A novel apoptotic mechanism of genetically engineered adenovirus-mediated tumour-specific p53 overexpression through E1A-dependent p21 and MDM2 suppression

European Journal of Cancer

Volumn 48, Issue 14, 2012, Pages 2282-2291

  Yamasaki, Yasumoto ^a   Tazawa, Hiroshi ^a,b   Hashimoto, Yuuri ^a   Kojima, Toru ^a   Kuroda, Shinji ^a   Yano, Shuya ^a   Yoshida, Ryosuke ^a   Uno, Futoshi ^a   Mizuguchi, Hiroyuki ^c   Ohtsuru, Akira ^d   Urata, Yasuo ^e   Kagawa, Shunsuke ^a   Fujiwara, Toshiyoshi ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY HOSPITAL   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d NAGASAKI UNIVERSITY HOSPITAL   (Japan)

^e National Institute of Infectious Diseases   (Japan)

Author keywords

Apoptosis; Oncolytic adenovirus; P21; P53; Telomerase

Indexed keywords

CASPASE 3; OBP 301; OBP 702; ONCOLYTIC ADENOVIRUS; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; UNCLASSIFIED DRUG;

ADENOVIRUS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; GENETIC ENGINEERING; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN TUMOR; UPREGULATION;

ADENOVIRIDAE; ADENOVIRUS E1A PROTEINS; ADENOVIRUS E1B PROTEINS; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; GENETIC VECTORS; HUMANS; MICE; MICE, NUDE; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MDM2; TELOMERASE; TIME FACTORS; TRANSDUCTION, GENETIC; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84865474540     PISSN: 09598049     EISSN: 18790852     Source Type: Journal    
DOI: 10.1016/j.ejca.2011.12.020     Document Type: Article

References (49)

