Berberine inhibits NADPH oxidase mediated superoxide anion production in macrophages

Canadian Journal of Physiology and Pharmacology

Volumn 88, Issue 3, 2010, Pages 369-378

  Sarna, Lindsei K ^a,b   Wu, Nan ^a,b   Hwang, Sun Young ^a,b   Siow, Yaw L ^b,c   Karmin, O ^a,b  

^a ST BONIFACE GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Berberine; Macrophage; NADPH oxidase; Oxidative stress

Indexed keywords

BERBERINE; GLYCOPROTEIN GP 91; LIPOPOLYSACCHARIDE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LEUKEMIA CELL; MACROPHAGE; MONOCYTE; MYELOID LEUKEMIA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME;

BERBERINE; CELL LINE, TUMOR; CELL SURVIVAL; HUMANS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MONOCYTES; NADPH OXIDASE; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 77950900334     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y09-136     Document Type: Article

References (71)

1. Abo, A., Webb, M.R., Grogan, A., and Segal, A.W. 1994. Activation of NADPH oxidase involves the dissociation of p21rac from its inhibitory GDP/GTP exchange protein (rhoGDI) followed by its translocation to the plasma membrane. Biochem. J. 298(Pt 3): 585-591. PMID: 8141770.
2. Afanas'ev, I.B. 2005. On mechanism of superoxide signaling under physiological and pathophysiological conditions. Med. Hypotheses, 64(1): 127-129. doi:10.1016/j.mehy.2004.05.009. PMID: 15533629.
3. Au-Yeung, K.K.W., Woo, C.W.H., Sung, F.L., Yip, J.C.W., Siow, Y.L., and O, K. 2004. Hyperhomocysteinemia activates nuclear factor-kB in endothelial cells via oxidative stress. Circ. Res. 94(1): 28-36. doi:10.1161/01.RES. 0000108264.67601.2C. PMID: 14630727.
4. Azumi, H., Inoue, N., Takeshita, S., Rikitake, Y., Kawashima, S., Hayashi, Y., et al. 1999. Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation, 100(14): 1494-1498. PMID: 10510050.
5. Azumi, H., Inoue, N., Ohashi, Y., Terashima, M., Mori, T., Fujita, H., et al. 2002. Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arterioscler. Thromb. Vasc. Biol. 22(11): 1838-1844. doi:10.1161/01.ATV. 0000037101. 40667.62. PMID: 12426213.
6. Babior, B.M. 1984. Oxidants from phagocytes: agents of defense and destruction. Blood, 64(5): 959-966. PMID: 6386073.
7. Banerjee, R., Anguita, J., Roos, D., and Fikrig, E. 2000. Cutting edge: infection by the agent of human granulocytic ehrlichiosis prevents the respiratory burst by down-regulating gp91phox. J. Immunol. 164(8): 3946-3949. PMID: 10754283.
8. Bouin, A.P., Grandvaux, N., Vignais, P.V., and Fuchs, A. 1998. p40(phox) is phosphorylated on threonine 154 and serine 315 during activation of the phagocyte NADPH oxidase. Implication of a protein kinase c-type kinase in the phosphorylation process. J. Biol. Chem. 273(46): 30097-30103. doi:10.1074/jbc.273.46. 30097. PMID: 9804763.
9. Cathcart, M.K. 2004. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24(1): 23-28. doi:10.1161/01.ATV.0000097769. 47306.12. PMID: 14525794.
10. Champelovier, P., Laporte, F., Verhoeven, A.J., Hilarius, P., de Klein, A., Revol, C., et al. 1993. Absence of both subunits of cytochrome b558 in the UM384 cell line relative to the inability to generate superoxide anions. Exp. Hematol. 21(7): 885-892. PMID: 8391470.
