Juglone, a naphthoquinone from walnut, exerts cytotoxic and genotoxic effects against cultured melanoma tumor cells

Cell Biology International

Volumn 33, Issue 10, 2009, Pages 1039-1049

  Kiran Aithal, B ^a   Sunil Kumar, M R ^a   Nageshwar Rao, B ^a   Udupa, Nayanabhirama ^b   Satish Rao, B S ^a  

^a MANIPAL UNIVERSITY   (India)

^b MANIPAL COLLEGE OF PHARMACEUTICAL SCIENCES   (India)

Author keywords

Apoptosis; Genotoxicity; Juglone; Melanoma; Necrosis; Reactive oxygen species

Indexed keywords

ACETOACETIC ACID; CYTOKINE; DICHLOROFLUORESCEIN; DNA; FLUORESCEIN ISOTHIOCYANATE; GLUTATHIONE; JUGLONE; LACTATE DEHYDROGENASE; LIPOCORTIN 5; NAPHTHOQUINONE; REACTIVE OXYGEN METABOLITE;

AGAR GEL ELECTROPHORESIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DAMAGE; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CLONOGENIC ASSAY; CONTROLLED STUDY; CYTOGENETICS; CYTOTOXICITY; DNA CONTENT; FLOW CYTOMETRY; GENOTOXICITY; IN VITRO STUDY; MELANOMA CELL; MICROSCOPY; NONHUMAN; OXIDATIVE STRESS; WALNUT;

ANIMALS; ANNEXIN A5; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DNA FRAGMENTATION; GLUTATHIONE; JUGLANS; L-LACTATE DEHYDROGENASE; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; NAPHTHOQUINONES; REACTIVE OXYGEN SPECIES;

JUGLANS;

EID: 69549105800     PISSN: 10656995     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cellbi.2009.06.018     Document Type: Article

References (50)

