Novel o-naphthoquinones induce apoptosis of EL-4 T lymphoma cells through the increase of reactive oxygen species

Toxicology in Vitro

Volumn 27, Issue 7, 2013, Pages 2094-2104

  Di Rosso, María Emilia ^a   Barreiro Arcos, María Laura ^b   Elingold, Igal ^a   Sterle, Helena ^b   Baptista Ferreira, Sabrina ^c   Ferreira, Vitor Francisco ^c   Galleano, Mónica ^d   Cremaschi, Graciela ^b   Dubin, Marta ^a  

^a Centre de Estudios Farmacologicos y Botanicos   (Argentina)

^b PONTIFICIA UNIVERSIDAD CATÓLICA ARGENTINA   (Argentina)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Apoptosis; O naphthoquinones; Oxidative stress

Indexed keywords

1,4 NAPHTHOQUINONE DERIVATIVE; 2 METHYL 2 PHENYL 3,4 DIHYDRO 2H BENZO[H]CHROMENE 5,6 DIONE; 2 PARA TOLYL 3,4 DIHYDRO 2H BENZO[H]CHROMENE 5,6 DIONE; 2 PHENYL 3,4 DIHYDRO 2H BENZO[H]CHROMENE 5,6 DIONE; ACETYLCYSTEINE; CASPASE 3; CASPASE 9; FLUORESCEIN ISOTHIOCYANATE; GLUTATHIONE; LIPOCORTIN 5; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL STRAIN L 4; CELL VIABILITY; CHROMATIN CONDENSATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; FLOW CYTOMETRY; IMMUNOBLOTTING; LYMPHOMA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PROTEIN DEGRADATION; T CELL LYMPHOMA;

MURINAE;

2,7-DICHLORODIHYDROFLUORESCEIN DIACETATE; 2-METHYL-2-PHENYL-3,4-DIHYDRO-2H-BENZO[H]CHROMENE-5,6-DIONE; 2-NITRO-5-THIOBENZOIC ACID; 2-P-TOLYL-3,4-DIHYDRO-2H-BENZO[H]CHROMENE-5,6-DIONE; 2-PHENYL-3,4-DIHYDRO-2H-BENZO[H]CHROMENE-5,6-DIONE; 5,5′-DITHIOBIS-2-NITROBENZOIC ACID; ACRIDINE ORANGE; AO; APOPTOSIS; DMFA; DTNB; EB; ELECTRON PARAMAGNETIC RESONANCE; EPR; ETHIDIUM BROMIDE; H2DCF-DA; MITOCHONDRIAL MEMBRANE POTENTIAL; MMP; N,N-DIMETHYL-FORMAMIDE; N-ACETYL-L-CYSTEINE; NAC; NQ1; NQ3; NQ7; O-NAPHTHOQUINONES; OXIDATIVE STRESS; PARP; PERMEABILITY TRANSITION PORE; PI; POLY (ADP-RIBOSE) POLYMERASE; PROPIDIUM IODIDE; PTP; REACTIVE OXYGEN SPECIES; RHO-123; RHODAMINE-123; ROS; TCA; TNB; TRICHLOROACETIC ACID;

ACETYLCYSTEINE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOPYRANS; BENZOQUINONES; CELL LINE, TUMOR; CELL NUCLEUS SHAPE; CELL PROLIFERATION; CELL SURVIVAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; FREE RADICAL SCAVENGERS; GLUTATHIONE; KINETICS; LYMPHOMA, T-CELL; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NAPHTHOQUINONES; REACTIVE OXYGEN SPECIES; TRYPANOCIDAL AGENTS; UP-REGULATION;

EID: 84884180331     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2013.08.002     Document Type: Article

References (71)

