry, J.A. Clikeman, J.R. Hoidal, and K.S. Callahan Effect of tumor necrosis factor-alpha and interleukin-1 alpha on heme oxygenase-1 expression in human endothelial cells Am J Physiol 274 1998 H883 H891
10. A.M. Choi, and J. Alam Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury Am J Respir Cell Mol Biol 15 1996 9 19 (Pubitemid 126439851)
11. T.S. Lee, and L.Y. Chau Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice Nat Med 8 2002 240 246
12. T. Minamino, H. Christou, C.M. Hsieh, Y. Liu, V. Dhawan, and N.G. Abraham Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia Proc Natl Acad Sci USA 98 2001 8798 8803 (Pubitemid 32678107)
13. I.T. Lee, S.W. Wang, C.W. Lee, C.C. Chang, C.C. Lin, and S.F. Luo Lipoteichoic acid induces HO-1 expression via the TLR2/MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells J Immunol 181 2008 5098 5110
14. S.F. Yet, A. Pellacani, C. Patterson, L. Tan, S.C. Folta, and L. Foster Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock J Biol Chem 272 1997 4295 4301 (Pubitemid 27078501)
15. A. Cuadrado, and A.I. Rojo Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections Curr Pharm Des 14 2008 429 442 (Pubitemid 351516848)
16. D.Y. Lu, Y.Y. Tsao, Y.M. Leung, and K.P. Su Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for omega-3 fatty acids Neuropsychopharmacology 35 2010 2238 2248
17. P.R. Vuddanda, S. Chakraborty, and S. Singh Berberine: a potential phytochemical with multispectrum therapeutic activities Expert Opin Investig Drugs 19 2010 1297 1307
18. Y. Sun, K. Xun, Y. Wang, and X. Chen A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs Anticancer Drugs 20 2009 757 769
19. H. Chu, G. Jin, E. Friedman, and X. Zhen Recent development in studies of tetrahydroprotoberberines: mechanism in antinociception and drug addiction Cell Mol Neurobiol 28 2008 491 499 (Pubitemid 351637559)
20. S.K. Kulkarni, and A. Dhir On the mechanism of antidepressant-like action of berberine chloride Eur J Pharmacol 589 2008 163 172
21. K.Y. Yoo, I.K. Hwang, J.D. Kim, I.J. Kang, J. Park, and J.S. Yi Antiinflammatory effect of the ethanol extract of Berberis koreana in a gerbil model of cerebral ischemia/reperfusion Phytother Res 22 2008 1527 1532 (Pubitemid 352789624)
22. S.K. Kulkarni, and A. Dhir Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders Phytother Res 24 2010 317 324
23. D.Y. Lu, C.H. Tang, Y.H. Chen, and I.H. Wei Berberine suppresses neuroinflammatory responses through AMP-activated protein kinase activation in BV-2 microglia J Cell Biochem 110 2010 697 705
24. J. Alam, and J.L. Cook Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway Curr Pharm Des 9 2003 2499 2511 (Pubitemid 37236369)
25. Y. Kobayashi, M. Murata, H. Minami, S. Yamamoto, Y. Kagaya, and T. Hobo Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors Plant J 44 2005 939 949 (Pubitemid 43906723)
26. U.C. Adler, A.H. Marques, and H.M. Calil Inflammatory aspects of depression Inflamm Allergy Drug Targets 7 2008 19 23 (Pubitemid 351688296)
27. M.R. Vargas, M. Pehar, P. Cassina, L. Martinez-Palma, J.A. Thompson, and J.S. Beckman Fibroblast growth factor-1 induces heme oxygenase-1 via nuclear factor erythroid 2-related factor 2 (Nrf2) in spinal cord astrocytes: consequences for motor neuron survival J Biol Chem 280 2005 25571 25579 (Pubitemid 40962264)
28. J.P. O'Callaghan, D.B. Miller, and J.F. Reinhard Jr. Characterization of the origins of astrocyte response to injury using the dopaminergic neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Brain Res 521 1990 73 80 (Pubitemid 20208736)
29. B. Becher, A. Prat, and J.P. Antel Brain-immune connection: immuno-regulatory properties of CNS-resident cells Glia 29 2000 293 304 (Pubitemid 30121420)
30. G.C. Brown, and A. Bal-Price Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria Mol Neurobiol 27 2003 325 355 (Pubitemid 38156291)
31. D.Y. Lu, W.H. Yu, W.L. Yeh, C.H. Tang, Y.M. Leung, and K.L. Wong Hypoxia-induced matrix metalloproteinase-13 expression in astrocytes enhances permeability of brain endothelial cells J Cell Physiol 220 2009 163 173
32. T.C. Jou, M.J. Jou, J.Y. Chen, and S.Y. Lee Properties of rat brain astrocytes in long-term culture Taiwan Yi Xue Hui Za Zhi 84 1985 865 881