1. Botanical Dermatology Database. Juglandaceae (1999). www.uwcm.ac.uk/uwcm/dm/BoDD/BotDermFolder/BotDermJ/JUGL.html
2. Babula P., Adam V., Havel L., and Kizek R. Naphthoquinones and their pharmacological properties. Ceska Slov Farm 56 3 (2007) 114-120
3. Bachur N.R., Gordon S.L., Gee M.V., and Kon H. NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proc Natl Acad Sci USA 76 2 (1979) 954-957
4. Bai J., and Cederbaum A.I. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents by accelerating the degradation of p53. J Biol Chem 278 7 (2003) 4660-4667
5. Bhargava U.C., and Westfall B.A. Antitumor activity of Juglans niga (black walnut) extractives. J Pharm Sci 57 10 (1968) 1674-1677
6. Blumenthal M. Walnut hull, the complete German commission E monographs (1998), TX American Botanical Council, Austin
7. Cenas N., Prast S., Nivinskas H., Sarlauskas J., and Arner E.S. Interactions of nitroaromatic compounds with the mammalian selenoprotein thioredoxin reductase and the relation to induction of apoptosis in human cancer cells. J Biol Chem 281 9 (2006) 5593-5603
8. Chang D., Chen F., Zhang F., McKay B.C., and Ljungman M. Dose-dependent effects of DNA-damaging agents on p53-mediated cell cycle arrest. Cell Growth Differ 10 3 (1999) 155-162
9. Conklin K.A. Chemotherapy-associated oxidative stress: impact on chemotherapeutic effectiveness. Integr Cancer Ther 3 4 (2004) 294-300
10. Devi P.U., Rao B.S., and Solomon F.E. Effect of plumbagin on the radiation induced cytogenetic and cell cycle changes in mouse Ehrlich ascites carcinoma in vivo. Indian J Exp Biol 36 9 (1998) 891-895
11. Duke J.A., and Ayensu E.S. Medicinal plants of China (1985), Reference Publications Inc.
12. Fenech M. Cytokinesis-block micronucleus cytome assay. Nat Protoc 2 5 (2007) 1084-1104
13. Fenech M., Chang W.P., Kirsch-Volders M., Holland N., Bonassi S., and Zeiger E. HUMN project: detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat Res 534 1-2 (2003) 65-75
14. Fenech M., and Morley A.A. Measurement of micronuclei in lymphocytes. Mutat Res 147 1-2 (1985) 29-36
15. Geard C.R., and Chen C.Y. Micronuclei and clonogenicity following low- and high-dose-rate gamma irradiation of normal human fibroblasts. Radiat Res 124 1 Suppl. (1990) S56-S61
16. Giulivi C., and Cadenas E. One- and two-electron reduction of 2-methyl-1,4-naphthoquinone bioreductive alkylating agents: kinetic studies, free-radical production, thiol oxidation and DNA-strand-break formation. Biochem J 301 Pt 1 (1994) 21-30
17. Han W., Li L., Qiu S., Lu Q., Pan Q., Gu Y., et al. Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther 6 5 (2007) 1641-1649
18. Helson L., Helson C., Malik S., Ainsworth S., and Mangiardi J. A saturation threshold for taxol cytotoxicity in human glial and neuroblastoma cells. Anticancer Drugs 4 4 (1993) 487-490
19. Higuchi Y. Chromosomal DNA fragmentation in apoptosis and necrosis induced by oxidative stress. Biochem Pharmacol 66 8 (2003) 1527-1535
20. Hwang J.M., Wang C.J., Chou F.P., Tseng T.H., Hsieh Y.S., Lin W.L., et al. Inhibitory effect of berberine on tert-butyl hydroperoxide-induced oxidative damage in rat liver. Arch Toxicol 76 11 (2002) 664-670
21. Inbaraj J.J., and Chignell C.F. Cytotoxic action of juglone and plumbagin: a mechanistic study using HaCaT keratinocytes. Chem Res Toxicol 17 1 (2004) 55-62
22. Jewell S.A., Di Monte D., Richelmi P., Bellomo G., and Orrenius S. Tert-Butylhydroperoxide-induced toxicity in isolated hepatocytes: contribution of thiol oxidation and lipid peroxidation. J Biochem Toxicol 1 3 (1986) 13-22
23. Kim B.H., Yoo J., Park S.H., Jung J.K., Cho H., and Chung Y. Synthesis and evaluation of antitumor activity of novel 1,4-naphthoquinone derivatives (IV). Arch Pharm Res 29 2 (2006) 123-130
24. Korzeniewski C., and Callewaert D.M. An enzyme-release assay for natural cytotoxicity. J Immunol Methods 64 3 (1983) 313-320
25. Kumar M.R., Aithal K., Rao B.N., Udupa N., and Rao B.S. Cytotoxic, genotoxic and oxidative stress induced by 1,4-naphthoquinone in B16F1 melanoma tumor cells. Toxicol In Vitro 23 2 (2009) 242-250
26. Liu C.L., Wang J.M., Chu C.Y., Cheng M.T., and Tseng T.H. In vivo protective effect of protocatechuic acid on tert-butyl hydroperoxide-induced rat hepatotoxicity. Food Chem Toxicol 40 5 (2002) 635-641
27. Mariya Y., Streffer C., Fuhrmann C., and Wojcik A. Correlation of radiation-induced micronucleus frequency with clonogenic survival in cells of one diploid and two tetraploid murine tumor cell lines of the same origin. Radiat Res 147 1 (1997) 29-34