1. Araujo A.J., de Souza A.A., da Silva Junior E.N., Marinho-Filho J.D., de Moura M.A., Rocha D.D., Vasconcellos M.C., Costa C.O., Pessoa C., de Moraes M.O., Ferreira V.F., de Abreu F.C., Pinto A.V., Montenegro R.C., Costa-Lotufo L.V., Goulart M.O. Growth inhibitory effects of 3'-nitro-3-phenylamino nor-beta-lapachone against HL-60: a redox-dependent mechanism. Toxicol. In Vitro 2012, 26:585-594.
2. Armstrong J.S., Steinauer K.K., Hornung B., Irish J.M., Lecane P., Birrell G.W., Peehl D.M., Knox S.J. Role of glutathione depletion and reactive oxygen species generation in apoptotic signaling in a human B lymphoma cell line. Cell Death Differ. 2002, 9:252-263.
3. Asche C. Antitumour quinones. Mini Rev. Med. Chem. 2005, 5:449-467.
4. Barreiro Arcos M.L., Gorelik G., Klecha A., Goren N., Cerquetti C., Cremaschi G.A. Inducible nitric oxide synthase-mediated proliferation of a T lymphoma cell line. Nitric oxide 2003, 8:111-118.
5. Bolton J.L., Trush M.A., Penning T.M., Dryhurst G., Monks T.J. Role of quinones in toxicology. Chem. Res. Toxicol. 2000, 13:135-160.
6. Boveris A., Docampo R., Turrens J.F., Stoppani A.O. Effect of beta-lapachone on superoxide anion and hydrogen peroxide production in Trypanosoma cruzi. Biochem. J. 1978, 175:431-439.
7. Boveris A., Stoppani A.O., Docampo R., Cruz F.S. Superoxide anion production and trypanocidal action of naphthoquinones on Trypanosoma cruzi. Comp. Biochem. Physiol. C 1978, 61:327-329.
8. Brunmark A., Cadenas E. Redox and addition chemistry of quinoid compounds and its biological implications. Free Radic. Biol. Med. 1989, 7:435-477.
9. Butler J., Hoey B.M., Lea J.S. The reduction of anti-tumour diaziridinyl benzoquinones. Biochim. Biophys. Acta 1987, 925:144-149.
10. Cadenas E. Antioxidant and prooxidant functions of DT-diaphorase in quinone metabolism. Biochem. Pharmacol. 1995, 49:127-140.
11. Choi B.T., Cheong J., Choi Y.H. Beta-Lapachone-induced apoptosis is associated with activation of caspase-3 and inactivation of NF-kappaB in human colon cancer HCT-116 cells. Anticancer Drugs 2003, 14:845-850.
12. Coligan J.E., Kruisbeek A.M., Margulies D.H., Shevach E.M., Strober W. Current protocols in immunology. Related Isolation Procedures and Functional Assays 1995, John Wiley & Sons, Inc., 3.17.11. R. Coico (Ed.).
13. Coppola S., Ghibelli L. GSH extrusion and the mitochondrial pathway of apoptotic signalling. Biochem. Soc. Trans. 2000, 28:56-61.
14. Costantino L., Barlocco D. Privileged structures as leads in medicinal chemistry. Curr. Med. Chem. 2006, 13:65-85.
15. da Silva E.N., Cavalcanti B.C., Guimaraes T.T., Pinto Mdo C., Cabral I.O., Pessoa C., Costa-Lotufo L.V., de Moraes M.O., de Andrade C.K., Dos Santos M.R., de Simone C.A., Goulart M.O., Pinto A.V. Synthesis and evaluation of quinonoid compounds against tumor cell lines. Eur. J. Med. Chem. 2011, 46:399-410.
16. D'Anneo A., Augello G., Santulli A., Giuliano M., di Fiore R., Messina C., Tesoriere G., Vento R. Paclitaxel and beta-lapachone synergistically induce apoptosis in human retinoblastoma Y79 cells by downregulating the levels of phospho-Akt. J. Cell Physiol. 2010, 222:433-443.
17. de Witte N.V., Stoppani A.O., Dubin M. 2-Phenyl-beta-lapachone can affect mitochondrial function by redox cycling mediated oxidation. Arch Biochem. Biophys. 2004, 432:129-135.
18. Dolan M.E., Frydman B., Thompson C.B., Diamond A.M., Garbiras B.J., Safa A.R., Beck W.T., Marton L.J. Effects of 1,2-naphthoquinones on human tumor cell growth and lack of cross-resistance with other anticancer agents. Anticancer Drugs 1998, 9:437-448.