11. Chen, X., Touyz, R.M., Park, J.B., and Schiffrin, E.L. 2001. Anti-oxidant effects of vitamins C and E are associated with altered activation of vascular NADPH oxidase and superoxide dismu-tase in stroke-prone SHR. Hypertension, 38(3 Pt 2): 606-611. doi:10.1161/hy09t1.094005. PMID: 11566940.
12. Chen, F.L., Yang, Z.H., Liu, Y., Li, L.X., Liang, W.C., Wang, X.C., et al. 2008. Berberine inhibits the expression of TNFalpha, MCP-1, and IL-6 in AcLDL-stimulated macrophages through PPARgamma pathway. Endocrine, 33(3): 331-337. doi:10.1007/s12020-008-9089-9093 PMID: 19034703.
13. Crapo, J.D., McCord, J.M., and Fridovich, I. 1978. Preparation and assay of superoxide dismutases. Methods Enzymol. 53: 382-393. doi:10.1016/S0076- 6879(78)53044-9. PMID: 362127.
14. Cross, A.R., and Segal, A.W. 2004. The NADPH oxidase of professional phagocytes-prototype of the NOX electron transport chain systems. Biochim. Biophys. Acta (BBA)-Bioenerg, 1657(1): 1-22. doi:10.1016/j.bbabio.2004.03.008. PMID: 15238208.
15. Cross, A.R., Rae, J., and Curnutte, J.T. 1995. Cytochrome b-245 of the neutrophil superoxide-generating system contains two noni-dentical hemes. Potentiometric studies of a mutant form of gp91phox. J. Biol. Chem. 270(29): 17075-17077. PMID: 7615499.
16. Dröge, W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82(1): 47-95. PMID: 11773609.
17. 2+-depleted human neutro-phils. Biochem. J. 290(Pt 1): 173-178. PMID: 8439286.
18. Dutta, N.K., Marker, P.H., and Rao, N.R. 1972. Berberine in toxin-induced experimental cholera. Br. J. Pharmacol. 44(1): 153-159. PMID: 5015035.
19. Fang, F.C. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2(10): 820-832. doi:10.1038/nrmicro1004. PMID: 15378046.
20. Finan, P., Shimizu, Y., Gout, I., Hsuan, J., Truong, O., Butcher, C., et al. 1994. An SH3 domain and proline-rich sequence mediate an interaction between two components of the phagocyte NADPH oxidase complex. J. Biol. Chem. 269(19): 13752-13755. PMID: 8188650.
21. Forman, H.J., and Torres, M. 2001. Redox signaling in macro-phages. Mol. Aspects Med. 22(4-5): 189-216. doi:10.1016/S0098-2997(01)00010-13 PMID: 11679166.
22. Genestra, M. 2007. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell. Signal. 19(9): 1807-1819. doi:10. 1016/j.cellsig.2007.04. 009. PMID: 17570640.
23. Griendling, K.K., Sorescu, D., and Ushio-Fukai, M. 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86(5): 494-501. PMID: 10720409.
24. Guo, Y., Wang, Q.Z., Li, F.M., Jiang, X., Zuo, Y.F., and Wang, L. 2008. Biochemical pathways in the antiatherosclerotic effect of berberine. Chin. Med. J. (Engl.), 121(13): 1197-1203. PMID: 18710638.
25. Guzik, T.J., West, N.E., Black, E., McDonald, D., Ratnatunga, C., Pillai, R., and Channon, K.M. 2000. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ. Res. 86(9): E85-E90. PMID: 10807876.
26. Guzik, T.J., Sadowski, J., Guzik, B., Jopek, A., Kapelak, B., Przy-bylowski, P., et al. 2006. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 26(2): 333-339. doi:10.1161/01.ATV.0000196651.64776.51. PMID: 16293794. (Pubitemid 43732196)
27. Hancock, J.T. 1997. Superoxide, hydrogen peroxide and nitric oxide as signalling molecules: their production and role in disease. Br. J. Biomed. Sci. 54(1): 38-46. PMID: 9167306.
28. Hashida, S., Yuzawa, S., Suzuki, N.N., Fujioka, Y., Takikawa, T., Sumimoto, H., et al. 2004. Binding of FAD to cytochrome b558 is facilitated during activation of the phagocyte NADPH oxi-dase, leading to superoxide production. J. Biol. Chem. 279(25): 26378-26386. doi:10.1074/jbc.M309724200. PMID: 15102859.
