Supernatant of bacterial fermented soybean induces apoptosis of human hepatocellular carcinoma Hep 3B cells via activation of caspase 8 and mitochondria

Food and Chemical Toxicology

Volumn 45, Issue 2, 2007, Pages 303-314

  Su, Chun Li ^a   Wu, Chao Jung ^a   Chen, Fang Nan ^b   Wang, Be Jen ^c   Sheu, Shane Rong ^d   Won, Shen Jeu ^e  

^a CHANG JUNG CHRISTIAN UNIVERSITY   (Taiwan)

^b Institute of Nong Cyuan Hao   (Taiwan)

^c NATIONAL CHIAYI UNIVERSITY   (Taiwan)

^d FAR EAST UNIVERSITY   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Caspases; Cyclooxygenase; Fermented soybean; Mitochondria

Indexed keywords

ANTINEOPLASTIC AGENT; BINDING PROTEIN; CASPASE 3; CASPASE 8; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME C; DNA FRAGMENT; KU ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; SC 1;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; BREVIBACILLUS BREVIS; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE G1 PHASE; CELL LYSATE; CELL POPULATION; CLONOGENESIS; COLORECTAL CARCINOMA; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; FERMENTATION; FRAGMENTATION REACTION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SOYBEAN;

ANIMALS; APOPTOSIS; BACILLUS; BACILLUS SUBTILIS; CARCINOMA, HEPATOCELLULAR; CASPASE 8; CELL LINE, TUMOR; CYCLOOXYGENASE 2; DNA FRAGMENTATION; ENZYME ACTIVATION; FERMENTATION; G1 PHASE; HCT116 CELLS; HT29 CELLS; HUMANS; LIVER NEOPLASMS; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; SOYBEANS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); BREVIBACILLUS BREVIS; GLYCINE MAX;

EID: 33845303999     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2006.07.031     Document Type: Article

References (77)

