ROS-independent JNK activation and multisite phosphorylation of Bcl-2 link diallyl tetrasulfide-induced mitotic arrest to apoptosis

Carcinogenesis

Volumn 33, Issue 11, 2012, Pages 2162-2171

  Kelkel, Mareike ^a   Cerella, Claudia ^a   Mack, Fabienne ^a   Schneider, Thomas ^c   Jacob, Claus ^c   Schumacher, Marc ^a   Dicato, Mario ^a   Diederich, Marc ^a,b  

^a LABORATOIRE DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE DU CANCER   (Luxembourg)

^b Seoul National University   (South Korea)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLYL COMPOUND; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BETA ACTIN; DIALLYL TETRASULFIDE; DIALLYL TRISULFIDE; PACLITAXEL; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TUBULIN; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME ACTIVATION; GARLIC; HUMAN; HUMAN CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION;

ALLYL COMPOUNDS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL CYCLE; ENZYME ACTIVATION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LYMPHOMA, LARGE B-CELL, DIFFUSE; MAP KINASE KINASE 4; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOSIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SULFIDES; TUBULIN; TUMOR CELLS, CULTURED;

EID: 84868629206     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs240     Document Type: Article

References (63)

1. Powolny, A.A. et al. (2008) Multitargeted prevention and therapy of cancer by diallyl trisulfide and related Allium vegetable-derived organosulfur compounds. Cancer Lett., 269, 305-314.
2. Shukla, Y. et al. (2007) Cancer chemoprevention with garlic and its constituents. Cancer Lett., 247, 167-181.
3. Gonzalez, C.A. et al. (2006) Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int. J. Cancer, 118, 2559-2566.
4. Hsing, A.W. et al. (2002) Allium vegetables and risk of prostate cancer: a population-based study. J. Nat. Cancer Inst., 94, 1648-1651.
5. Scherer, C. et al. (2009) Potential role of organic sulfur compounds from Allium species in cancer prevention and therapy. Phytochem Rev., 8, 349-368.
6. Wargovich, M.J. (2001) Colon cancer chemoprevention with ginseng and other botanicals. J. Korean Med. Sci., 16, S81-S86.
7. Cerella, C. et al. (2011) Chemical properties and mechanisms determining the anti-cancer action of garlic-derived organic sulfur compounds. Anticancer Agents Med. Chem., 11, 267-271.
8. Cerella, C. et al. (2011) Naturally occurring organic sulfur compounds: an example of a multitasking class of phytochemicals in anti-cancer research. In Rasooli, I. (Ed.) Anti-Cancer Research, Phytochemicals - Bioactivities and Impact on Health. Vol. 2. InTech, Rijeka, Croatia, pp. 1-40.
9. Anwar, A. et al. (2008) Naturally occurring reactive sulfur species, their activity against Caco-2 cells, and possible modes of biochemical action. J. Sulphur Chem., 29, 251-268.
10. Cerella, C. et al. (2009) Cell cycle arrest in early mitosis and induction of caspase-dependent apoptosis in U937 cells by diallyltetrasulfide (Al2S4). Apoptosis, 14, 641-654.
11. Fukao, T. et al. (2004) The effects of allyl sulfides on the induction of phase II detoxification enzymes and liver injury by carbon tetrachloride. Food Chem. Toxicol, 42, 743-749.
12. Jakubikova, J. et al. (2006) Garlic-derived organosulfides induce cytotoxicity, apoptosis, cell cycle arrest and oxidative stress in human colon carcinoma cell lines. Neoplasma, 53, 191-199.
13. Busch, C. et al. (2010) Diallylpolysulfides induce growth arrest and apoptosis. Int. J. Oncol, 36, 743-749.
14. Viry, E. et al. (2011) Antiproliferative effect of natural tetrasulfides in human breast cancer cells is mediated through the inhibition of the cell division cycle 25 phosphatases. Int. J. Oncol., 38, 1103-1111.
15. Antosiewicz, J. et al. (2006) c-Jun NH(2)-terminal kinase signaling axis regulates diallyl trisulfide-induced generation of reactive oxygen species and cell cycle arrest in human prostate cancer cells. Cancer Res., 66, 5379-5386.
