ATP depletion alters the mode of cell death induced by benzyl isothiocyanate

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1782, Issue 10, 2008, Pages 566-573

  Miyoshi, Noriyuki ^a   Watanabe, Etsuko ^b   Osawa, Toshihiko ^b   Okuhira, Masashi ^c   Murata, Yoshiyuki ^c   Ohshima, Hiroshi ^a   Nakamura, Yoshimasa ^c  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

2 ,7 dichlorofluorescin diacetate; 2 DG; AKR1C; aldo keto reductase 1C; Apoptosis; ataxia telangiectasia mutated; ATM; ATP; Benzyl isothiocyanate; benzyl ITC; BITC; CHX; cycloheximide; etoposide; ETP; GAPDH; GCLC; glutamate cysteine ligase catalytic subunit; glutathione; glutathione peroxidase; glutathione S transferase; glyceraldehyde 3 phosphate dehydrogenase; GPx; GSH; GST; H2DCF DA; HeLa cell; isothiocyanate; ITC; lactate dehydrogenase; LDH; Necrosis; PEITC; phenethyl ITC; PI; propidium iodide; reactive oxygen species; ROS; thioredoxin; TR

Indexed keywords

ADENOSINE TRIPHOSPHATE; BENZYL ISOTHIOCYANATE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE INHIBITOR; DEOXYGLUCOSE; DNA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; FLOW CYTOMETRY; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; MORPHOLOGY; PRIORITY JOURNAL; RESPIRATORY CHAIN; UTERINE CERVIX CANCER; WILD TYPE;

ADENOSINE TRIPHOSPHATE; AMINO ACID CHLOROMETHYL KETONES; APOPTOSIS; CASPASES; CELL MEMBRANE; CELL NUCLEUS; CELL SHAPE; CELL SURVIVAL; CYCLOHEXIMIDE; DEOXYGLUCOSE; DNA FRAGMENTATION; DNA, MITOCHONDRIAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ETHIDIUM; HELA CELLS; HUMANS; ISOTHIOCYANATES; MITOCHONDRIA; PHOSPHATIDYLSERINES; REACTIVE OXYGEN SPECIES;

ATAXIA TELANGIECTASIA;

EID: 52049112536     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2008.07.002     Document Type: Article

References (51)