28. Moron M.S., Depierre J.W., and Mannervik B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582 1 (1979) 67-78
29. Mujagic H., Chen S.S., Geist R., Occhipinti S.J., Conger B.M., Smith C.A., et al. Effects of vincristine on cell survival, cell cycle progression, and mitotic accumulation in asynchronously growing Sarcoma 180 cells. Cancer Res 43 8 (1983) 3591-3597
30. Muller I., Jenner A., Bruchelt G., Niethammer D., and Halliwell B. Effect of concentration on the cytotoxic mechanism of doxorubicin-apoptosis and oxidative DNA damage. Biochem Biophys Res Commun 230 2 (1997) 254-257
31. Naresh R.A., Udupa N., and Devi P.U. Niosomal plumbagin with reduced toxicity and improved anticancer activity in BALB/C mice. J Pharm Pharmacol 48 11 (1996) 1128-1132
32. Ollinger K., and Brunmark A. Effect of hydroxy substituent position on 1,4-naphthoquinone toxicity to rat hepatocytes. J Biol Chem 266 32 (1991) 21496-21503
33. Pelicano H., Carney D., and Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 7 2 (2004) 97-110
34. Pisha E., Chai H., Lee I.S., Chagwedera T.E., Farnsworth N.R., Cordell G.A., et al. Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat Med 1 10 (1995) 1046-1051
35. Prasad V.S., Devi P.U., Rao B.S., and Kamath R. Radiosensitizing effect of plumbagin on mouse melanoma cells grown in vitro. Indian J Exp Biol 34 9 (1996) 857-858
36. Puck T.T., and Marcus P.I. A rapid method for viable cell titration and clone production with Hela cells in tissue culture: the use of X-irradiated cells to supply conditioning factors. Proc Natl Acad Sci USA 41 7 (1955) 432-437
37. Rao B.S., Shanbhoge R., Upadhya D., Jagetia G.C., Adiga S.K., Kumar P., et al. Antioxidant, anticlastogenic and radioprotective effect of Coleus aromaticus on Chinese hamster fibroblast cells (V79) exposed to gamma radiation. Mutagenesis 21 4 (2006) 237-242
38. Reinicke K.E., Bey E.A., Bentle M.S., Pink J.J., Ingalls S.T., Hoppel C.L., et al. Development of beta-lapachone prodrugs for therapy against human cancer cells with elevated NAD(P)H:quinone oxidoreductase 1 levels. Clin Cancer Res 11 8 (2005) 3055-3064
39. Renvoize C., Biola A., Pallardy M., and Breard J. Apoptosis: identification of dying cells. Cell Biol Toxicol 14 2 (1998) 111-120
40. Ross D., Thor H., Threadgill M.D., Sandy M.S., Smith M.T., Moldeus P., et al. The role of oxidative processes in the cytotoxicity of substituted 1,4-naphthoquinones in isolated hepatocytes. Arch Biochem Biophys 248 2 (1986) 460-466
41. Rowley D.A., and Halliwell B. DNA damage by superoxide-generating systems in relation to the mechanism of action of the anti-tumour antibiotic adriamycin. Biochim Biophys Acta 761 1 (1983) 86-93
42. Satish Rao B.S., Sreedevi M.V., and Nageshwar Rao B. Cytoprotective and antigenotoxic potential of Mangiferin, a glucosylxanthone against cadmium chloride induced toxicity in HepG2 cells. Food Chem Toxicol 47 3 (2009) 592-600
43. Segura-Aguilar J., Jonsson K., Tidefelt U., and Paul C. The cytotoxic effects of 5-OH-1,4-naphthoquinone and 5,8-diOH-1,4-naphthoquinone on doxorubicin-resistant human leukemia cells (HL-60). Leuk Res 16 6-7 (1992) 631-637
44. Srinivas P., Gopinath G., Banerji A., Dinakar A., and Srinivas G. Plumbagin induces reactive oxygen species, which mediate apoptosis in human cervical cancer cells. Mol Carcinog 40 4 (2004) 201-211
45. Sugie S., Okamoto K., Rahman K.M., Tanaka T., Kawai K., Yamahara J., et al. Inhibitory effects of plumbagin and juglone on azoxymethane-induced intestinal carcinogenesis in rats. Cancer Lett 127 1-2 (1998) 177-183
46. Sun X., Li Y., Li W., Zhang B., Wang A.J., Sun J., et al. Selective induction of necrotic cell death in cancer cells by beta-lapachone through activation of DNA damage response pathway. Cell Cycle 5 17 (2006) 2029-2035
47. Tiwari S.B., Pai R.M., and Udupa N. Temperature sensitive liposomes of plumbagin: characterization and in vivo evaluation in mice bearing melanoma B16F1. J Drug Target 10 8 (2002) 585-591
48. Wroblewski F., and Ladue J.S. Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med 90 1 (1955) 210-213
49. Wu Z., Wu L., Li L., Tashiro S., Onodera S., and Ikejima T. p53-mediated cell cycle arrest and apoptosis induced by shikonin via a caspase-9-dependent mechanism in human malignant melanoma A375-S2 cells. J Pharmacol Sci 94 2 (2004) 166-176
50. Yamashita Y., Kawada S., Fujii N., and Nakano H. Induction of mammalian DNA topoisomerase I and II mediated DNA cleavage by saintopin, a new antitumor agent from fungus. Biochemistry (Mosc) 30 24 (1991) 5838-5845