16. Filomeni, G. et al. (2003) Reactive oxygen species-dependent c-Jun NH2-terminal kinase/c-Jun signaling cascade mediates neuroblastoma cell death induced by diallyl disulfide. Cancer Res., 63, 5940-5949.
17. Kim, Y.A. et al. (2007) Mitochondria-mediated apoptosis by diallyl trisulfide in human prostate cancer cells is associated with generation of reactive oxygen species and regulated by Bax/Bak. Mol. Cancer. Ther., 6, 1599-1609.
18. Xiao, D. et al. (2005) Diallyl trisulfide-induced G(2)-M phase cell cycle arrest in human prostate cancer cells is caused by reactive oxygen species-dependent destruction and hyperphosphorylation of Cdc 25 C. Oncogene, 24, 6256-6268.
19. Yang, J.S. et al. (2009) Diallyl disulfide induces apoptosis in human colon cancer cell line (COLO 205) through the induction of reactive oxygen species, endoplasmic reticulum stress, caspases casade and mitochondrial-dependent pathways. Food Chem. Toxicol., 47, 171-179.
20. Yi, L. et al. (2010) Diallyl disulfide induces apoptosis in human leukemia HL-60 cells through activation of JNK mediated by reactive oxygen. Die. Pharmazie., 65, 693-698.
21. Panayiotidis, M. (2008) Reactive oxygen species (ROS) in multistage carcinogenesis. Cancer Lett., 266, 3-5.
22. Hosono, T. et al. (2005) Diallyl trisulfide suppresses the proliferation and induces apoptosis of human colon cancer cells through oxidative modification of beta-tubulin. J. Biol. Chem., 280, 41487-41493.
23. Hosono, T. et al. (2008) Alkenyl group is responsible for the disruption of microtubule network formation in human colon cancer cell line HT-29 cells. Carcinogenesis, 29, 1400-1406.
24. Xiao, D. et al. (2003) Induction of apoptosis by the garlic-derived compound S-allylmercaptocysteine (SAMC) is associated with microtubule depolymerization and c-Jun NH(2)-terminal kinase 1 activation. Cancer Res., 63, 6825-6837.
25. Ghibelli, L. et al. (2010) Multistep and multitask Bax activation. Mitochondrion, 10, 604-613.
26. Ito, T. et al. (1997) Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem., 272, 11671-11673.
27. Ruvolo, P.P. et al. (2001) Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia, 15, 515-522.
28. Yamamoto, K. et al. (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol., 19, 8469-8478.
29. Basu, A. et al. (1998) Microtubule-damaging drugs triggered bcl2 phosphorylation-requirement of phosphorylation on both serine-70 and serine-87 residues of bcl2 protein. Int. J. Oncol., 13, 659-664.
30. Haldar, S. et al. (1995) Inactivation of Bcl-2 by phosphorylation. Proc. Natl. Acad. Sci. U. S. A., 92, 4507-4511.
31. Haldar, S. et al. (1996) Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res., 56, 1253-1255.
32. Derbesy, G. et al. (1994) A simple method to prepare unsymmetrical di- triand tetrasulfides. Tetrahedron Lett., 35, 5381-5384.
33. Milligan, B. et al. (1961) New syntheses of trisulphides. J. Chem. Soc., 4850-4853.
34. Schneider, T. et al. (2011) Interactions of polysulfanes with components of red blood cells. Med. Chem. Comm., 2, 196-200.
35. Juncker, T. et al. (2011) UNBS1450, a steroid cardiac glycoside inducing apoptotic cell death in human leukemia cells. Biochem. Pharmacol., 81, 13-23.
36. Schumacher, M. et al. (2010) Heteronemin, a spongean sesterterpene, inhibits TNF alpha-induced NF-kappa B activation through proteasome inhibition and induces apoptotic cell death. Biochem. Pharmacol., 79, 610-622.
37. Wang, H.C. et al. (2010) Allyl sulfides inhibit cell growth of skin cancer cells through induction of DNA damage mediated G2/M arrest and apoptosis. J. Agric. Food Chem., 58, 7096-7103.
38. Wu, X.J. et al. (2009) Apoptosis induction in human lung adenocarcinoma cells by oil-soluble allyl sulfides: triggers, pathways, and modulators. Environ. Mol. Mutagen., 50, 266-275.
39. Dickinson, D.A. et al. (2002) Cellular glutathione and thiols metabolism. Biochem. Pharmacol., 64, 1019-1026.
