Sulforaphane sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-resistant hepatoma cells to TRAIL-induced apoptosis through reactive oxygen species-mediated up-regulation of DR5

Cancer Research

Volumn 66, Issue 3, 2006, Pages 1740-1750

  Kim, Heesue ^a   Kim, Eun Hee ^a   Eom, Young Woo ^a   Kim, Wook Hwan ^a   Kwon, Taeg Kyu ^b   Lee, Soo Jae ^c   Choi, Kyeong Sook ^a  

^a Ajou University School of Medicine   (South Korea)

^b Keimyung University   (South Korea)

^c Korea Institute of Radiation and Medical Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING ANTIBODY; DEATH RECEPTOR; MESSENGER RNA; N ACETYLASPARTIC ACID; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SULFORAPHANE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEDIATED CYTOTOXICITY; CHEMOPROPHYLAXIS; DRUG EFFECT; DRUG SENSITIVITY; ENZYME INHIBITION; HEPATOMA CELL; HISTOPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-X PROTEIN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; HEPATOCYTES; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; LIVER NEOPLASMS; MEMBRANE GLYCOPROTEINS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; THIOCYANATES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANS-ACTIVATION (GENETICS); TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 32944475745     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-1568     Document Type: Article

References (52)

1. Ashkenazi A, Pai RC, Fong S, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999;104:155-62.
2. Ashkenazi A, Dixit VM. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 1999;11:255-60.
3. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000;12:611-20.
4. Srivastava RK. TRAIL/Apo-2L: mechanisms and clinical applications in cancer. Neoplasia 2001;3:535-46.
5. Parkin DM. Global cancer statistics in the year 2000. Lancet Oncol 2001;2:533-43.
6. Carr BI. Hepatocellular carcinoma: current management and future trends. Gastroenterology 2004;127: S218-24.
7. Yamanaka T, Shiraki K, Sugimoto K, et al. Chemotherapeutic agents augment TRAIL-induced apoptosis in human hepatocellular carcinoma cell lines. Hepatology 2000;32:482-90.
8. Shankar S, Srivastava R. Enhancement of therapeutic potential of TRAIL by cancer chemotherapy and irradiation: mechanisms and clinical implications. Drug Resist Updat 2004;7:139-56.
9. Cohen JH, Kristal AR, Stanford JL. Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 2000;5:61-8.
10. Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci U S A 1997;94:10367-72.
11. Barcelo S, Gardiner JM, Gescher A, Chipman JK. CYP2E1-mediated mechanism of anti-genotoxicity of the broccoli constituent sulforaphane. Carcinogenesis 1996;17:277-82.
12. Brooks JD, Paton VG, Vidanes G. Potent induction of phase 2 enzymes in human prostate cells by sulforaphane. Cancer Epidemiol Biomarkers Prev 2001;10:949-54.
13. Gamet-Payrastre L, Li P, Lumeau S, et al. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 2000;60:1426-33.
14. Fimognari C, Nusse M, Cesari R, Iori R, Cantelli-Forti G, Hrelia P. Growth inhibition, cell-cycle arrest and apoptosis in human T-cell leukemia by the isothiocyanate sulforaphane. Carcinogenesis 2002;23:581-6.
15. Roncero C, Lorenzo M, Fabregat I, Benito M. Rates of lipogenesis in fetal hepatocytes in suspension and in primary culture: hormonal effects. Biochim Biophys Acta 1989;1012:320-4.
16. Kim YH, Park JW, Lee JY, Kwon TK. Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 2004;25:1813-20.
17. Kim EH, Kim SU, Shin DY, Choi KS. Roscovitine sensitizes glioma cells to TRAIL-mediated apoptosis by downregulation of survivin and XIAP. Oncogene 2004;23:446-56.
18. Chawla-Sarker M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004;11:915-23.
19. Bai J, Sui J, Demirjian A, Vollmer CM, Jr, Marasco W, Gallery MP. Predominant Bcl-XL knockdown disables antiapoptotic mechanisms: tumor necrosis factor-related apoptosis-inducing ligand-based triple chemotherapy overcomes chemoresistance in pancreatic cancer cells in vitro. Cancer Res 2005;65:2344-52.
20. Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS, Reed JC. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 1999;18:5241-51.
21. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001;104:487-501.
22. Pan G, O'Rourke K, Chinnaiyan AM, et al. The receptor for the cytotoxic ligand TRAIL. Science 1997;276:111-3.
23. Sheridan JP, Marsters SA, Pitti RM, et al. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997;277:818-21.
24. Yoshida T, Maeda A, Tani N, Sakai T. Promoter structure and transcription initiation sites of the human death receptor 5/TRAIL-R2 gene. FEBS Lett 2001;507:381-5.