33. D.Y. Lu, Y.M. Leung, C.W. Cheung, Y.R. Chen, and K.L. Wong Glial cell line-derived neurotrophic factor induces cell migration and matrix metalloproteinase-13 expression in glioma cells Biochem Pharmacol 80 2010 1201 1209
34. E.J. Joung, M.H. Li, H.G. Lee, N. Somparn, Y.S. Jung, and H.K. Na Capsaicin induces heme oxygenase-1 expression in HepG2 cells via activation of PI3K-Nrf2 signaling: NAD(P)H:quinone oxidoreductase as a potential target Antioxid Redox Signal 9 2007 2087 2098 (Pubitemid 350059030)
35. D. Martin, A.I. Rojo, M. Salinas, R. Diaz, G. Gallardo, and J. Alam Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol J Biol Chem 279 2004 8919 8929 (Pubitemid 38295953)
36. S. Makabe, Y. Takahashi, H. Watanabe, M. Murakami, T. Ohba, and H. Ito Fluvastatin protects vascular smooth muscle cells against oxidative stress through the Nrf2-dependent antioxidant pathway Atherosclerosis 213 2010 377 384
37. W.H. Hsu, Y.S. Hsieh, H.C. Kuo, C.Y. Teng, H.I. Huang, and C.J. Wang Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL Arch Toxicol 81 2007 719 728
38. S.M. Meeran, S. Katiyar, and S.K. Katiyar Berberine-induced apoptosis in human prostate cancer cells is initiated by reactive oxygen species generation Toxicol Appl Pharmacol 229 2008 33 43
39. Y.H. Chou, F.M. Ho, D.Z. Liu, S.Y. Lin, L.H. Tsai, and C.H. Chen The possible role of heat shock factor-1 in the negative regulation of heme oxygenase-1 Int J Biochem Cell Biol 37 2005 604 615
40. Y. Lavrovsky, M.L. Schwartzman, R.D. Levere, A. Kappas, and N.G. Abraham Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene Proc Natl Acad Sci U S A 91 1994 5987 5991 (Pubitemid 24188267)
41. H.Y. Li, S.Y. Wu, and N. Shi Transcription factor Nrf2 activation by deltamethrin in PC12 cells: involvement of ROS Toxicol Lett 171 2007 87 98 (Pubitemid 46994730)
42. H.Y. Cho, A.E. Jedlicka, S.P. Reddy, T.W. Kensler, M. Yamamoto, and L.Y. Zhang Role of NRF2 in protection against hyperoxic lung injury in mice Am J Respir Cell Mol Biol 26 2002 175 182 (Pubitemid 34107870)
43. K. Igarashi, K. Kataoka, K. Itoh, N. Hayashi, M. Nishizawa, and M. Yamamoto Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins Nature 367 1994 568 572 (Pubitemid 24055517)
44. A.A. Anwar, F.Y. Li, D.S. Leake, T. Ishii, G.E. Mann, and R.C. Siow Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2 Free Radic Biol Med 39 2005 227 236 (Pubitemid 40814548)
45. J.M. Chow, S.C. Shen, S.K. Huan, H.Y. Lin, and Y.C. Chen Quercetin, but not rutin and quercitrin, prevention of H2O2-induced apoptosis via anti-oxidant activity and heme oxygenase 1 gene expression in macrophages Biochem Pharmacol 69 2005 1839 1851 (Pubitemid 40780083)
46. C.C. Wu, M.C. Hsu, C.W. Hsieh, J.B. Lin, P.H. Lai, and B.S. Wung Upregulation of heme oxygenase-1 by Epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways Life Sci 78 2006 2889 2897
47. H.C. Lin, T.H. Cheng, Y.C. Chen, and S.H. Juan Mechanism of heme oxygenase-1 gene induction by quercetin in rat aortic smooth muscle cells Pharmacology 71 2004 107 112
48. J.S. Kim, H.J. Song, S.K. Ko, W.K. Whang, and U.D. Sohn Quercetin-3-O-beta-d-glucuronopyranoside (QGC)-induced HO-1 expression through ERK and PI3K activation in cultured feline esophageal epithelial cells Fitoterapia 81 2010 85 92
49. Y.M. Kim, Y.M. Ha, Y.C. Jin, L.Y. Shi, Y.S. Lee, and H.J. Kim Palmatine from Coptidis rhizoma reduces ischemia-reperfusion-mediated acute myocardial injury in the rat Food Chem Toxicol 47 2009 2097 2102
50. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nat Rev Cancer 3 2003 768 780
51. B.J. Buckley, Z.M. Marshall, and A.R. Whorton Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium Biochem Biophys Res Commun 307 2003 973 979 (Pubitemid 36871668)
52. K.K. Elbirt, A.J. Whitmarsh, R.J. Davis, and H.L. Bonkovsky Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases J Biol Chem 273 1998 8922 8931 (Pubitemid 28176175)
53. Y.P. Hwang, H.G. Kim, E.H. Han, and H.G. Jeong Metallothionein-III protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a PI3K and ERK/Nrf2-dependent manner Toxicol Appl Pharmacol 231 2008 318 327
54. J.M. Lee, J.M. Hanson, W.A. Chu, and J.A. Johnson Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells J Biol Chem 276 2001 20011 20016