19. Donadelli M., Dalla Pozza E., Costanzo C., Scupoli M.T., Piacentini P., Scarpa A., Palmieri M. Increased stability of P21(WAF1/CIP1) mRNA is required for ROS/ERK-dependent pancreatic adenocarcinoma cell growth inhibition by pyrrolidine dithiocarbamate. Biochim. Biophys. Acta 2006, 1763:917-926.
20. dos Santos E.V., Carneiro J.W., Ferreira V.F. Quantitative structure-activity relationship in aziridinyl-1,4-naphthoquinone antimalarials: study of theoretical correlations by the PM3 method. Bioorg. Med. Chem. 2004, 12:87-93.
21. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
22. Edmonson J.H., Ryan L.M., Blum R.H., Brooks J.S., Shiraki M., Frytak S., Parkinson D.R. Randomized comparison of doxorubicin alone versus ifosfamide plus doxorubicin or mitomycin, doxorubicin, and cisplatin against advanced soft tissue sarcomas. J. Clin. Oncol. 1993, 11:1269-1275.
23. Elingold I., Taboas M.I., Casanova M.B., Galleano M., Silva R.S., Menna-Barreto R.F., Ventura Pinto A., de Castro S.L., Costa L.E., Dubin M. Mechanism of action of novel naphthofuranquinones on rat liver microsomal peroxidation. Chem. Biol. Interact. 2009, 182:213-219.
24. Fernandez Villamil S., Stoppani A.O., Dubin M. Redox cycling of beta-lapachone and structural analogues in microsomal and cytosol liver preparations. Methods Enzymol. 2004, 378:67-87.
25. Fernandez Villamil S.H., Carrizo P.H., Di Rosso M.E., Molina Portela M.P., Dubin M. The metabolism of 9-chloro-beta-lapachone and its effects in isolated hepatocytes. The involvement of NAD(P)H:quinone oxidoreductase 1 (NQO1). Chem. Biol. Interact. 2012, 200:84-91.
26. Ferreira S.B., Salomao K., de Carvalho da Silva F., Pinto A.V., Kaiser C.R., Pinto A.C., Ferreira V.F., de Castro S.L. Synthesis and anti-Trypanosoma cruzi activity of beta-lapachone analogues. Eur. J. Med. Chem. 2011, 46:3071-3077.
27. Frydman B., Marton L.J., Sun J.S., Neder K., Witiak D.T., Liu A.A., Wang H.M., Mao Y., Wu H.Y., Sanders M.M., Liu L.F. Induction of DNA topoisomerase II-mediated DNA cleavage by beta-lapachone and related naphthoquinones. Cancer Res. 1997, 57:620-627.
28. Gago-Martinez A., Nogueiras M.J., Rellan S., Prado J., Alpendurada M.F., Vetter W. Optimization of solid-phase microextraction for the gas chromatography/mass spectrometry analysis of persistent organic pollutants. J. AOAC Int. 2004, 87:1021-1027.
29. Goijman S.G., Stoppani A.O. Effects of beta-lapachone, a peroxide-generating quinone, on macromolecule synthesis and degradation in Trypanosoma cruzi. Arch Biochem. Biophys. 1985, 240:273-280.
30. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106:207-212.
31. Gross C.L., Innace J.K., Hovatter R.C., Meier H.L., Smith W.J. Biochemical manipulation of intracellular glutathione levels influences cytotoxicity to isolated human lymphocytes by sulfur mustard. Cell Biol. Toxicol. 1993, 9:259-267.
32. Halliwell B., Aruoma O.I. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett. 1991, 281:9-19.
33. Hampton M.B., Fadeel B., Orrenius S. Redox regulation of the caspases during apoptosis. Ann. N Y Acad. Sci. 1998, 854:328-335.
34. Hillard E.A., de Abreu F.C., Ferreira D.C., Jaouen G., Goulart M.O., Amatore C. Electrochemical parameters and techniques in drug development, with an emphasis on quinones and related compounds. Chem. Commun. (Camb) 2008, 2612-2628.
35. Inbaraj J.J., Chignell C.F. Cytotoxic action of juglone and plumbagin: a mechanistic study using HaCaT keratinocytes. Chem. Res. Toxicol. 2004, 17:55-62.
36. Kalyanaraman B., Morehouse K.M., Mason R.P. An electron paramagnetic resonance study of the interactions between the adriamycin semiquinone, hydrogen peroxide, iron-chelators, and radical scavengers. Arch Biochem. Biophys. 1991, 286:164-170.