29. Heyworth, P.G., Bohl, B.P., Bokoch, G.M., and Curnutte, J.T. 1994. Rac translocates independently of the neutrophil NADPH oxidase components p47phox and p67phox. Evidence for its interaction with flavocytochrome b558. J. Biol. Chem. 269(49): 30749-30752. PMID: 7982999.
30. Hsieh, Y.S., Kuo, W.H., Lin, T.W., Chang, H.R., Lin, T.H., Chen, P.N., and Chu, S.C. 2007. Protective effects of berberine against low-density lipoprotein (LDL) oxidation and oxidized LDL-in-duced cytotoxicity on endothelial cells. J. Agric. Food Chem. 55(25): 10437-10445. doi:10.1021/jf071868c. PMID: 18001034.
31. Iles, K.E., and Forman, H.J. 2002. Macrophage signaling and respiratory burst. Immunol. Res. 26(1-3): 95-105. doi:10.1385/IR:26:1-3:095. PMID: 12403349.
32. Inoue, N., Ramasamy, S., Fukai, T., Nerem, R.M., and Harrison, D.G. 1996. Shear stress modulates expression of Cu/Zn superox-ide dismutase in human aortic endothelial cells. Circ. Res. 79(1): 32-37. PMID: 8925565.
33. Isogai, Y., Shiro, Y., Nasuda-Kouyama, A., and Iizuka, T. 1991. Superoxide production by cytochrome b558 purified from neu-trophils in a reconstituted system with an exogenous reductase. J. Biol. Chem. 266(21): 13481-13484. PMID: 1649821.
34. Ito, T., Nakamura, R., Sumimoto, H., Takeshige, K., and Sakaki, Y. 1996. An SH3 domain-mediated interaction between the phagocyte NADPH oxidase factors p40phox and p47phox. FEBS Lett. 385(3): 229-232. doi:10.1016/0014-5793(96)00387- 0. PMID: 8647257.
35. Kanai, F., Liu, H., Field, S.J., Akbary, H., Matsuo, T., Brown, G.E., et al. 2001. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3(7): 675-678. doi:10.1038/35083070. PMID: 11433300.
36. Ko, Y.J., Lee, J.S., Park, B.C., Shin, H.M., and Kim, J.A. 2007. Inhibitory effects of Zoagumhwan water extract and berberine on angiotensin II-induced monocyte chemoattractant protein (MCP)-1 expression and monocyte adhesion to endothelial cells. Vascul. Pharmacol. 47(2-3): 189-196. doi:10.1016/j.vph.2007. 06.004. PMID: 17631057.
37. Kong, W., Wei, J., Abidi, P., Lin, M., Inaba, S., Li, C., et al. 2004. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat. Med. 10(12): 1344-1351. doi:10.1038/nm1135. PMID: 15531889.
38. Koshkin, V., Lotan, O., and Pick, E. 1997. Electron transfer in the superoxide-generating NADPH oxidase complex reconstituted in vitro. Biochim. Biophys. Acta, 1319(2-3): 139-146. doi:10.1016/S0005-2728(96)00154-155 PMID: 9131041.
39. Kwong, C.H., Malech, H.L., Rotrosen, D., and Leto, T.L. 1993. Regulation of the human neutrophil NADPH oxidase by rho-re-lated G-proteins. Biochemistry, 32(21): 5711-5717. doi:10.1021/bi00072a029. PMID: 8504089.
40. Lambeth, J.D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4(3): 181-189. doi:10.1038/nri1312. PMID: 15039755.
41. Lambeth, J.D. 2007. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 43(3): 332-347. doi:10.1016/j.freeradbiomed.2007.03.027. PMID: 17602948.
42. Lambeth, J.D., Kawahara, T., and Diebold, B. 2007. Regulation of Nox and Duox enzymatic activity and expression. Free Radic. Biol. Med. 43(3): 319-331. doi:10.1016/j.freeradbiomed.2007. 03.028. PMID: 17602947.