25. Singh SV, Srivastava SK, Choi S, et al. Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J Biol Chem 2005;280:19911-24.
26. Takehara T, Liu X, Fujimoto J, Friedman SL, Takahashi H. Expression and role of Bcl-xL in human hepatocellular carcinomas. Hepatology 2001;34:55-61.
27. Fiers W. Tumor necrosis factor. Characterization at the molecular, cellular and in vivo level. FEES Lett 1991;285:199-212.
28. Ogasawara J, Watanabe-Fukunaga R, Adachi M, et al. Lethal effect of the anti-Fas antibody in mice. Nature 1993;364:806-9.
29. Hao C, Song JH, Hsi B, et al. TRAIL inhibits tumor growth but is nontoxic to human hepatocytes in chimeric mice. Cancer Res 2004;64:8502-6.
30. Pei Z, Chu L, Zou W, et al. An oncolytic adenoviral vector of Smac increases antitumor activity of TRAIL against HCC in human cells and in mice. Hepatology 2004;39:1371-81.
31. Kim YS, Schwabe RF, Qian T, Lemasters JJ, Brenner DA. TRAIL-mediated apoptosis requires NF-κB inhibition and the mitochondrial permeability transition in human hepatoma cells. Hepatology 2002;36:1498-508.
32. Van Geelen CM, de Vries EG, de Jong S. Lessons from TRAIL-resistance mechanisms in colorectal cancer cells: paving the road to patient-tailored therapy. Drug Resist Updat 2004;7:345-58.
33. LeBlanc H, Lawrence D, Varfolomeev E, et al. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002;8:274-81.
34. Truneh A, Sharma S, Silverman C, et al. Temperature-sensitive differential affinity of TRAIL for its receptors. DR5 is the highest affinity receptor. J Biol Chem 2000;275:23319-25.
35. Kelley RF, Totpal K, Lindstrom SH, et al. Receptor-selective mutants of apoptosis-inducing ligand 2/tumor necrosis factor-related apoptosis-inducing ligand reveal a greater contribution of death receptor (DR) 5 than DR4 to apoptosis signaling. J Biol Chem 2005;280:2205-12.
36. Chinnaiyan AM, Prasad U, Shankar S, et al. Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc Natl Acad Sci U S A 2000;97:1754-9.
37. Wang S, El-Deiry WS. Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci U S A 2003;100:15095-100.
38. Nakata S, Yoshida T, Horinaka M, et al. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004;23:6261-71.
39. Higuchi H, Grambihler A, Canbay A, Bronk SF, Gores GJ. Bile acids up-regulate death receptor 5/TRAIL-receptor 2 expression via a c-Jun N-terminal kinase-dependent pathway involving Sp1. J Biol Chem 2004;279:51-60.
40. Shigeno M, Nakao K, Ichikawa T, et al. Interferon-α sensitizes human hepatoma cells to TRAIL-induced apoptosis through DR5 upregulation and NF-κB inactivation. Oncogene 2003;22:1653-62.
41. 2-terminal kinase-mediated up-regulation of death receptor 5 contributes to induction of apoptosis by the novel synthetic triterpenoid methyl-2-cyano-3,12-dioxooleana-1,9-dien-28-oate in human lung cancer cells. Cancer Res 2004;64:7570-8.
42. He Q, Huang Y, Sheikh MS. Proteasome inhibitor MG132 upregulates death receptor 5 and cooperates with Apo2L/TRAIL to induce apoptosis in Bax-proficient and -deficient cells. Oncogene 2004;23:2554-8.
43. 2-M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C. J Biol Chem 2004;279:25813-22.
44. Paolini M, Perocco P, Canistro D, et al. Induction of cytochrome P450, generation of oxidative stress and in vitro cell-transforming and DNA-damaging activities by glucoraphanin, the bioprecursor of the chemopreventive agent sulforaphane found in broccoli. Carcinogenesis 2004;25:61-7.
45. Murata M, Yamashita N, Inoue S, Kawanishi S. Mechanism of oxidative DNA damage induced by carcinogenic allyl isothiocyanate. Free Radic Biol Med 2000;28:797-805.
46. Tang L, Zhang Y. Mitochondria are the primary target in isothiocyanate-induced apoptosis in human bladder cancer cells. Mol Cancer Ther 2005;4:1250-9.
47. Velculescu VE, El-Deiry WS. Biological and clinical importance of the p53 tumor suppressor gene. Clin Chem 1996;42:858-68.
48. Nishida N, Fukuda Y, Kokuryu H, et al. Role and mutational heterogeneity of the p53 gene in hepatocellular carcinoma. Cancer Res 1993;53:368-72.
49. Hsu IC, Tokiwa T, Bennett W, et al. p53 gene mutation and integrated hepatitis B viral DNA sequences in human liver cancer cell lines. Carcinogenesis 1993;14:987-92.
50. Kang MS, Lee HJ, Lee JH, et al. Mutation of p53 gene in hepatocellular carcinoma cell lines with HBX DNA. Int J Cancer 1996;67:898-902.
51. Staib F, Hussein SP, Hofseth LJ, Wang XW, Harris CC. TP53 and liver Carcinogenesis. Hum Mutat 2003;21:201-16.
52. Watanabe J, Kushihata F, Honda K, et al. Prognostic significance of Bcl-xL in human hepatocellular carcinoma. Surgery 2004;135:604-12.