1. Adams J.M., and Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 281 (1998) 1322-1326
2. Amarante-Mendes G.P., Finucane D.M., Martin S.J., Cotter T.G., Salvesen G.S., and Green D.R. Anti-apoptotic oncogenes prevent caspase-dependent and independent commitment for cell death. Cell Death and Differentiation 5 (1998) 298-306
3. Beasley R.P., Hwang L.Y., Lin C.C., and Chien C.S. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet 2 (1981) 1129-1133
4. Belka C., Jendrossek V., Pruschy M., Vink S., Verheij M., and Budach W. Apoptosis-modulating agents in combination with radiotherapy-current status and outlook. International Journal of Radiation Oncology Biology Physics 58 (2004) 542-554
5. Birt D.F., Hendrich S., and Wang W. Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacology & Therapeutics 90 (2001) 157-177
6. Borner C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Molecular Immunology 39 (2003) 615-647
7. Bruix J., and Llovet J.M. Hepatitis B virus and hepatocellular carcinoma. Journal of Hepatology 39 Suppl. 1 (2003) S59-S63
8. Cao D.Z., Sun W.H., Ou X.L., Yu Q., Yu T., Zhang Y.Z., Wu Z.Y., Xue Q.P., and Cheng Y.L. Effects of folic acid on epithelial apoptosis and expression of Bcl-2 and p53 in premalignant gastric lesions. World Journal of Gastroenterology 11 (2005) 1571-1576
9. Chang W.H., Liu J.J., Chen C.H., Huang T.S., and Lu F.J. Growth inhibition and induction of apoptosis in MCF-7 breast cancer cells by fermented soy milk. Nutrition and Cancer 43 (2002) 214-226
10. Chendil D., Das A., Dey S., Mohiuddin M., and Ahmed M.M. Par-4, a pro-apoptotic gene, inhibits radiation-induced NF kappa B activity and Bcl-2 expression leading to induction of radiosensitivity in human prostate cancer cells PC-3. Cancer Biology & Therapy 1 (2002) 152-160
11. Chen S.H., Hu C.P., and Chang C.M. Hepatitis B virus replication in well differentiated mouse hepatocyte cell lines immortalized by plasmid DNA. Cancer Research 52 (1992) 1329-1335
12. Chen D., Stetler R.A., Cao G., Pei W., O'Horo C., Yin X.M., and Chen J. Characterization of the rat DNA fragmentation factor 35/Inhibitor of caspase-activated DNase (Short form). The endogenous inhibitor of caspase-dependent DNA fragmentation in neuronal apoptosis. Journal of Biological Chemistry 275 (2000) 38508-38517
13. Cheng A.S., Chan H.L., Leung W.K., To K.F., Go M.Y., Chan J.Y., Liew C.T., and Sung J.J. Expression of HBx and COX-2 in chronic hepatitis B, cirrhosis and hepatocellular carcinoma: implication of HBx in upregulation of COX-2. Modern Pathology 17 (2004) 1169-1179
14. Chinnaiyan A.M., O'Rourke K., Tewari M., and Dixit V.M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81 (1995) 505-512
15. Compton M.M. A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Reviews 11 (1992) 105-119
16. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
17. Desagher S., and Martinou J.C. Mitochondria as the central control point of apoptosis. Trends in Cell Biology 10 (2000) 369-377
18. Di Leonardo A., Linke S.P., Clarkin K., and Wahl G.M. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes & Development 8 (1994) 2540-2551
19. Dubois R.N., Abramson S.B., Crofford L., Gupta R.A., Simon L.S., Van De Putte L.B., and Lipsky P.E. Cyclooxygenase in biology and disease. FASEB Journal 12 (1998) 1063-1073
20. Du C., Fang M., Li Y., Li L., and Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102 (2000) 33-42
21. Earnshaw W.C., Martins L.M., and Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annual Review of Biochemistry 68 (1999) 383-424
22. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., and Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391 (1998) 43-50
23. Feng S.H., and Lo S.C. Lipid extract of Mycoplasma penetrans proteinase K-digested lipid-associated membrane proteins rapidly activates NF-kB and activator protein 1. Infection and Immunity 67 (1999) 2951-2956
24. Fournier D.B., Erdman Jr. J.W., and Gordon G.B. Soy, its components, and cancer prevention: a review of the in vitro, animal, and human data. Cancer Epidemiology Biomarkers & Prevention 7 (1998) 1055-1065
25. Galle P.R., Hofmann W.J., Walczak H., Schaller H., Otto G., Stremmel W., Krammer P.H., and Runkel L. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. Journal of Experimental Medicine 182 (1995) 1223-1230
26. Green D.R. Apoptosis. Death deceiver. Nature 396 (1998) 629-630
27. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102 (2000) 1-4
28. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
29. Green S., Zeiger E., Palmer K.A., Springer J.A., and Legator M.S. Protocols for the dominant lethal test, host-mediated assay, and in vivo cytogenetic test used in the food and drug administration's review of substances in the GRAS (generally recognized as safe) list. Journal of Toxicology and Environmental Health 1 (1976) 921-928
30. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
31. Hu W., and Kavanagh J.J. Anticancer therapy targeting the apoptotic pathway. Lancet Oncology 4 (2003) 721-729
32. Hung J.H., Su I.J., Lei H.Y., Wang H.C., Lin W.C., Chang W.T., Huang W., Chang W.C., Chang Y.S., Chen C.C., and Lai M.D. Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-κB and pp38 mitogen-activated protein kinase. Journal of Biological Chemistry 279 (2004) 46384-46392
33. Hutchins A.M., Slavin J.L., and Lampe J.W. Urinary isoflavonoid phytoestrogen and lignan excretion after consumption of fermented and unfermented soy products. Journal of American Dietetic Association 95 (1995) 545-551
34. Jacobson M.D., Weil M., and Raff M.C. Programmed cell death in animal development. Cell 88 (1997) 347-354
35. Jiang M.C., Liao C.F., and Lee P.H. Aspirin inhibits matrix metalloproteinase-2 activity, increases E-cadherin production, and inhibits in vitro invasion of tumor cells. Biochemical Biophysical Research Communications 282 (2001) 671-677
36. Komatsu S.I., Watanabe H., Oka T., Tsuge H., Nii H., and Kato N. Vitamin B-6-supplemented diets compared with a low vitamin B-6 diet suppress azoxymethane-induced colon tumorigenesis in mice by reducing cell proliferation. Journal of Nutrition 131 (2001) 2204-2207
37. Komatsu S., Watanabe H., Oka T., Tsuge H., and Kat N. Dietary vitamin B6 suppresses colon tumorigenesis, 8-hydroxyguanosine, 4-hydroxynonenal, and inducible nitric oxide synthase protein in azoxymethane-treated mice. Journal of Nutritional Science and Vitaminology (Tokyo) 48 (2002) 65-68