37. Kongkathip N., Kongkathip B., Siripong P., Sangma C., Luangkamin S., Niyomdecha M., Pattanapa S., Piyaviriyagul S., Kongsaeree P. Potent antitumor activity of synthetic 1,2-Naphthoquinones and 1,4-Naphthoquinones. Bioorg. Med. Chem. 2003, 11:3179-3191.
38. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
39. Kumar S., Villinger F., Oakley M., Aguiar J.C., Jones T.R., Hedstrom R.C., Gowda K., Chute J., Stowers A., Kaslow D.C., Thomas E.K., Tine J., Klinman D., Hoffman S.L., Weiss W.W. A DNA vaccine encoding the 42 kDa C-terminus of merozoite surface protein 1 of Plasmodium falciparum induces antibody, interferon-gamma and cytotoxic T cell responses in rhesus monkeys: immuno-stimulatory effects of granulocyte macrophage-colony stimulating factor. Immunol. Lett. 2002, 81:13-24.
40. Kumar S.G., Narayana K., Bairy K.L., D'Souza U.J., Samuel V.P., Gopalakrishna K. Dacarbazine induces genotoxic and cytotoxic germ cell damage with concomitant decrease in testosterone and increase in lactate dehydrogenase concentration in the testis. Mutat. Res. 2006, 607:240-252.
41. Lai C.C., Liu T.J., Ho L.K., Don M.J., Chau Y.P. Beta-Lapachone induced cell death in human hepatoma (HepA2) cells. Histol. Histopathol. 1998, 13:89-97.
42. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992, 5:227-231.
43. Li C.J., Averboukh L., Pardee A.B. Beta-Lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin. J. Biol. Chem. 1993, 268:22463-22468.
44. Li C.J., Wang C., Pardee A.B. Induction of apoptosis by beta-lapachone in human prostate cancer cells. Cancer Res. 1995, 55:3712-3715.
45. Li C.J., Li Y.Z., Pinto A.V., Pardee A.B. Potent inhibition of tumor survival in vivo by beta-lapachone plus taxol: combining drugs imposes different artificial checkpoints. Proc. Natl. Acad. Sci. USA 1999, 96:13369-13374.
46. Li Y.Z., Li C.J., Pinto A.V., Pardee A.B. Release of mitochondrial cytochrome C in both apoptosis and necrosis induced by beta-lapachone in human carcinoma cells. Mol. Med. 1999, 5:232-239.
47. Li Y., Li C.J., Yu D., Pardee A.B. Potent induction of apoptosis by beta-lapachone in human multiple myeloma cell lines and patient cells. Mol. Med. 2000, 6:1008-1015.
48. Lin C.H., Huang C.C., Wang T.W., Wang Y.J., Lin P.H. Disparity in the induction of glutathione depletion, ROS formation, poly(ADP-ribose) polymerase-1 activation, and apoptosis by quinonoid derivatives of naphthalene in human cultured cells. Chem. Biol. Interact. 2007, 165:200-210.
49. Lopes J.N., Cruz F.S., Docampo R., Vasconcellos M.E., Sampaio M.C., Pinto A.V., Gilbert B. In vitro and in vivo evaluation of the toxicity of 1,4-naphthoquinone and 1,2-naphthoquinone derivatives against Trypanosoma cruzi. Ann. Trop. Med. Parasitol. 1978, 72:523-531.
50. Molina Portela M.P., Stoppani A.O. Redox cycling of beta-lapachone and related o-naphthoquinones in the presence of dihydrolipoamide and oxygen. Biochem. Pharmacol. 1996, 51:275-283.
51. Molina Portela M.P., Fernandez Villamil S.H., Perissinotti L.J., Stoppani A.O. Redox cycling of o-naphthoquinones in trypanosomatids. Superoxide and hydrogen peroxide production. Biochem. Pharmacol. 1996, 52:1875-1882.
52. Nogueira C.W., Zeni G., Rocha J.B. Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem. Rev. 2004, 104:6255-6285.
53. Ough M., Lewis A., Bey E.A., Gao J., Ritchie J.M., Bornmann W., Boothman D.A., Oberley L.W., Cullen J.J. Efficacy of beta-lapachone in pancreatic cancer treatment: exploiting the novel, therapeutic target NQO1. Cancer Biol. Ther. 2005, 4:95-102.
54. Pardee A.B., Li Y.Z., Li C.J. Cancer therapy with beta-lapachone. Curr. Cancer Drug. Targets 2002, 2:227-242.
