Photochemical and phototoxic activity of berberine on murine fibroblast NIH-3T3 and Ehrlich ascites carcinoma cells

Journal of Photochemistry and Photobiology B: Biology

Volumn 85, Issue 3, 2006, Pages 163-176

  Jantová, Soňa ^a   Letašiová, Silvia ^a   Brezová, Vlasta ^a   Čipák, L'uboš ^b   Lábaj, Juraj ^b  

^a SLOVAK UNIVERSITY OF TECHNOLOGY   (Slovakia)

^b CANCER RESEARCH INSTITUTE   (Slovakia)

Author keywords

Berberine; Cell death; DNA damage; EPR; NIH 3T3 and EAC cells; Phototoxicity; Spin trap

Indexed keywords

BERBERINE; FREE RADICAL; SINGLET OXYGEN; SUPEROXIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DEATH; CELL PROLIFERATION; CELL STRAIN 3T3; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA STRAND BREAKAGE; DRUG CYTOTOXICITY; DRUG STRUCTURE; DRUG UPTAKE; EHRLICH ASCITES TUMOR CELL; ELECTRON SPIN RESONANCE; FIBROBLAST CULTURE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOCHEMISTRY; PHOTOSTIMULATION; PHOTOTOXICITY; PRIORITY JOURNAL; RADIOSENSITIVITY; SENSITIVITY ANALYSIS; ULTRAVIOLET A RADIATION;

ANIMALS; APOPTOSIS; BERBERINE; CARCINOMA, EHRLICH TUMOR; CELL CYCLE; DNA; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; MICE; NIH 3T3 CELLS; OXIDANTS, PHOTOCHEMICAL; REACTIVE OXYGEN SPECIES; SPIN TRAPPING; SUPEROXIDES; TIME FACTORS; TUMOR CELLS, CULTURED; ULTRAVIOLET RAYS;

MURINAE;

EID: 33750022870     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2006.07.001     Document Type: Article

References (52)

