Berberine protects 6-hydroxydopamine-induced human dopaminergic neuronal cell death through the induction of heme oxygenase-1

Molecules and Cells

Volumn 35, Issue 2, 2013, Pages 151-157

  Bae, Jinbum ^a   Lee, Danbi ^a   Kim, Yun Kyu ^a   Gil, Minchan ^a,b   Lee, Joo Yong ^a,b   Lee, Kyung Jin ^a,b  

^a Asan Medical Center   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

Author keywords

berberine; heme oxygenase 1; neuroprotection; NF E2 related factor; phosphatidylinositol 3 kinase

Indexed keywords

BERBERINE; CASPASE 3; HEME OXYGENASE 1; MESSENGER RNA; OXIDOPAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROPHORESIS; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; HUMAN; HUMAN CELL; NERVE CELL NECROSIS; NEUROPROTECTION; NICK END LABELING; PARKINSON DISEASE; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

BERBERINE; CELL DEATH; CELL LINE, TUMOR; CELL NUCLEUS; DOPAMINERGIC NEURONS; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HUMANS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDOPAMINE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84879688010     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-013-2298-5     Document Type: Article

References (31)

1. Alam, J., and Cook, J.L. (2003). Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr. Pharm. Des. 9, 2499-2511.
2. Alam, J., Stewart, D., Touchard, C., Boinapally, S., Choi, A.M., and Cook, J.L. (1999). Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071-26078.
3. Balogun, E., Hoque, M., Gong, P., Killeen, E., Green, C.J., Foresti, R., Alam, J., and Motterlini, R. (2003). Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J. 371, 887-895.
4. Chen, X.L., and Kunsch, C. (2004). Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr. Pharm. Des. 10, 879-891.
5. Chen, K., Gunter, K., and Maines, M.D. (2000). Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 75, 304-313.
6. Chowdhury, A.K., Watkins, T., Parinandi, N.L., Saatian, B., Kleinberg, M.E., Usatyuk, P.V., and Natarajan, V. (2005). Src-mediated tyrosine phosphorylation of p47phox in hyperoxia-induced activation of NADPH oxidase and generation of reactive oxygen species in lung endothelial cells. J. Biol. Chem. 280, 20700-20711.
7. Feng, J., Zhang, P., Chen, X., and He, G. (2011). PI3K and ERK/ Nrf2 pathways are involved in oleanolic acid-induced heme oxygenase-1 expression in rat vascular smooth muscle cells. J. Cell. Biochem. 112, 1524-1531.
8. Gong, P., Stewart, D., Hu, B., Li, N., Cook, J., Nel, A., and Alam, J. (2002). Activation of the mouse heme oxygenase-1 gene by 15-deoxy-Delta(12,14)- prostaglandin J(2) is mediated by the stress response elements and transcription factor Nrf2. Antioxid. Redox Signal. 4, 249-257.
9. Greenamyre, J.T., and Hastings, T.G. (2004). Biomedicine. Parkinson's-divergent causes, convergent mechanisms. Science 304, 1120-1122.
10. Hsu, Y.Y., Chen, C.S., Wu, S.N., Jong, Y.J., and Lo, Y.C. (2012). Berberine activates Nrf2 nuclear translocation and protects against oxidative damage via a phosphatidylinositol 3-kinase/Akt-dependent mechanism in NSC34 motor neuron-like cells. Eur. J. Pharm. Sci. 46, 415-425.
11. Hu, X., Wang, J., and Jiang, H. (2012). Heme oxygenase-1: An important therapeutic target for protecting against myocardial ischemia and reperfusion injury. Int. J. Cardiol. pii: S0167-5273(12)01348-4.
12. Hwang, Y.P., and Jeong, H.G. (2008). The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett. 582, 2655-2662.
