Critical role of p53 upregulated modulator of apoptosis in benzyl isothiocyanate-induced apoptotic cell death

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Antony, Marie Lue ^a   Kim, Su Hyeong ^a   Singh, Shivendra V ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYL ISOTHIOCYANATE; BIM PROTEIN; CYCLIN DEPENDENT KINASE 1; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P21; PUMA PROTEIN; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; BBC3 PROTEIN, HUMAN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; ISOTHIOCYANIC ACID DERIVATIVE; MEMBRANE PROTEIN; ONCOPROTEIN;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RESISTANCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; KNOCKOUT GENE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RNA INTERFERENCE; TUMOR XENOGRAFT; UPREGULATION; WILD TYPE; CHEMISTRY; PHYSIOLOGY; TUMOR CELL LINE; VEGETABLE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; HUMANS; ISOTHIOCYANATES; MEMBRANE PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; VEGETABLES;

EID: 84863173894     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032267     Document Type: Article

References (48)

1. Sahin K, Tuzcu M, Sahin N, Akdemir F, Ozercan I, et al. (2011) Inhibitory effects of combination of lycopene and genistein on 7,12- dimethyl benz(a)anthracene-induced breast cancer in rats. Nutr Cancer 63: 1279-1286.
2. Sakata M, Ikeda T, Imoto S, Jinno H, Kitagawa Y, (2011) Prevention of mammary carcinogenesis in C3H/OuJ mice by green tea and tamoxifen. Asian Pac J Cancer Prev 12: 567-571.
3. Park K, Choi K, Kim H, Kim K, Lee MH, et al. (2009) Isoflavone-deprived soy peptide suppresses mammary tumorigenesis by inducing apoptosis. Exp Mol Med 41: 371-381.
4. Jemal A, Siegel R, Xu J, Ward E, (2010) Cancer Statistics, 2010. CA Cancer J Clin 60: 277-300.
5. Wattenberg LW, (1977) Inhibition of carcinogenic effects of polycyclic hydrocarbons by benzyl isothiocyanate and related compounds. J Natl Cancer Inst 58: 395-398.
6. Warin R, Chambers WH, Potter DM, Singh SV, (2009) Prevention of mammary carcinogenesis in MMTV-neu mice by cruciferous vegetable constituent benzyl isothiocyanate. Cancer Res 69: 9473-9480.
7. Warin R, Xiao D, Arlotti JA, Bommareddy A, Singh SV, (2010) Inhibition of human breast cancer xenograft growth by cruciferous vegetable constituent benzyl isothiocyanate. Mol Carcinogenesis 49: 500-507.
8. Kim EJ, Hong JE, Eom SJ, Lee JY, Park JH, (2011) Oral administration of benzyl-isothiocyanate inhibits solid tumor growth and lung metastasis of 4T1 murine mammary carcinoma cells in BALB/c mice. Breast Cancer Res Treat 130: 61-71.
9. Zhang Y, Tang L, Gonzalez V, (2003) Selected isothiocyanates rapidly induce growth inhibition of cancer cells. Mol Cancer Ther 2: 1045-1052.
10. Tseng E, Scott-Ramsay EA, Morris ME, (2004) Dietary organic isothiocyanates are cytotoxic in human breast cancer MCF-7 and mammary epithelial MCF-12A cell lines. Exp Biol Med 229: 835-842.
11. Xiao D, Vogel V, Singh SV, (2006) Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol Cancer Ther 5: 2931-2945.
12. Xiao D, Powolny AA, Singh SV, (2008) Benzyl isothiocyanate targets mitochondrial respiratory chain to trigger reactive oxygen species-dependent apoptosis in human breast cancer cells. J Biol Chem 283: 30151-30163.
13. Kim SH, Singh SV, (2010) p53-Independent apoptosis by benzyl isothiocyanate in human breast cancer cells is mediated by suppression of XIAP expression. Cancer Prev Res 3: 718-726.
14. Kim SH, Nagalingam A, Saxena NK, Singh SV, Sharma D, (2011) Benzyl isothiocyanate inhibits oncogenic actions of leptin in human breast cancer cells by suppressing activation of signal transducer and activator of transcription 3. Carcinogenesis 32: 359-367.
15. Sehrawat A, Singh SV, (2011) Benzyl isothiocyanate inhibits epithelial-mesenchymal transition in cultured and xenografted human breast cancer cells. Cancer Prev Res 4: 1107-1117.
16. Chao DT, Korsmeyer SJ, (1998) Bcl-2 family: regulators of cell death. Annu Rev Immunol 16: 395-419.
17. Adams JM, Cory S, (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
18. Akiyama T, Dass CR, Choong PF, (2009) Bim-targeted cancer therapy: a link between drug action and underlying molecular changes. Mol Cancer Ther 8: 3173-3180.
19. Gillings AS, Balmanno K, Wiggins CM, Johnson M, Cook SJ, (2009) Apoptosis and autophagy: BIM as a mediator of tumour cell death in response to oncogene-targeted therapeutics. FEBS J 276: 6050-6062.
20. Yu J, Zhang L, (2008) PUMA, a potent killer with or without p53. Oncogene 27: S71-S83.