1. Amin A.H., Subbahaiah T.V., and Abbasi K.M. Berberine sulfate: Antimicrobial activity, bioassay, and mode of action. Can. J. Microbiol. 15 (1969) 1067-1076
2. Musumeci R., Speciale A., Costanzo R., Annino A., Ragusa S., Rapisarda A., et al. Berberis aetnensis C. Presl. extracts: antimicrobial properties and interaction with ciprofloxacin. Int. J. Antimicrob. Agents 1 (2003) 48-53
3. Ko W.H., Yao X.Q., Lau C.W., Law W.I., Chen Z.Y., Kwok W., et al. Vasorelaxant and antiproliferative effects of berberine. Eur. J. Pharmacol. 2-3 (2000) 187-196
4. Lee D.U., Kang Y.J., Park M.K., Lee Y.S., Seo H.G., Kim T.S., et al. Effects of 13- alkyl-substituted berberine alkaloids on the expression of COX-II, TNF-α, iNOS, and IL-12 production in LPS-stimulated macrophages. Life Sci. 73 (2003) 1401-1412
5. Huang W.M., Wu Z.D., and Gan Y.Q. Effects of berberine on ischemic ventricular arrhythmia. Chin. J. Cardiol. 17 (1989) 300-301+319
6. Lau C.W., Yao X.Q., Chen Z.Y., Ko W.H., and Juany Y. Cardiovascular actions of berberine. Cardiovasc. Drug. Rev. 3 (2001) 234-244
7. Küpeli E., Koşar M., Yeşilada E., Hüsnü K., and Baser C. A comparative study on the anti-inflammatory, antinociceptive and antipyretic effects of isoquinoline alkaloids from the roots of Turkish Berberis species. Life Sci. 6 (2002) 645-657
8. Kuo C.L., Chi C.W., and Liu T.Y. The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Lett. 2 (2004) 127-137
9. Račková L., Májeková M., Košálová D., and Štefek M. Antiradical and antioxidant activities of alkaloids isolated from Mahonia aquifolium. structural aspects. Bioorg. Med. Chem. 12 (2004) 4709-4715
10. Chen K.T., Hao D.M., Liu Z.X., Chen Y.C., and You Z.S. Effect of berberine alone or in combination with argon ion laser treatment on 9L rat glioma cell line. Chin. Med. J. 107 (1994) 808-812
11. Kuo C.L., Chou C.C., and Yung B.Y.M. Berberine complexes with DNA in the berberine-induced apoptosis in human leukemic HL-60 cells. Cancer Lett. 93 (1995) 193-200
12. Yang I.W., Chou C.C., and Yung B.Y.M. Dose-dependent effects of berberine on cell cycle pause and apoptosis in Balb/c 3T3 cells. Naunyn-Schmiedeberg's Arch. Pharm. 2 (1996) 102-108
13. Miura N., Yamamoto M., Ueki T., Kitani T., Fukuda K., and Komatu Y. Inhibition of thymocyte apoptosis by berberine. Biochem. Pharmacol. 9 (1997) 1315-1322
14. Iizuka N., Miyamoto K., Okita K., Tangoku A., Hayashi H., Yosino S., et al. Inhibitory effect of Coptidis Rhizoma and berberine on the proliferation of human esophageal cancer cell lines. Cancer Lett. 1 (2000) 19-25
15. Orfila L., Rodriguez M., Colman T., Hasegawa M., Merentes E., and Arvelo F. Structural modification of berberine alkaloids in relation to cytotoxic activity in vitro. J. Ethnopharmacol. 3 (2000) 449-456
16. Tang W., Hemm I., and Bertram B. Recent development of antitumor agents from Chinese herbal medicine; part I. Low molecular compounds. Planta. Med. 2 (2003) 97-108
17. Gibbons S. Plants as a source of bacterial resistance modulator and anti-infective agents. Phytochem. Rev. 4 (2005) 63-78
18. Kuo C.L., Chi C.W., and Liu T.Y. Modulation of apoptosis by berberine through inhibition of cyclooxygenase-2 and Mcl-1 expression in oral cancer cells. In Vivo 1 (2005) 247-252
19. Wu H.L., Hsu C.Y., Liu W.H., and Yung B.Y. Berberine-induced apoptosis of human leukemia HL-60 cells is associated with down-regulation of nucleophosmin/B23 and telomerase activity. Int. J. Cancer 81 (1999) 923-929
20. Nishida S., Kikuichi S., Yoshioka S., Tsubaki M., Fujii Y., Matsuda H., et al. Induction of apoptosis in HL-60 cells treated with medicinal herbs. Am. J. Chin. Med. 4 (2003) 551-562
21. Jantová S., Čipák L., Čerňaková M., and Košálová D. Effect of berberine on proliferation, cell cycle and apoptosis in HeLa and L1210 cells. J. Pharm. Pharmacol. 55 (2003) 1143-1149
22. Letašiová S., Jantová S., Čipák L., and Múčková M. Berberine - antiproliferative activity in vitro and induction of apoptosis/necrosis of U937 and B16 cells. Cancer Lett. 239 (2006) 254-262
23. Letašiová S., Jantová S., Miko M., Ovádeková R., and Horváthová M. Effect of berberine on proliferation, biosynthesis of macromolecules, cell cycle and induction of intercalation with DNA, dsDNA damage and apoptosis in Ehrlich ascites carcinoma cells. J. Pharm. Pharmacol. 58 (2006) 263-270
24. Anis K.V., Rajeshkumar N.V., and Kuttan R. Inhibition of chemical carcinogenesis by berberine in rats and mice. J. Pharm. Pharmacol. 5 (2001) 763-768
25. Slaninová I., Táborská E., Bochořáková H., and Slanina J. Interaction of benzo[c]phenanthridine and protoberberine alkaloids with animal and yeast cells. Cell. Biol. Toxicol. 1 (2001) 51-63
26. Kobayashi Y., Yamashita Y., Fujii N., Takaboshi K., Kawakami T., Kawamura M., Mizukami T., and Nakano H. Inhibitors of DNA topoisomerase I and II from Coptis rhizomes. Planta Med. 61 (1995) 414-418