38. Kroemer G., Zamzami N., and Susin S.A. Mitochondrial control of apoptosis. Immunology Today 18 (1997) 44-51
39. Lee J.C., Lee C.H., Su C.L., Huang C.W., Liu H.S., Lin C.N., and Won S.J. Justicidin A decreases the level of cytosolic Ku70 leading to apoptosis in human colorectal cancer cells. Carcinogenesis 26 (2005) 1716-1730
40. Levin B. An overview of preventive strategies for pancreatic cancer. Annals of Oncology 10 Suppl. 4 (1999) 193-196
41. Li H., and Yuan J. Deciphering the pathways of life and death. Current Opinion in Cell Biology 11 (1999) 261-266
42. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
43. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
44. Llovet J.M., Burroughs A., and Bruix J. Hepatocellular carcinoma. Lancet 362 (2003) 1907-1917
45. Mancinelli F., Caraglia M., Budillon A., Abbruzzese A., and Bismuto E. Molecular dynamics simulation and automated docking of the pro-apoptotic Bax protein and its complex with a peptide designed from the Bax-binding domain of anti-apoptotic Ku70. Journal of Cellular Biochemistry 99 (2006) 305-318
46. Marchetti P., Castedo M., Susin S.A., Zamzami N., Hirsch T., Macho A., Haeffner A., Hirsch F., Geuskens M., and Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. Journal of Experimental Medicine 184 (1996) 1155-1160
47. Moore S.M., Rintoul R.C., Walker T.R., Chilvers E.R., Haslett C., and Sethi T. The presence of a constitutively active phosphoinositide 3-kinase in small cell lung cancer cells mediates anchorage-independent proliferation via a protein kinase B and p70s6k-dependent pathway. Cancer Research 58 (1998) 5239-5247
48. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65 (1983) 55-63
49. Muller M., Strand S., Hug H., Heinemann E.M., Walczak H., Hofmann W.J., Stremmel W., Krammer P.H., and Galle P.R. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. Journal of Clinical Investigation 99 (1997) 403-413
50. Natoli G., Ianni A., Costanzo A., De Petrillo G., Ilari I., Chirillo P., Balsano C., and Levrero M. Resistance to Fas-mediated apoptosis in human hepatoma cells. Oncogene 11 (1995) 1157-1164
51. Newmeyer D.D., and Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112 (2003) 481-490
52. Nicholson D.W. Apoptosis. Baiting death inhibitors. Nature 410 (2001) 33-34
53. Nicoletti I., Migliorati G., Pagliacci M.C., Grignani F., and Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. Journal of Immunological Methods 139 (1991) 271-279
54. Nothwehr S.F., and Martinou J.C. A retention factor keeps death at bay. Nature Cell Biology 5 (2003) 281-283
55. Ohta T., Nakatsugi S., Watanabe K., Kawamori T., Ishikawa F., Morotomi M., Sugie S., Toda T., Sugimura T., and Wakabayashi K. Inhibitory effects of Bifidobacterium-fermented soy milk on 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine-induced rat mammary carcinogenesis, with a partial contribution of its component isoflavones. Carcinogenesis 21 (2000) 937-941
56. Roth W., and Reed J.C. Apoptosis and cancer: when BAX is TRAILing away. Nature Medicine 8 (2002) 216-218
57. Sakahira H., Enari M., and Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391 (1998) 96-99
58. Sandstrom P.A., and Buttke T.M. Autocrine production of extracellular catalase prevents apoptosis of the human CEM T-cell line in serum-free medium. Proceedings of the National Academy of Science of the United States of American 90 (1993) 4708-4712
59. Sawada M., Sun W., Hayes P., Leskov K., Boothman D.A., and Matsuyama S. Ku70 suppresses the apoptotic translocation of Bax to mitochondria. Nature Cell Biology 5 (2003) 320-329
60. Schallmey M., Singh A., and Ward O.P. Developments in the use of Bacillus species for industrial production. Canadian Journal of Microbiology 50 (2004) 1-17
61. Shi Y. A structural view of mitochondria-mediated apoptosis. Nature Structural Biology 8 (2001) 394-401
62. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., Wang H.G., Reed J.C., Nicholson D.W., Alnemri E.S., Green D.R., and Martin S.J. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. Journal of Cell Biology 144 (1999) 281-292
63. Smith W.L., Garavito R.M., and DeWitt D.L. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. Journal of Biological Chemistry 271 (1996) 33157-33160
64. Soldani C., Lazze M.C., Bottone M.G., Tognon G., Biggiogera M., Pellicciari C.E., and Scovassi A.I. Poly(ADP-ribose) polymerase cleavage during apoptosis: when and where?. Experimental Cell Research 269 (2001) 193-201
65. Stewart Z.A., Mays D., and Pietenpol J.A. Defective G1-S cell cycle checkpoint function sensitizes cells to microtubule inhibitor-induced apoptosis. Cancer Research 59 (1999) 3831-3837
66. Tsujii M., and DuBois R.N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 83 (1995) 493-501
67. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. Journal of Cellular Physiology 195 (2003) 158-167
68. Vaux D.L., and Korsmeyer S.J. Cell death in development. Cell 96 (1999) 245-254
69. Wajant H. The Fas signaling pathway: more than a paradigm. Science 296 (2002) 1635-1636
70. Wang B.J., Won S.J., Yu Z.R., and Su C.L. Free radical scavenging and apoptotic effects of Cordyceps sinensis fractionated by supercritical carbon dioxide. Food and Chemical Toxicology 43 (2005) 543-552
71. Watabe M., Machida K., and Osada H. MT-21 is a synthetic apoptosis inducer that directly induces cytochrome c release from mitochondria. Cancer Research 60 (2000) 5214-5222
72. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., and Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
73. Wieder T., Essmann F., Prokop A., Schmelz K., Schulze-Osthoff K., Beyaert R., Dorken B., and Daniel P.T. Activation of caspase-8 in drug-induced apoptosis of B-lymphoid cells is independent of CD95/Fas receptor-ligand interaction and occurs downstream of caspase-3. Blood 97 (2001) 1378-1387
74. Williams G.T. Programmed cell death: apoptosis and oncogenesis. Cell 65 (1991) 1097-1098
75. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 (1980) 555-556
76. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.I., Jones D.P., and Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275 (1997) 1129-1132
77. Yang Z., Liu S., Chen X., Chen H., Huang M., and Zheng J. Induction of apoptotic cell death and in vivo growth inhibition of human cancer cells by a saturated branched-chain fatty acid, 13-methyltetradecanoic acid. Cancer Research 60 (2000) 505-509