13. Hwang, Y.P., and Jeong, H.G. (2010). Ginsenoside Rb1 protects against 6-hydroxydopamine-induced oxidative stress by increasing heme oxygenase-1 expression through an estrogen receptor-related PI3K/Akt/Nrf2-dependent pathway in human dopaminergic cells. Toxicol. Appl. Pharmacol. 242, 18-28.
14. Jazwa, A., and Cuadrado, A. (2010). Targeting heme oxygenase-1 for neuroprotection and neuroinflammation in neurodegenerative diseases. Curr. Drug Targets 11, 1517-1531.
15. Johnson, M.R., Wang, K., Smith, J.B., Heslin, M.J., and Diasio, R.B. (2000). Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 278, 175-184.
16. Kusunoki, C., Yang, L., Yoshizaki, T., Nakagawa, F., Ishikado, A., Kondo, M., Morino, K., Sekine, O., Ugi, S., Nishio, Y., et al. (2012). Omega-3 polyunsaturated fatty acid has an anti-oxidant effect via the Nrf-2/HO-1 pathway in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. pii: S0006-291X(12)02107- 9.
17. Lau, C.W., Yao, X.Q., Chen, Z.Y., Ko, W.H., and Huang, Y. (2001). Cardiovascular actions of berberine. Cardiovasc. Drug Rev. 19, 234-244.
18. Maines, M.D. (2007). Biliverdin reductase: PKC interaction at the cross-talk of MAPK and PI3K signaling pathways. Antioxid. Redox Signal. 9, 2187-2195.
19. Martin, D., Rojo, A.I., Salinas, M., Diaz, R., Gallardo, G., Alam, J., De Galarreta, C.M., and Cuadrado, A. (2004). 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, 8919-8929.
20. Panahian, N., Yoshiura, M., and Maines, M.D. (1999). Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187-1203.
21. Ryter, S.W., Otterbein, L.E., Morse, D., and Choi, A.M. (2002). Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234-235, 249-263.
22. Schober, A. (2004). Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res. 318, 215-224.
23. Shrivastava, P., Vaibhav, K., Tabassum, R., Khan, A., Ishrat, T., Khan, M.M., Ahmad, A., Islam, F., Safhi, M.M., and Islam, F. (2012). Anti-apoptotic and Anti-inflammatory effect of Piperine on 6-OHDA induced Parkinson's Rat model. J. Nutr. Biochem. [Epub ahead of print].
24. Srisook, K., Kim, C., and Cha, Y.N. (2005). Molecular mechanisms involved in enhancing HO-1 expression: derepression by heme and activation by Nrf2, the "one-two" punch. Antioxid. Redox Signal. 7, 1674-1687.
25. Sun, G.B., Sun, X., Wang, M., Ye, J.X., Si, J.Y., Xu, H.B., Meng, X.B., Qin, M., Sun, J., Wang, H.W., et al. (2012). Oxidative stress suppression by luteolin-induced heme oxygenase-1 expression. Toxicol. Appl. Pharmacol. 265, 229-240.
26. Surh, Y.J., Kundu, J.K., Li, M.H., Na, H.K., and Cha, Y.N. (2009). Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress. Arch. Pharm. Res. 32, 1163-1176.
27. Tobon-Velasco, J.C., Carmona-Aparicio, L., Ali, S.F., and Santamaria, A. (2010). Biomarkers of cell damage induced by oxidative stress in Parkinson's disease and related models. Cent. Nerv. Syst. Agents Med. Chem. 10, 278-286.
28. Tong, N., Zhang, J., Chen, Y., Li, Z., Luo, Y., Zuo, H., and Zhao, X. (2012). Berberine sensitizes mutliple human cancer cells to the anticancer effects of doxorubicin in vitro. Oncol. Lett. 3, 1263-1267.
29. Xu, C., Li, C.Y., and Kong, A.N. (2005). Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28, 249-268.
30. Zhang, X., Lu, L., Dixon, C., Wilmer, W., Song, H., Chen, X., and Rovin, B.H. (2004). Stress protein activation by the cyclopentenone prostaglandin 15-deoxy-delta12,14-prostaglandin J2 in human mesangial cells. Kidney Int. 65, 798-810.
31. Zhou, X.Q., Zeng, X.N., Kong, H., and Sun, X.L. (2008). Neuroprotective effects of berberine on stroke models in vitro and in vivo. Neurosci. Lett. 447, 31-36.