1. Hecht S.S. Inhibition of carcinogenesis by isothiocyanates. Drug. Metab. Rev. 32 (2000) 395-411
2. Kelloff G.J., Crowell J.A., Steele V.E., Lubet R.A., Boone C.W., Malone W.A., Hawk E.T., Lieberman R., Lawrence J.A., Kopelovich L., Ali I., Viner J.L., and Sigman C.C. Progress in cancer chemoprevention. Ann. N. Y. Acad. Sci 889 (1999) 1-13
3. Zhao B., Seow A., Lee E.J., Poh W.T., Teh M., Eng P., Wang Y.T., Tan W.C., Yu M.C., and Lee H.P. Dietary isothiocyanates, glutathione S-transferase-M1, -T1 polymorphisms and lung cancer risk among Chinese women in Singapore. Cancer Epidemiol. Biomarkers Prev. 10 (2001) 1063-1067
4. Lin H.J., Probst-Hensch N.M., Louie A.D., Kau I.H., Witte J.S., Ingles S.A., Frankl H.D., Lee E.R., and Haile R.W. Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal adenomas. Cancer Epidemiol. Biomarkers Prev. 7 (1998) 647-652
5. Zhang Y. Cancer-preventive isothiocyanates: measurement of human exposure and mechanism of action. Mutat. Res. 555 (2004) 173-190
6. Miyoshi N., Uchida K., Osawa T., and Nakamura Y. A link between benzyl isothiocyanate-induced cell cycle arrest and apoptosis: involvement of mitogen-activated protein kinases in the Bcl-2 phosphorylation. Cancer Res. 64 (2004) 2134-2142
7. Miyoshi N., Takabayashi S., Osawa T., and Nakamura Y. Benzyl isothiocyanate inhibits excessive superoxide generation in inflammatory leukocytes: implication for prevention against inflammation-related carcinogenesis. Carcinogenesis 25 (2004) 567-575
8. Nakamura Y., and Miyoshi N. Cell death induction by isothiocyanates and their underlying molecular mechanisms. Biofactors 26 (2006) 123-134
9. Nakamura Y., Kawakami M., Yoshihiro A., Miyoshi N., Ohigashi H., Kawai K., Osawa T., and Uchida K. Involvement of the mitochondrial death pathway in chemopreventive benzyl isothiocyanate-induced apoptosis. J. Biol. Chem. 277 (2002) 8492-8499
10. Hirose M., Yamaguchi T., Kimoto N., Ogawa K., Futakuchi M., Sano M., and Shirai T. Strong promoting activity of phenylethyl isothiocyanate and benzyl isothiocyanate on urinary bladder carcinogenesis in F344 male rats. Int. J. Cancer 77 (1998) 773-777
11. Akagi K., Sano M., Ogawa K., Hirose M., Goshima H., and Shirai T. Involvement of toxicity as an early event in urinary bladder carcinogenesis induced by phenethyl isothiocyanate, benzyl isothiocyanate, and analogues in F344 rats. Toxicol. Pathol. 31 (2003) 388-396
12. Kroemer G., El-Deiry W.S., Golstein P., Peter M.E., Vaux D., Vandenabeele P., Zhivotovsky B., Blagosklonny M.V., Malorni W., Knight R.A., Piacentini M., Nagata S., and Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 12 Suppl 2 (2005) 1463-1467
13. Denecker G., Vercammen D., Declercq W., and Vandenabeele P. Apoptotic and necrotic cell death induced by death domain receptors. Cell Mol. Life Sci. 58 (2001) 356-370
14. Festjens N., Vanden Berghe T., and Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta 1757 (2006) 1371-1387
15. Zong W.X., and Thompson C.B. Necrotic death as a cell fate. Genes Dev. 20 (2006) 1-15
16. Yuan J. Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death. Mol. Cell 23 (2006) 1-12
17. Edinger A.L., and Thompson C.B. Death by design: apoptosis, necrosis and autophagy. Curr. Opin. Cell Biol. 16 (2004) 663-669
18. Zitvogel L., Casares N., Pequignot M.O., Chaput N., Albert M.L., and Kroemer G. Immune response against dying tumor cells. Adv. Immunol. 84 (2004) 131-179
19. Golstein P., and Kroemer G. Redundant cell death mechanisms as relics and backups. Cell Death Differ. 12 Suppl 2 (2005) 1490-1496
20. Chautan M., Chazal G., Cecconi F., Gruss P., and Golstein P. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr. Biol. 9 (1999) 967-970
21. Kroemer G., and Martin S.J. Caspase-independent cell death. Nat. Med. 11 (2005) 725-730
22. Hayashi J., Ohta S., Kikuchi A., Takemitsu M., Goto Y., and Nonaka I. Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc. Natl. Acad. Sci. U. S. A 88 (1991) 10614-10618
23. Miyoshi N., Uchida K., Osawa T., and Nakamura Y. Benzyl isothiocyanate modifies expression of the G2/M arrest-related genes. Biofactors 21 (2004) 23-26
24. Miyoshi N., Uchida K., Osawa T., and Nakamura Y. Selective cytotoxicity of benzyl isothiocyanate in the proliferating fibroblastoid cells. Int. J. Cancer 120 (2007) 484-492
25. Zhang R., Loganathan S., Humphreys I., and Srivastava S.K. Benzyl isothiocyanate-induced DNA damage causes G2/M cell cycle arrest and apoptosis in human pancreatic cancer cells. J. Nutr. 136 (2006) 2728-2734
26. Kalkunte S., Swamy N., Dizon D.S., and Brard L. Benzyl isothiocyanate (BITC) induces apoptosis in ovarian cancer cells in vitro. J. Exp. Ther. Oncol. 5 (2006) 287-300