21. Shanlou Q, Keiko M, Qinghong Z, Baoling W, Hisao S, et al. (2011) Mimosine-induced apoptosis in C6 glioma cells requires the release of mitochondria-derived reactive oxygen species and p38, JNK activation. Neurochem Res DOI 10.1007/s11064-011-0628-6.
22. Dhansekaran DN, Reddy EP, (2008) JNK signaling and apoptosis. Oncogene 27: 6245-6251.
23. Xiao D, Choi S, Johnson DE, Vogel VG, Johnson CS, 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.
24. Xiao D, Zeng Y, Prakash L, Badmaev V, Majeed M, et al. (2011) Reactive oxygen species-dependent apoptosis by gugulipid extract of Ayurvedic medicine plant Commiphora mukul in human prostate cancer cells is regulated by c-JUN N-terminal kinase. Mol Pharmacol 79: 499-507.
25. Putcha GV, Le S, Frank S, Besirli CG, Clark K, et al. (2003) JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 38: 899-914.
26. Lei K, Davis RJ, (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100: 2432-2437.
27. Jabbour AM, Heraud JE, Daunt CP, Kaufmann T, Sandow J, et al. (2009) Puma indirectly activates Bax to cause apoptosis in the absence of Bid or Bim. Cell Death Differ 16: 555-563.
28. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B, (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7: 673-682.
29. Kaeser MD, Iggo RD, (2002) Chromatin immunoprecipitation analysis fails to support the latency model for regulation of p53 DNA binding activity in vivo. Proc Natl Acad Sci USA 99: 95-100.
30. Wang P, Yu J, Zhang L, (2007) The nuclear function of p53 is required for PUMA-mediated apoptosis induced by DNA damage. Proc Natl Acad Sci USA 104: 4054-4059.
31. Wu WS, Heinrichs S, Xu D, Garrison SP, Zambetti GP, et al. (2005) Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123: 641-653.
32. Melino G, Bernassola F, Ranalli M, Yee K, Zong WX, et al. (2004) p73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J Biol Chem 279: 8076-8083.
33. You H, Pellegrini M, Tsuchihara K, Yamamoto K, Hacker G, et al. (2006) FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med 203: 1657-1663.
34. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, et al. (2003) Genomic targets of the human c-Myc protein. Genes Dev 17: 1115-1129.
35. Hershko T, Ginsberg D, (2004) Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F1 mediates apoptosis. J Biol Chem 279: 8627-8634.
36. Iyer NG, Chin SF, Ozdag H, Daigo Y, Hu DE, et al. (2004) p300 regulates p53-dependent apoptosis after DNA damage in colorectal cancer cells by modulation of PUMA/p21 levels. Proc Natl Acad Sci USA 101: 7386-7391.
37. Jackson JG, Pereira-Smith OM, (2006) p53 is preferentially recruited to the promoters of growth arrest genes p21 and GADD45 during replicative senescence of normal human fibroblasts. Cancer Res 66: 8356-8360.
38. Steckley D, Karajgikar M, Dale LB, Fuerth B, Swan P, et al. (2007) Puma is a dominant regulator of oxidative stress induced Bax activation and neuronal apoptosis. J Neurosci 27: 12989-12999.
39. Macip S, Igarashi M, Berggren P, Yu J, Lee SW, et al. (2003) Influence of induced reactive oxygen species in p53-mediated cell fate decisions. Mol Cell Biol 23: 8576-8585.
40. Liu Z, Lu H, Shi H, Du Y, Yu J, et al. (2005) PUMA overexpression induces reactive oxygen species generation and proteasome-mediated stathmin degradation in colorectal cancer cells. Cancer Res 65: 1647-1654.
41. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L, (2003) PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 100: 1931-1936.
42. Ming L, Wang P, Bank A, Yu J, Zhang L, (2006) PUMA dissociates Bax and Bcl-X(L) to induce apoptosis in colon cancer cells. J Biol Chem 281: 16034-16042.
43. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403.
44. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, et al. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535.
45. Xiao D, Srivastava SK, Lew KL, Zeng Y, Hershberger P, et al. (2003) Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits proliferation of human prostate cancer cells by causing G2/M arrest and inducing apoptosis. Carcinogenesis 24: 891-897.
46. Xiao D, Lew KL, Kim YA, Zeng Y, Hahm ER, et al. (2006) Diallyl trisulfide suppresses growth of PC-3 human prostate cancer xenograft in vivo in association with Bax and Bak induction. Clin Cancer Res 15: 6836-6843.
47. Powolny AA, Bommareddy A, Hahm ER, Normolle DP, Beumer JH, et al. (2011) Chemopreventative potential of the cruciferous vegetable constituent phenethyl isothiocyanate in a mouse model of prostate cancer. J Natl Cancer Inst 103: 571-584.
48. Herman-Antosiewicz A, Singh SV, (2005) Checkpoint kinase 1 regulates diallyl trisulfide-induced mitotic arrest in human prostate cancer cells. J Biol Chem 280: 28519-28528.