1. D. Kirn, R.L. Martuza, and J. Zwiebel Replication-selective virotherapy for cancer: biological principles, risk management and future directions Nat Med 7 7 2001 781 787
2. L.K. Hawkins, N.R. Lemoine, and D. Kirn Oncolytic biotherapy: a novel therapeutic platform Lancet Oncol 3 1 2002 17 26
3. E.A. Chiocca Oncolytic viruses Nat Rev Cancer 2 12 2002 938 950
4. M.J. Vaha-Koskela, J.E. Heikkila, and A.E. Hinkkanen Oncolytic viruses in cancer therapy Cancer Lett 254 2 2007 178 216
5. M. Aghi, and R.L. Martuza Oncolytic viral therapies - the clinical experience Oncogene 24 52 2005 7802 7816
6. T.C. Liu, E. Galanis, and D. Kirn Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress Nat Clin Pract Oncol 4 2 2007 101 117
7. S. Pesonen, L. Kangasniemi, and A. Hemminki Oncolytic adenoviruses for the treatment of human cancer: focus on translational and clinical data Mol Pharm 8 1 2011 12 28
8. R.M. Eager, and J. Nemunaitis Clinical development directions in oncolytic viral therapy Cancer Gene Ther 18 5 2011 305 317
9. T. Kawashima, S. Kagawa, and N. Kobayashi Telomerase-specific replication-selective virotherapy for human cancer Clin Cancer Res 10 1 Pt. 1 2004 285 292
10. T. Fujiwara, Y. Urata, and N. Tanaka Telomerase-specific oncolytic virotherapy for human cancer with the hTERT promoter Curr Cancer Drug Targets 7 2 2007 191 201
11. Y. Hashimoto, Y. Watanabe, and Y. Shirakiya Establishment of biological and pharmacokinetic assays of telomerase-specific replication-selective adenovirus Cancer Sci 99 2 2008 385 390
12. J. Nemunaitis, A.W. Tong, and M. Nemunaitis A phase I study of telomerase-specific replication competent oncolytic adenovirus (Telomelysin) for various solid tumors Mol Ther 18 2 2010 429 434
13. J.J. Cody, and J.T. Douglas Armed replicating adenoviruses for cancer virotherapy Cancer Gene Ther 16 6 2009 473 488
14. K.H. Vousden, and C. Prives Blinded by the light: the growing complexity of p53 Cell 137 3 2009 413 431
15. M.V. Blagosklonny, and W.S. el-Deiry In vitro evaluation of a p53-expressing adenovirus as an anti-cancer drug Int J Cancer 67 3 1996 386 392
16. Y. Zeng, N. Prabhu, R. Meng, and W. Eldeiry Adenovirus-mediated p53 gene therapy in nasopharyngeal cancer Int J Oncol 11 2 1997 221 226
17. G.L. Clayman, A.K. el-Naggar, and S.M. Lippman Adenovirus-mediated p53 gene transfer in patients with advanced recurrent head and neck squamous cell carcinoma J Clin Oncol 16 6 1998 2221 2232
18. S.G. Swisher, J.A. Roth, and J. Nemunaitis Adenovirus-mediated p53 gene transfer in advanced non-small-cell lung cancer J Natl Cancer Inst 91 9 1999 763 771
19. H. Shimada, H. Matsubara, and T. Shiratori Phase I/II adenoviral p53 gene therapy for chemoradiation resistant advanced esophageal squamous cell carcinoma Cancer Sci 97 6 2006 554 561
20. T. Fujiwara, N. Tanaka, and S. Kanazawa Multicenter phase I study of repeated intratumoral delivery of adenoviral p53 in patients with advanced non-small-cell lung cancer J Clin Oncol 24 11 2006 1689 1699
21. V.W. van Beusechem, P.B. van den Doel, J. Grill, H.M. Pinedo, and W.R. Gerritsen Conditionally replicative adenovirus expressing p53 exhibits enhanced oncolytic potency Cancer Res 62 21 2002 6165 6171
22. H.C. Zhao, Q. Zhang, and Y. Yang P53-expressing conditionally replicative adenovirus CNHK500-p53 against hepatocellular carcinoma in vitro World J Gastroenterol 13 5 2007 683 691
23. X. Wang, C. Su, and H. Cao A novel triple-regulated oncolytic adenovirus carrying p53 gene exerts potent antitumor efficacy on common human solid cancers Mol Cancer Ther 7 6 2008 1598 1603
24. R. Sakai, S. Kagawa, and Y. Yamasaki Preclinical evaluation of differentially targeting dual virotherapy for human solid cancer Mol Cancer Ther 9 6 2010 1884 1893
25. M. Gorospe, C. Cirielli, and X. Wang P21(Waf1/Cip1) protects against p53-mediated apoptosis of human melanoma cells Oncogene 14 8 1997 929 935
26. T. Itoshima, T. Fujiwara, and T. Waku Induction of apoptosis in human esophageal cancer cells by sequential transfer of the wild-type p53 and E2F-1 genes: involvement of p53 accumulation via ARF-mediated MDM2 down-regulation Clin Cancer Res 6 7 2000 2851 2859