55. Planchon S.M., Wuerzberger S., Frydman B., Witiak D.T., Hutson P., Church D.R., Wilding G., Boothman D.A. Beta-lapachone-mediated apoptosis in human promyelocytic leukemia (HL-60) and human prostate cancer cells: a p53-independent response. Cancer Res. 1995, 55:3706-3711.
56. Planchon S.M., Wuerzberger-Davis S.M., Pink J.J., Robertson K.A., Bornmann W.G., Boothman D.A. Bcl-2 protects against beta-lapachone-mediated caspase 3 activation and apoptosis in human myeloid leukemia (HL-60) cells. Oncol. Rep. 1999, 6:485-492.
57. Pritsos C.A., Vimalachandra B. Mitochondrial dysfunction and ATP depletion in mitomycin C treated mice. Proc. Am. Assoc. Cancer Res. 1995, 36:352-356.
58. Rios-Luci C., Bonifazi E.L., Leon L.G., Montero J.C., Burton G., Pandiella A., Misico R.I., Padron J.M. Beta-Lapachone analogs with enhanced antiproliferative activity. Eur. J. Med. Chem. 2012, 53:264-274.
59. Samali A., Nordgren H., Zhivotovsky B., Peterson E., Orrenius S. A comparative study of apoptosis and necrosis in HepG2 cells: oxidant-induced caspase inactivation leads to necrosis. Biochem. Biophys. Res. Commun. 1999, 255:6-11.
60. Seshadri P., Rajaram A., Rajaram R. Plumbagin and juglone induce caspase-3-dependent apoptosis involving the mitochondria through ROS generation in human peripheral blood lymphocytes. Free Radic. Biol. Med. 2011, 51:2090-2107.
61. Thor H., Smith M.T., Hartzell P., Bellomo G., Jewell S.A., Orrenius S. The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. A study of the implications of oxidative stress in intact cells. J. Biol. Chem. 1982, 257:12419-12425.
62. Tudor G., Gutierrez P., Aguilera-Gutierrez A., Sausville E.A. Cytotoxicity and apoptosis of benzoquinones: redox cycling, cytochrome c release, and BAD protein expression. Biochem. Pharmacol. 2003, 65:1061-1075.
63. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
64. Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 1995, 184:39-51.
65. Walsh G.M., Dewson G., Wardlaw A.J., Levi-Schaffer F., Moqbel R. A comparative study of different methods for the assessment of apoptosis and necrosis in human eosinophils. J. Immunol. Methods 1998, 217:153-163.
66. Weller M., Winter S., Schmidt C., Esser P., Fontana A., Dichgans J., Groscurth P. Topoisomerase-I inhibitors for human malignant glioma: differential modulation of p53, p21, bax and bcl-2 expression and of CD95-mediated apoptosis by camptothecin and beta-lapachone. Int. J. Cancer 1997, 73:707-714.
67. Woo H.J., Park K.Y., Rhu C.H., Lee W.H., Choi B.T., Kim G.Y., Park Y.M., Choi Y.H. Beta-lapachone, a quinone isolated from Tabebuia avellanedae, induces apoptosis in HepG2 hepatoma cell line through induction of Bax and activation of caspase. J. Med. Food. 2006, 9:161-168.
68. Wuerzberger S.M., Pink J.J., Planchon S.M., Byers K.L., Bornmann W.G., Boothman D.A. Induction of apoptosis in MCF-7:WS8 breast cancer cells by beta-lapachone. Cancer Res. 1998, 58:1876-1885.
69. Xu H.L., Yu X.F., Qu S.C., Zhang R., Qu X.R., Chen Y.P., Ma X.Y., Sui D.Y. Anti-proliferative effect of Juglone from Juglans mandshurica Maxim on human leukemia cell HL-60 by inducing apoptosis through the mitochondria-dependent pathway. Eur. J. Pharmacol. 2010, 645:14-22.
70. Xu H.L., Yu X.F., Qu S.C., Qu X.R., Jiang Y.F., Sui da Y. Juglone, from Juglans mandshruica Maxim, inhibits growth and induces apoptosis in human leukemia cell HL-60 through a reactive oxygen species-dependent mechanism. Food Chem. Toxicol. 2012, 50:590-596.
71. Zafarullah M., Li W.Q., Sylvester J., Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cell Mol. Life Sci. 2003, 60:6-20.