27. Fukuda K., Hibiya Y., Mutoh M., Koshiji M., Akao S., and Fujiwarw H. Inhibition of activator protein 1 activity by berberine in human hepatoma cells. Planta Med. 4 (1999) 381-383
28. Hwang J.M., Kuo H.C., Tseng T.H., Li J.Y., and Chu C.Y. Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells. Arch. Toxicol. 11 (2005) 664-670
29. Inbaraj J.J., Kukielezak B.M., Bilski P., Sandvik S.L., and Chignell C.F. Photochemistry and phototoxicity of alkaloids from Goldenseal (Hydrastis canadensis L.) 1. Berberine. Chem. Res. Toxicol. 11 (2001) 1529-1534
30. Agostinis P., Vantieghem A., Merlevede W., and de Witte P.A.M. Hypericin in cancer treatment: more light on the way. Int. J. Biochem. Cell Biol. 34 (2002) 221-241
31. Sacki K., Kadoi M., Kawazoe Y., Futakuchi M., Tiwawech D., and Shirai T. Modification of the carcinogenic potency of quinoline, a hepatocarcinogen, by fluorine atom substitution: evaluation of carcinogenicity by a medium-term assay. Biol. Pharm. Bull. 20 (1997) 40-43
32. Spikes J. Photosensitizing properties of quinine and synthetic antimalarials. J. Photochem. Photobiol. 42 (1998) 1-11
33. Hudson J.B., and Towers G.H.N. Therapeutic potential of plant photosensitizers. Pharmacol. Therapeutics 3 (1991) 181-222
34. Arnason J.T., Guerin B., Kraml M.M., Mehta B., Redmont R.W., and Scaiano J.C. Phototoxic and photochemical properties of sanguinarine. Photochem. Photobiol. 1 (1992) 35-38
35. Liao J., Li P.P., and Wu C.J. Screening new photosensitizers from Chinese medicinal herbs and searching for herbal photodynamic killing effects on human stomach cancer cells. Zhongguo Zhong Xi Yi Jie He Za Zhi 12 (1997) 726-729
36. Brezová V., Dvoranová D., and Košt'álová D. Oxygen activation by photoexcited protoberberinium alkaloids from Mahonia aquifolium. Phytother. Res. 8 (2004) 640-646
37. Miko M., Krepelka J., and Melka M. 9-Hydroxybenfluron: cytostatic effects and inhibition of macromolecular biosynthesis in Ehrlich ascites and P388 murine leukemia cells. Anti-Cancer Drugs 2 (1991) 289-295
38. Catalogue of Light Sources 2000-2002, Philips, Inc., Available from: .
39. Singh N.P., McCoy M.T., Tice R.R., and Schneider E.L. A simple technique for quantification of low levels of DNA damage in individual cells. Exp. Cell Res. 175 (1988) 184-191
40. Slameňová D., Gábelová A., Ružeková L., Chalupa I., Horváthová E., Farkašová T., Bozsakyová E., and Štětina R. Detection of MNNG-induced DNA lesions in mammalian cells; validation of comet assay against DNA unwinding technique, alkaline elution of DNA and chromosomal aberrations. Mutat. Res. 383 (1997) 243-252
41. Gábelová A., Slameňová D., Ružeková L., Farkašová T., and Horváthová E. Measurement of DNA strand breakage and DNA repair induced with hydrogen peroxide using single cell gel electrophoresis, alkaline DNA unwinding and alkaline elution of DNA. Neoplasma 44 (1997) 380-388
42. Collins A.R., Duthie S.J., and Dobson V.L. Direct enzymatic detection of endogenous oxidative base damage in human lymphocyte DNA. Carcinogenesis 14 (1993) 1733-1735
43. McKelvey-Martin V.J., Green M.H.L., Schmezer P., Pool-Zobel B.L., de Méo M.P., and Collins R.A. The single cell electrophoresis assay (comet assay): a European review. Mutat. Res. 288 (1993) 47-63
44. Parker A.J. The effects of solvation on the properties of anions in dipolar aprotic solvents. Quart. Rev. Chem. Soc. 16 (1962) 163-187
45. Li A.S.W., Cummings K.B., Buettner H.P.G.R., and Chignell C.F. A spin-trapping database implemented on the IBM PC/AT. J. Magn. Reson. 79 (1988) 140. Available from:
46. Sinha R., Islam M.M., Bhadra K., Kumar G.S., Banerjee A., and Maiti M. The binding of DNA intercalating and non-intercalating compounds to A-form and protonated form of poly(rC)Æpoly(rG): Spectroscopic and viscometric study. Bioorg. Med. Chem. 14 (2006) 800-814
47. Brown S.B., Brown J.E., and Vernon D.I. Photosensitising drugs - their potential in oncology. Expert. Opin. Investig. Drugs 12 (1999) 1967-1979
48. Halliwell B., and Gutteridge J.M.C. Free Radicals in Biology and Medicine (1999), Oxford University Press
49. Hirakawa K., Kawanishi S., and Hirano T. The mechanism of guanine specific photooxidation in the presence of berberine and palmatine: activation of photosensitized singlet oxygen generation through DNA-binding interaction. Chem. Res. Toxicol. 18 (2005) 1545-1552
50. Yang H.T., and Wang G.J. Transport and uptake characteristics of a new derivative of berberine (CPU-86017) by human intestinal epithelial cell line: Caco-2. Acta Pharmacol. Sin. 24 (2003) 1185-1191
51. Shitan N., Bazin I., Dan K., Obata K., Kigawa K., Ueda K., Sato F., Forestier C., and Yazaki K. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc. Natl. Acad. Sci. USA 100 (2003) 751-756
52. Choi D.S., Kim S.J., and Jung M.Y. Inhibitory activity of berberine on DNA strand cleavage induced by hydrogen peroxide and cytochrome c. Biosci. Biotechnol. Biochem. 2 (2001) 452-455