Adenovirus 5 E1A enhances histone deacetylase inhibitors-induced apoptosis through Egr-1-mediated Bim upregulation

Oncogene

Volumn 29, Issue 41, 2010, Pages 5619-5629

  Yamaguchi, H ^a   Chen, C T ^a,b   Chou, C K ^a   Pal, A ^a   Bornmann, W ^a   Hortobagyi, G N ^a   Hung, M C ^a,b,c,d  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d ASIA UNIVERSITY   (Taiwan)

Author keywords

apoptosis; Bim; E1A; gene therapy; HDAC inhibitors

Indexed keywords

ADENOVIRUS 5 E1A PROTEIN; ADENOVIRUS VECTOR; BIM PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; ETOPOSIDE; FLUOROURACIL; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; PACLITAXEL; PROTEIN BCL XL; UNCLASSIFIED DRUG; VORINOSTAT;

ADENOVIRUS 5; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; GENE THERAPY; HUMAN; HUMAN CELL; LIPOSOMAL GENE DELIVERY SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACETYLATION; ADENOVIRUS E1 PROTEINS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; GENE THERAPY; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; HYDROXAMIC ACIDS; MEMBRANE PROTEINS; MICE; NEOPLASMS, EXPERIMENTAL; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

HUMAN ADENOVIRUS TYPE 5;

EID: 77958015556     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.295     Document Type: Article

References (58)