40. Cerella, C. et al. (2011) COX-2 inhibitors block chemotherapeutic agent-induced apoptosis prior to commitment in hematopoietic cancer cells. Biochem. Pharmacol., 82, 1277-1290.
41. Singh, P. et al. (2008) Microtubule assembly dynamics: an attractive target for anticancer drugs. IUBMB life, 60, 368-375.
42. Karr, T.L. et al. (1980) Calcium ion induces endwise depolymerization of bovine brain microtubules. J. Biol. Chem., 255, 11853-11856.
43. Munchberg, U. et al. (2007) Polysulfides as biologically active ingredients of garlic. Org. Biomol. Chem., 5, 1505-1518.
44. Wang, T.H. et al. (1998) Microtubule-interfering agents activate c-Jun N-terminal kinase/stress-activated protein kinase through both Ras and apoptosis signal-regulating kinase pathways. J. Biol. Chem., 273, 4928-4936.
45. Mhaidat, N.M. et al. (2007) Docetaxel-induced apoptosis of human melanoma is mediated by activation of c-Jun NH2-terminal kinase and inhibited by the mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway. Clin. Cancer Res., 13, 1308-1314.
46. Wang, T.H. et al. (1999) Microtubule dysfunction induced by paclitaxel initiates apoptosis through both c-Jun N-terminal kinase (JNK)-dependent and -independent pathways in ovarian cancer cells. J. Biol. Chem., 274, 8208-8216.
47. Lee, L.F. et al. (1998) Paclitaxel (Taxol)-induced gene expression and cell death are both mediated by the activation of c-Jun NH2-terminal kinase (JNK/SAPK). J. Biol. Chem., 273, 28253-28260.
48. Fan, M. et al. (2000) Modulation of mitogen-activated protein kinases and phosphorylation of Bcl-2 by vinblastine represent persistent forms of normal fluctuations at G2-M1. Cancer Res., 60, 6403-6407.
49. Lei, X.Y. et al. (2008) Apoptosis induced by diallyl disulfide in human breast cancer cell line MCF-7. Acta Pharmacol. Sin., 29, 1233-1239.
50. Radogna, F. et al. (2007) Melatonin antagonizes apoptosis via receptor interaction in U937 monocytic cells. J. Pineal Res., 43, 154-162.
51. Enyedy, I.J. et al. (2001) Discovery of small-molecule inhibitors of Bcl-2 through structure-based computer screening. J. Med. Chem., 44, 4313-4324.
52. Song, J.D. et al. (2009) Molecular mechanism of diallyl disulfide in cell cycle arrest and apoptosis in HCT-116 colon cancer cells. J. Biochem. Mol. Toxicol., 23, 71-79.
53. Prager-Khoutorsky, M. et al. (2007) Allicin inhibits cell polarization, migration and division via its direct effect on microtubules. Cell Motil. Cytoskeleton, 64, 321-337.
54. Xiao, D. et al. (2004) Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene, 23, 5594-5606.
55. Lee, B.C. et al. (2011) Role of Bim in diallyl trisulfide-induced cytotoxicity in human cancer cells. J. Cell. Biochem., 112, 118-127.
56. Basu, A. et al. (2003) Identification of a novel Bcl-xL phosphorylation site regulating the sensitivity of taxol- or 2-methoxyestradiol-induced apoptosis. FEBS Lett., 538, 41-47.
57. Chen, J. et al. (2008) Microtubule depolymerization and phosphorylation of c-Jun N-terminal kinase-1 and p38 were involved in gambogic acid induced cell cycle arrest and apoptosis in human breast carcinoma MCF-7 cells. Life Sci., 83, 103-109.
58. Stone, A.A. et al. (2000) Microtubule inhibitors elicit differential effects on MAP kinase (JNK, ERK, and p38) signaling pathways in human KB-3 carcinoma cells. Exp. Cell Res., 254, 110-119.
59. Ueda, S. et al. (2002) Redox control of cell death. Antioxid. Redox Signal., 4, 405-414.
60. Nagata, K. et al. (1998) The MAP kinase kinase kinase MLK2 co-localizes with activated JNK along microtubules and associates with kinesin superfamily motor KIF3. EMBO J., 17, 149-158.
61. Pereira, A.M. et al. (2011) Integrin-dependent activation of the JNK signaling pathway by mechanical stress. PloS one, 6, e26182.
62. Oktay, K. et al. (2008) The c-Jun N-terminal kinase JNK functions upstream of Aurora B to promote entry into mitosis. Cell Cycle, 7, 533-541.
63. Hirota, T. et al. (2005) Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature, 438, 1176-1180.