27. Kuang Y.F., and Chen Y.H. Induction of apoptosis in a non-small cell human lung cancer cell line by isothiocyanates is associated with p53 and p21. Food Chem. Toxicol. 42 (2004) 1711-1718
28. Srivastava S.K., and Singh S.V. Cell cycle arrest, apoptosis induction and inhibition of nuclear factor kappa B activation in anti-proliferative activity of benzyl isothiocyanate against human pancreatic cancer cells. Carcinogenesis 25 (2004) 1701-1709
29. Lui V.W., Wentzel A.L., Xiao D., Lew K.L., Singh S.V., and Grandis J.R. Requirement of a carbon spacer in benzyl isothiocyanate-mediated cytotoxicity and MAPK activation in head and neck squamous cell carcinoma. Carcinogenesis 24 (2003) 1705-1712
30. Yang Y.M., Conaway C.C., Chiao J.W., Wang C.X., Amin S., Whysner J., Dai W., Reinhardt J., and Chung F.L. Inhibition of benzo(a)pyrene-induced lung tumorigenesis in A/J mice by dietary N-acetylcysteine conjugates of benzyl and phenethyl isothiocyanates during the postinitiation phase is associated with activation of mitogen-activated protein kinases and p53 activity and induction of apoptosis. Cancer Res. 62 (2002) 2-7
31. Bonnesen C., Eggleston I.M., and Hayes J.D. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Res. 61 (2001) 6120-6130
32. Yu R., Mandlekar S., Harvey K.J., Ucker D.S., and Kong A.N. Chemopreventive isothiocyanates induce apoptosis and caspase-3-like protease activity. Cancer Res. 58 (1998) 402-408
33. Miyoshi N., Oubrahim H., Chock P.B., and Stadtman E.R. Age-dependent cell death and the role of ATP in hydrogen peroxide-induced apoptosis and necrosis. Proc. Natl. Acad. Sci. U. S. A 103 (2006) 1727-1731
34. Kawakami M., Harada N., Hiratsuka M., Kawai K., and Nakamura Y. Dietary isothiocyanates modify mitochondrial functions through their electrophilic reaction. Biosci. Biotechnol. Biochem. 69 (2005) 2439-2444
35. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 15 (2001) 2922-2933
36. Leist M., Single B., Castoldi A.F., Kuhnle S., and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185 (1997) 1481-1486
37. Nicotera P., and Melino G. Regulation of the apoptosis-necrosis switch. Oncogene 23 (2004) 2757-2765
38. Fishelson Z., Attali G., and Mevorach D. Complement and apoptosis. Mol. Immunol. 38 (2001) 207-219
39. Kanduc D., Mittelman A., Serpico R., Sinigaglia E., Sinha A.A., Natale C., Santacroce R., Di Corcia M.G., Lucchese A., Dini L., Pani P., Santacroce S., Simone S., Bucci R., and Farber E. Cell death: apoptosis versus necrosis (review). Int. J. Oncol. 21 (2002) 165-170
40. Vergara L., Bao X., Bello-Reuss E., and Reuss L. Do connexin 43 gap-junctional hemichannels activate and cause cell damage during ATP depletion of renal-tubule cells?. Acta. Physiol. Scand. 179 (2003) 33-38
41. Leist M., Gantner F., Jilg S., and Wendel A. Activation of the 55 kDa TNF receptor is necessary and sufficient for TNF-induced liver failure, hepatocyte apoptosis, and nitrite release. J. Immunol. 154 (1995) 1307-1316
42. Yoshida H., Kawane K., Koike M., Mori Y., Uchiyama Y., and Nagata S. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437 (2005) 754-758
43. Kawane K., Ohtani M., Miwa K., Kizawa T., Kanbara Y., Yoshioka Y., Yoshikawa H., and Nagata S. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 443 (2006) 998-1002
44. Nagata S. DNA degradation in development and programmed cell death. Annu. Rev. Immunol. 23 (2005) 853-875
45. Nakamura Y., Ohigashi H., Masuda S., Murakami A., Morimitsu Y., Kawamoto Y., Osawa T., Imagawa M., and Uchida K. Redox regulation of glutathione S-transferase induction by benzyl isothiocyanate: correlation of enzyme induction with the formation of reactive oxygen intermediates. Cancer Res. 60 (2000) 219-225
46. Wang X.J., Hayes J.D., Henderson C.J., and Wolf C.R. Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor alpha. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 19589-19594
47. Lee Y.J., and Shacter E. Oxidative stress inhibits apoptosis in human lymphoma cells. J. Biol. Chem. 274 (1999) 19792-19798
48. Lee Y.J., and Shacter E. Hydrogen peroxide inhibits activation, not activity, of cellular caspase-3 in vivo. Free Radic. Biol. Med. 29 (2000) 684-692
49. Conaway C.C., Krzeminski J., Amin S., and Chung F.L. Decomposition rates of isothiocyanate conjugates determine their activity as inhibitors of cytochrome p450 enzymes. Chem. Res. Toxicol. 14 (2001) 1170-1176
50. Tang C.S., and Tang W.J. Inhibition of papain by isothiocyanates. Biochim. Biophys. Acta 452 (1976) 510-520
51. Cornblatt B.S., Ye L., Dinkova-Kostova A.T., Erb M., Fahey J.W., Singh N.K., Chen M.S., Stierer T., Garrett-Mayer E., Argani P., Davidson N.E., Talalay P., Kensler T.W., and Visvanathan K. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis 28 (2007) 1485-1490