27. S. Bagchi, P. Raychaudhuri, and J.R. Nevins Adenovirus E1A proteins can dissociate heteromeric complexes involving the E2F transcription factor: a novel mechanism for E1A trans-activation Cell 62 4 1990 659 669
28. W.T. Steegenga, T. van Laar, and N. Riteco Adenovirus E1A proteins inhibit activation of transcription by p53 Mol Cell Biol 16 5 1996 2101 2109
29. K. Somasundaram, and W.S. El-Deiry Inhibition of p53-mediated transactivation and cell cycle arrest by E1A through its p300/CBP-interacting region Oncogene 14 9 1997 1047 1057
30. D. Chattopadhyay, M.K. Ghosh, A. Mal, and M.L. Harter Inactivation of p21 by E1A leads to the induction of apoptosis in DNA-damaged cells J Virol 75 20 2001 9844 9856
31. A. Thomas, and E. White Suppression of the p300-dependent mdm2 negative-feedback loop induces the p53 apoptotic function Genes Dev 12 13 1998 1975 1985
32. M. Idogawa, Y. Sasaki, and H. Suzuki A single recombinant adenovirus expressing p53 and p21-targeting artificial microRNAs efficiently induces apoptosis in human cancer cells Clin Cancer Res 15 11 2009 3725 3732
33. G.A. Horwitz, K. Zhang, and M.A. McBrian Adenovirus small e1a alters global patterns of histone modification Science 321 5892 2008 1084 1085
34. R. Ferrari, M. Pellegrini, and G.A. Horwitz Epigenetic reprogramming by adenovirus e1a Science 321 5892 2008 1086 1088
35. I. Savelyeva, and M. Dobbelstein Infection with E1B-mutant adenovirus stabilizes p53 but blocks p53 acetylation and activity through E1A Oncogene 30 7 2011 865 875
36. N.G. Iyer, S.F. Chin, and H. Ozdag P300 regulates p53-dependent apoptosis after DNA damage in colorectal cancer cells by modulation of PUMA/p21 levels Proc Natl Acad Sci USA 101 19 2004 7386 7391
37. M. Shiina, M.D. Lacher, C. Christian, and W.M. Korn RNA interference-mediated knockdown of p21(WAF1) enhances anti-tumor cell activity of oncolytic adenoviruses Cancer Gene Ther 16 11 2009 810 819
38. N. Hoti, W.H. Chowdhury, and S. Mustafa Armoring CRAds with p21/Waf-1 shRNAs: the next generation of oncolytic adenoviruses Cancer Gene Ther 17 8 2010 585 597
39. H. Ito, H. Aoki, and F. Kuhnel Autophagic cell death of malignant glioma cells induced by a conditionally replicating adenovirus J Natl Cancer Inst 98 9 2006 625 636
40. H. Jiang, C. Gomez-Manzano, and H. Aoki Examination of the therapeutic potential of Delta-24-RGD in brain tumor stem cells: role of autophagic cell death J Natl Cancer Inst 99 18 2007 1410 1414
41. K. Fujiwara, S. Daido, and A. Yamamoto Pivotal role of the cyclin-dependent kinase inhibitor p21WAF1/CIP1 in apoptosis and autophagy J Biol Chem 283 1 2008 388 397
42. M. Kusumoto, T. Ogawa, and K. Mizumoto Adenovirus-mediated p53 gene transduction inhibits telomerase activity independent of its effects on cell cycle arrest and apoptosis in human pancreatic cancer cells Clin Cancer Res 5 8 1999 2140 2147
43. T. Kanaya, S. Kyo, and K. Hamada Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription Clin Cancer Res 6 4 2000 1239 1247
44. I. Shats, M. Milyavsky, and X. Tang P53-dependent down-regulation of telomerase is mediated by p21waf1 J Biol Chem 279 49 2004 50976 50985
45. T. Sasaki, H. Tazawa, and J. Hasei Preclinical evaluation of telomerase-specific oncolytic virotherapy for human bone and soft tissue sarcomas Clin Cancer Res 17 7 2011 1828 1838
46. T. Fujiwara, E.A. Grimm, and T. Mukhopadhyay Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene Cancer Res 54 9 1994 2287 2291
47. N. Ogawa, T. Fujiwara, and S. Kagawa Novel combination therapy for human colon cancer with adenovirus-mediated wild-type p53 gene transfer and DNA-damaging chemotherapeutic agent Int J Cancer 73 3 1997 367 370
48. J.L. Cook, B.A. Routes, T.A. Walker, K.L. Colvin, and J.M. Routes E1A oncogene induction of cellular susceptibility to killing by cytolytic lymphocytes through target cell sensitization to apoptotic injury Exp Cell Res 251 2 1999 414 423
49. J.L. Cook, T.A. Miura, D.N. Ikle, A.M. Lewis Jr., and J.M. Routes E1A oncogene-induced sensitization of human tumor cells to innate immune defenses and chemotherapy-induced apoptosis in vitro and in vivo Cancer Res 63 12 2003 3435 3443