1. Baek SJ, Wilson LC, Hsi LC, Eling TE. (2003). Troglitazone, a peroxisome proliferator-activated receptor gamma (PPAR gamma ) ligand, selectively induces the early growth response-1 gene independently of PPAR gamma. A novel mechanism for its anti-tumorigenic activity. J Biol Chem 278: 5845-5853.
2. Bolden JE, Peart MJ, Johnstone RW. (2006). Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784.
3. Bouillet P, Zhang LC, Huang DC, Webb GC, Bottema CD, Shore P et al. (2001). Gene structure alternative splicing, and chromosomal localization of pro-apoptotic Bcl-2 relative Bim. Mamm Genome 12: 163-168.
4. Brader KR, Wolf JK, Hung MC, Yu D, Crispens MA, van Golen KL et al. (1997). Adenovirus E1A expression enhances the sensitivity of an ovarian cancer cell line to multiple cytotoxic agents through an apoptotic mechanism. Clin Cancer Res 3: 2017-2024.
5. Burgess A, Ruefli A, Beamish H, Warrener R, Saunders N, Johnstone R et al. (2004). Histone deacetylase inhibitors specifically kill nonproliferating tumour cells. Oncogene 23: 6693-6701.
6. Byrd PJ, Grand RJ, Gallimore PH. (1988). Differential transformation of primary human embryo retinal cells by adenovirus E1 regions and combinations of E1A+ ras. Oncogene 2: 477-484.
7. Chang JY, Xia W, Shao R, Sorgi F, Hortobagyi GN, Huang L et al. (1997). The tumor suppression activity of E1A in HER-2/ neu-overexpressing breast cancer. Oncogene 14: 561-568.
8. Chou CK, Lee DF, Sun HL, Li LY, Lin CY, Huang WC et al. (2009). The suppression of MAD1 by AKT-mediated phosphorylation activates MAD1 target genes transcription. Mol Carcinog 48: 1048-1058.
9. Cook JL, Routes JM. (2005). Adenovirus E1A gene-induced tumor cell rejection through cellular sensitization to immune and nonimmune apoptotic injuries. Front Biosci 10: 1396-1414.
10. Day CP, Rau KM, Qiu L, Liu CW, Kuo HP, Xie X et al. (2006). Mutant Bik expression mediated by the enhanced minimal topoisomerase IIalpha promoter selectively suppressed breast tumors in an animal model. Cancer Gene Ther 13: 706-719.
11. Deng J, Xia W, Hung MC. (1998). Adenovirus 5 E1A-mediated tumor suppression associated with E1A-mediated apoptosis in vivo. Oncogene 17: 2167-2175.
12. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. (1966). Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 50: 219-244.
13. Frisch SM. (1991). Antioncogenic effect of adenovirus E1A in human tumor cells. Proc Natl Acad Sci USA 88: 9077-9081.
14. Frisch SM. (2004). E1A as a tumor suppressor gene: commentary re S. Madhusudan et al. A multicenter Phase I gene therapy clinical trial involving intraperitoneal administration of E1A-lipid complex in patients with recurrent epithelial ovarian cancer overexpressing HER-2/neu oncogene. Clin Cancer Res 10: 2905-2907.
15. Frisch SM, Mymryk JS. (2002). Adenovirus-5 E1A: paradox and paradigm. Nat Rev Mol Cell Biol 3: 441-452.
16. Hortobagyi GN, Ueno NT, Xia W, Zhang S, Wolf JK, Putnam JB et al. (2001). Cationic liposome-mediated E1A gene transfer to human breast and ovarian cancer cells and its biologic effects: a phase I clinical trial. J Clin Oncol 19: 3422-3433.
17. Hubberstey AV, Pavliv M, Parks RJ. (2002). Cancer therapy utilizing an adenoviral vector expressing only E1A. Cancer Gene Ther 9: 321-329.
18. Hung MC, Hortobagyi GN, Ueno NT. (2000). Development of clinical trial of E1A gene therapy targeting HER-2/neu-overexpressing breast and ovarian cancer. Adv Exp Med Biol 465: 171-180.
19. Lane AA, Chabner BA. (2009). Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 27: 5459-5468.
20. Liao Y, Yu D, Hung MC. (2007). Novel approaches for chemosensi-tization of breast cancer cells: the E1A story. Adv Exp Med Biol 608: 144-169.
21. Liao Y, Zou YY, Xia WY, Hung MC. (2004). Enhanced paclitaxel cytotoxicity and prolonged animal survival rate by a nonviral-mediated systemic delivery of E1A gene in orthotopic xenograft human breast cancer. Cancer Gene Ther 11: 594-602.
22. Liu JW, Chandra D, Rudd MD, Butler AP, Pallotta V, Brown D et al. (2005). Induction of prosurvival molecules by apoptotic stimuli: involvement of FOXO3a and ROS. Oncogene 24: 2020-2031.
23. Lo HW, Day CP, Hung MC. (2005). Cancer-specific gene therapy. Adv Genet 54: 235-255.
24. Lowe SW, Ruley HE, Jacks T, Housman DE. (1993). p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967.
25. Lubieniecka JM, de Bruijn DR, Su L, van Dijk AH, Subramanian S, van de Rijn M et al. (2008). Histone deacetylase inhibitors reverse SS18-SSX-mediated polycomb silencing of the tumor suppressor early growth response 1 in synovial sarcoma. Cancer Res 68: 4303-4310.
26. Madhusudan S, Tamir A, Bates N, Flanagan E, Gore ME, Barton DP et al. (2004). A multicenter Phase I gene therapy clinical trial involving intraperitoneal administration of E1A-lipid complex in patients with recurrent epithelial ovarian cancer overexpressing HER-2/neu oncogene. Clin Cancer Res 10: 2986-2996.
27. Marks PA, Breslow R. (2007). Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 25: 84-90.
28. Minucci S, Pelicci PG. (2006). Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51.