43. Lee, S., Lim, H.J., Park, H.Y., Lee, K.S., Park, J.H., and Jang, Y. 2006. Berberine inhibits rat vascular smooth muscle cell proliferation and migration in vitro and improves neointima formation after balloon injury in vivo: berberine improves neointima formation in a rat model. Atherosclerosis, 186(1): 29-37. doi:10. 1016/j.atherosclerosis.2005.06.048. PMID: 16098530.
44. Leusen, J.H., de Boer, M., Bolscher, B.G., Hilarius, P.M., Weening, R.S., Ochs, H.D., et al. 1994. A point mutation in gp91-phox of cytochrome b558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox. J. Clin. Invest. 93(5): 2120-2126. doi:10.1172/JCI117207. PMID: 8182143.
45. Madamanchi, N.R., Vendrov, A., and Runge, M.S. 2005. Oxidative stress and vascular disease. Arterioscler. Thromb. Vasc. Biol. 25(1): 29-38. PMID: 15539615.
46. Mallozzi, C., Di Stasi, M.A., and Minetti, M. 2001. Peroxynitrite- dependent activation of src tyrosine kinases lyn and hck in ery-throcytes is under mechanistically different pathways of redox control. Free Radic. Biol. Med. 30(10): 1108-1117. doi:10. 1016/S0891-5849(01)00509-513 PMID: 11369500.
47. Meeran, S.M., Katiyar, S., and Katiyar, S.K. 2008. Berberine-in-duced apoptosis in human prostate cancer cells is initiated by reactive oxygen species generation. Toxicol. Appl. Pharmacol. 229(1): 33-43. doi:10.1016/j.taap.2007. 12.027. PMID: 18275980.
48. Mizrahi, A., Berdichevsky, Y., Ugolev, Y., Molshanski-Mor, S., Nakash, Y., Dahan, I., et al. 2006. Assembly of the phagocyte NADPH oxidase complex: chimeric constructs derived from the cytosolic components as tools for exploring structure-function relationships. J. Leukoc. Biol. 79(5): 881-895. doi:10.1189/jlb. 1005553. PMID: 16641134.
49. Mohazzab, K.M., Kaminski, P.M., and Wolin, M.S. 1994. NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am. J. Physiol. 266(6 Pt 2): H2568-H2572. PMID: 8024019.
50. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65(1-2): 55-63. doi:10.1016/0022-1759(83)90303-4. PMID: 6606682.
51. Quinn, M.T., Ammons, M.C., and Deleo, F.R. 2006. The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin. Sci. (Lond.), 111(1): 1-20. doi:10.1042/CS20060059. PMID: 16764554.
52. 2 formation. FASEB J. 14(13): 1953-1964. doi:10.1096/fj.00-0071com. PMID: 11023979.
53. Ross, R. 1993. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature, 362(6423): 801-809. doi:10.1038/362801a0. PMID: 8479518. (Pubitemid 23132154)
54. Segal, A.W., West, I., Wientjes, F., Nugent, J.H., Chavan, A.J., Haley, B., et al. 1992. Cytochrome b-245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbici-dal oxidase of phagocytes. Biochem. J. 284(Pt 3): 781-788. PMID: 1320378.
55. 2+-sensitive nonselective cation channel involved in epithelial cell necrosis. Am. J. Physiol. Cell Physiol. 287(4): C963-C970. doi:10.1152/ajpcell.00041.2004. PMID: 15163619. (Pubitemid 39238320)
56. Siow, Y.L., Au-Yeung, K.K., Woo, C.W., and O, K. 2006. Homo-cysteine stimulates phosphorylation of NADPH oxidase p47phox and p67phox subunits in monocytes via protein kinase Cbeta activation. Biochem. J. 398(1): 73-82. doi:10.1042/BJ20051810. PMID: 16626305.
57. Sorescu, D., Weiss, D., Lassègue, B., Clempus, R.E., Szöcs, K., Sorescu, G.P., et al. 2002. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation, 105(12): 1429-1435. doi:10.1161/01.CIR.0000012917.74432.66. PMID: 11914250.
58. Stolk, J., Hiltermann, T.J., Dijkman, J.H., and Verhoeven, A.J. 1994. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted cate-chol. Am. J. Respir. Cell Mol. Biol. 11(1): 95-102. PMID: 8018341.
59. Stone, J.R., and Yang, S. 2006. Hydrogen peroxide: a signaling messenger. Antioxid. Redox Signal. 8(3-4): 243-270. doi:10. 1089/ars.2006.8.243. PMID: 16677071.
60. Sumimoto, H., Hata, K., Mizuki, K., Ito, T., Kage, Y., Sakaki, Y., et al. 1996. Assembly and activation of the phagocyte NADPH oxidase. Specific interaction of the N-terminal Src homology 3 domain of p47phox with p22phox is required for activation of the NADPH oxidase. J. Biol. Chem. 271(36): 22152-22158. doi:10.1074/jbc.271.36.22152. PMID: 8703027.
61. Tan, Y., Tang, Q., Hu, B.R., and Xiang, J.Z. 2007. Antioxidant properties of berberine on cultured rabbit corpus cavernosum smooth muscle cells injured by hydrogen peroxide. Acta Pharmacol. Sin. 28(12): 1914-1918. doi:10.1111/j.1745-7254.2007. 00705.x. PMID: 18031604.
62. Thirupurasundari, C.J., Padmini, R., and Devaraj, S.N. 2009. Effect of berberine on the antioxidant status, ultrastructural modifications and protein bound carbohydrates in azoxymethane-induced colon cancer in rats. Chem. Biol. Interact. 177(3): 190-195. doi:10.1016/j.cbi.2008.09.027. PMID: 18951886.
63. Uhlinger, D.J., Taylor, K.L., and Lambeth, J.D. 1994. p67-phox enhances the binding of p47-phox to the human neutrophil respiratory burst oxidase complex. J. Biol. Chem. 269(35): 22095-22098. PMID: 8071333.
64. Vendrov, A.E., Hakim, Z.S., Madamanchi, N.R., Rojas, M., Mada-manchi, C., and Runge, M.S. 2007. Atherosclerosis is attenuated by limiting superoxide generation in both macrophages and vessel wall cells. Arterioscler. Thromb. Vasc. Biol. 27(12): 2714-2721. doi:10.1161/ATVBAHA.107.152629. PMID: 17823367.
65. Wang, G., Siow, Y.L., and O, K. 2001. Homocysteine induces monocyte chemoattractant protein-1 expression by activating NF-kappaB in THP-1 macrophages. Am. J. Physiol. Heart Circ. Physiol. 280(6): H2840-H2847. PMID: 11356643.
66. Wang, Y., Zeigler, M.M., Lam, G.K., Hunter, M.G., Eubank, T.D., Khramtsov, V.V., et al. 2007. The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macrophage survival. Am. J. Respir. Cell Mol. Biol. 36(1): 68-77. doi:10.1165/rcmb.2006-0165OC. PMID: 16931806.
67. Warnholtz, A., Nickenig, G., Schulz, E., Macharzina, R., Bräsen, J.H., Skatchkov, M., et al. 1999. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system. Circulation, 99(15): 2027-2033. PMID: 10209008.
68. Woo, C.W.H., Cheung, F., Chan, V.W.H., Siow, Y.L., and Karmin, O. 2003. Homocysteine stimulates inducible nitric oxide synthase expression in macrophages: antagonizing effect of ginkgolides and bilobalide. Mol. Cell. Biochem. 243(1-2): 37-47. doi:10.1023/A:1021601512058. PMID: 12619887.
69. Wu, N., Siow, Y.L., and O, K. 2009. Induction of hepatic cycloox-ygenase-2 by hyperhomocysteinemia via nuclear factor-kappaB activation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297(4): R1086-R1094. PMID: 19657099.
70. Zhang, Y., Li, X., Zou, D., Liu, W., Yang, J., Zhu, N., et al. 2008. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J. Clin. Endocrinol. Metab. 93(7): 2559-2565. doi:10.1210/jc.2007- 2404. PMID: 18397984.
71. Zhou, J., Zhou, S., Tang, J., Zhang, K., Guang, L., Huang, Y., et al. 2009. Protective effect of berberine on beta cells in streptozoto-cin-and high-carbohydrate/high-fat diet-induced diabetic rats. Eur. J. Pharmacol. 606(1-3): 262-268. doi:10.1016/j.ejphar. 2008.12.056. PMID: 19374872.