29. Pan L, Lu J, Wang X, Han L, Zhang Y, Han S et al. (2007). Histone deacetylase inhibitor trichostatin a potentiates doxorubicin-induced apoptosis by up-regulating PTEN expression. Cancer 109: 1676-1688.
30. Pirollo KF, Chang EH. (2008). Targeted delivery of small interfering RNA: approaching effective cancer therapies. Cancer Res 68: 1247-1250.
31. Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, White E. (1992). The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc Natl Acad Sci USA 89: 7742-7746.
32. Reagan-Shaw S, Nihal M, Ahmad N. (2008). Dose translation from animal to human studies revisited. Faseb J 22: 659-661.
33. Ruley HE. (1983). Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature 304: 602-606.
34. Samuelson AV, Lowe SW. (1997). Selective induction of p53 and chemosensitivity in RB-deficient cells by E1A mutants unable to bind the RB-related proteins. Proc Natl Acad Sci USA 94: 12094-12099.
35. Stoff-Khalili MA, Dall P, Curiel DT. (2006). Gene therapy for carcinoma of the breast. Cancer Gene Ther 13: 633-647.
36. Sunters A, Fernandez de Mattos S, Stahl M, Brosens JJ, Zoumpou-lidou G, Saunders CA et al. (2003). FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 278: 49795-49805.
37. Thiel G, Cibelli G. (2002). Regulation of life and death by the zinc finger transcription factor Egr-1. J Cell Physiol 193: 287-292.
38. Ueno NT, Bartholomeusz C, Herrmann JL, Estrov Z, Shao R, Andreeff M et al. (2000). E1A-mediated paclitaxel sensitization in HER-2/neu-overexpressing ovarian cancer SKOV3.ip1 through apoptosis involving the caspase-3 pathway. Clin Cancer Res 6: 250-259.
39. Ueno NT, Bartholomeusz C, Xia W, Anklesaria P, Bruckheimer EM, Mebel E et al. (2002). Systemic gene therapy in human xenograft tumor models by liposomal delivery of the E1A gene. Cancer Res 62: 6712-6716.
40. Ueno NT, Yu D, Hung MC. (1997). Chemosensitization of HER-2/ neu-overexpressing human breast cancer cells to paclitaxel (Taxol) by adenovirus type 5 E1A. Oncogene 15: 953-960.
41. Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G et al. (2005). Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci USA 102: 673-678.
42. Uren RT, Dewson G, Bonzon C, Lithgow T, Newmeyer DD, Kluck RM. (2005). Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J Biol Chem 280: 2266-2274.
43. Villaret D, Glisson B, Kenady D, Hanna E, Carey M, Gleich L et al. (2002). A multicenter phase II study of tgDCC-E1A for the intratumoral treatment of patients with recurrent head and neck squamous cell carcinoma. Head Neck 24: 661-669. (Pubitemid 34734362)
44. Wang YN, Chen YJ, Chang WC. (2006). Activation of extracellular signal-regulated kinase signaling by epidermal growth factor mediates c-Jun activation and p300 recruitment in keratin 16 gene expression. Mol Pharmacol 69: 85-98.
45. Xie X, Hsu JL, Choi MG, Xia W, Yamaguchi H, Chen CT et al. (2009). A novel hTERT promoter-driven E1A therapeutic for ovarian cancer. Mol Cancer Ther 8: 2375-2382.
46. Xie X, Xia W, Li Z, Kuo HP, Liu Y, Li Z et al. (2007). Targeted expression of BikDD eradicates pancreatic tumors in noninvasive imaging models. Cancer Cell 12: 52-65.
47. Xing X, Liu V, Xia W, Stephens LC, Huang L, Lopez-Berestein G et al. (1997). Safety studies of the intraperitoneal injection of E1A-liposome complex in mice. Gene Ther 4: 238-243.
48. Xing X, Zhang S, Chang JY, Tucker SD, Chen H, Huang L et al. (1998). Safety study and characterization of E1A-liposome complex gene-delivery protocol in an ovarian cancer model. Gene Ther 5: 1538-1544.
49. Xu W, Ngo L, Perez G, Dokmanovic M, Marks PA. (2006). Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc Natl Acad Sci USA 103: 15540-15545.
50. Yamaguchi H, Bhalla K, Wang HG. (2003). Bax plays a pivotal role in thapsigargin-induced apoptosis of human colon cancer HCT116 cells by controlling Smac/Diablo and Omi/HtrA2 release from mitochondria. Cancer Res 63: 1483-1489.
51. Yan DH, Chang LS, Hung MC. (1991). Repressed expression of the HER-2/c-erbB-2 proto-oncogene by the adenovirus E1a gene products. Oncogene 6: 343-345.
52. Yang XJ, Seto E. (2008). The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9: 206-218.
53. Yoo GH, Hung MC, Lopez-Berestein G, LaFollette S, Ensley JF, Carey M et al. (2001). Phase I trial of intratumoral liposome E1A gene therapy in patients with recurrent breast and head and neck cancer. Clin Cancer Res 7: 1237-1245.
54. Youle RJ, Strasser A. (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
55. Yu D, Matin A, Xia W, Sorgi F, Huang L, Hung MC. (1995). Liposome-mediated in vivo E1A gene transfer suppressed dissemination of ovarian cancer cells that overexpress HER-2/neu. Oncogene 11: 1383-1388.
56. Yu D, Wolf JK, Scanlon M, Price JE, Hung MC. (1993). Enhanced c-erbB-2/neu expression in human ovarian cancer cells correlates with more severe malignancy that can be suppressed by E1A. Cancer Res 53: 891-898.
57. Yu DH, Scorsone K, Hung MC. (1991). Adenovirus type 5 E1A gene products act as transformation suppressors of the neu oncogene. Mol Cell Biol 11: 1745-1750.
58. Zhang F, Lin M, Abidi P, Thiel G, Liu J. (2003). Specific interaction of Egr1 and c/EBPbeta leads to the transcriptional activation of the human low density lipoprotein receptor gene. J Biol Chem 278: 44246-44254.