Synergistic interaction of telomerase-specific oncolytic virotherapy and chemotherapeutic agents for human cancer

Current Pharmaceutical Biotechnology

Volumn 13, Issue 9, 2012, Pages 1809-1816

  Fujiwara, Toshiyoshi ^a   Kagawa, Shunsuke ^a   Tazawa, Hiroshi ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY HOSPITAL   (Japan)

Author keywords

Adenovirus; Docetaxel; Gemcitabine; Histon deacetylase inhibitor; Telomerase; Virotherapy

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; DOCETAXEL; FLUOROURACIL; FS 901228; GEMCITABINE; LONTUCIREV; OBP 301; OBP 401; ONCOLYTIC ADENOVIRUS; ONCOLYTIC VIRUS; ROMIDEPSIN; TELOMELYSIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADENOVIRUS 5; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; DRUG POTENTIATION; ENZYME ACTIVITY; HUMAN; NEOPLASM; NONHUMAN; ONCOLYTIC VIROTHERAPY; TELOMERE; TUMOR CELL DESTRUCTION; VIRUS ATTENUATION; VIRUS EXPRESSION; VIRUS GENE; VIRUS REPLICATION;

ANIMALS; ANTINEOPLASTIC AGENTS; COMBINED MODALITY THERAPY; DRUG SYNERGISM; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; TELOMERASE;

ADENOVIRIDAE; ANIMALIA; HUMAN ADENOVIRUS TYPE 5;

EID: 84863542042     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112800958887     Document Type: Article

References (77)

1. Fujiwara, T.; Cai, D.W.; Georges, R.N.; Mukhopadhyay, T.; Grimm, E.A.; Roth, J.A. Therapeutic effect of a retroviral wildtype p53 expression vector in an orthotopic lung cancer model. J. Natl. Cancer Inst., 1994, 86 (19), 1458-1462.
2. Fujiwara, T.; Grimm, E.A.; Mukhopadhyay, T.; Zhang, W.W.; Owen-Schaub, L.B.; Roth, J.A. Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res., 1994, 54 (9), 2287-2291.
3. Kagawa, S.; Gu, J.; Swisher, S.G.; Ji, L.; Roth, J.A.; Lai, D.; Stephens, L.C.; Fang, B. Antitumor effect of adenovirus-mediated Bax gene transfer on p53-sensitive and p53-resistant cancer lines. Cancer Res., 2000, 60 (5), 1157-1161.
4. Tsunemitsu, Y.; Kagawa, S.; Tokunaga, N.; Otani, S.; Umeoka, T.; Roth, J.A.; Fang, B.; Tanaka, N.; Fujiwara, T. Molecular therapy for peritoneal dissemination of xenotransplanted human MKN-45 gastric cancer cells with adenovirus mediated Bax gene transfer. Gut, 2004, 53 (4), 554-560.
5. Chen, S.H.; Shine, H.D.; Goodman, J.C.; Grossman, R.G.; Woo, S.L. Gene therapy for brain tumors: regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc. Natl. Acad. Sci. USA, 1994, 91 (8), 3054-3057.
6. Sterman, D.H.; Treat, J.; Litzky, L.A.; Amin, K.M.; Coonrod, L.; Molnar-Kimber, K.; Recio, A.; Knox, L.; Wilson, J.M.; Albelda, S.M.; Kaiser, L.R. Adenovirus-mediated herpes simplex virus thymidine kinase/ganciclovir gene therapy in patients with localized malignancy: results of a phase I clinical trial in malignant mesothelioma. Hum. Gene. Ther., 1998, 9 (7), 1083-1092.
7. Feldman, A.L.; Restifo, N.P.; Alexander, H.R.; Bartlett, D.L.; Hwu, P.; Seth, P.; Libutti, S.K. Antiangiogenic gene therapy of cancer utilizing a recombinant adenovirus to elevate systemic endostatin levels in mice. Cancer Res., 2000, 60 (6), 1503-1506.
8. Clayman, G.L.; el-Naggar, A.K.; Lippman, S.M.; Henderson, Y.C.; Frederick, M.; Merritt, J.A.; Zumstein, L.A.; Timmons, T.M.; Liu, T.J.; Ginsberg, L.; Roth, J.A.; Hong, W.K.; Bruso, P.; Goepfert, H. Adenovirus-mediated p53 gene transfer in patients with advanced recurrent head and neck squamous cell carcinoma. J. Clin. Oncol., 1998, 16 (6), 2221-2232.
9. Swisher, S.G.; Roth, J.A.; Nemunaitis, J.; Lawrence, D.D.; Kemp, B.L.; Carrasco, C.H.; Connors, D.G.; El-Naggar, A.K.; Fossella, F.; Glisson, B.S.; Hong, W.K.; Khuri, F.R.; Kurie, J.M.; Lee, J.J.; Lee, J.S.; Mack, M.; Merritt, J.A.; Nguyen, D.M.; Nesbitt, J.C.; Perez-Soler, R.; Pisters, K.M.; Putnam, J.B., Jr.; Richli, W.R.; Savin, M.; Schrump, D.S.; Shin, D.M.; Shulkin, A.; Walsh, G.L.; Wait, J.; Weill, D.; Waugh, M.K. Adenovirus-mediated p53 gene transfer in advanced non-small-cell lung cancer. J. Natl. Cancer Inst., 1999, 91 (9), 763-771.
10. Nemunaitis, J.; Swisher, S.G.; Timmons, T.; Connors, D.; Mack, M.; Doerksen, L.; Weill, D.; Wait, J.; Lawrence, D.D.; Kemp, B.L.; Fossella, F.; Glisson, B.S.; Hong, W.K.; Khuri, F.R.; Kurie, J.M.; Lee, J.J.; Lee, J.S.; Nguyen, D.M.; Nesbitt, J.C.; Perez-Soler, R.; Pisters, K.M.; Putnam, J.B.; Richli, W.R.; Shin, D.M.; Walsh, G.L.; Merritt, J.; Roth, J. Adenovirus-mediated p53 gene transfer in sequence with cisplatin to tumors of patients with non-small-cell lung cancer. J. Clin. Oncol., 2000, 18 (3), 609-622.
11. Swisher, S.G.; Roth, J.A.; Komaki, R.; Gu, J.; Lee, J.J.; Hicks, M.; Ro, J.Y.; Hong, W.K.; Merritt, J.A.; Ahrar, K.; Atkinson, N.E.; Correa, A.M.; Dolormente, M.; Dreiling, L.; El-Naggar, A.K.; Fossella, F.; Francisco, R.; Glisson, B.; Grammer, S.; Herbst, R.; Huaringa, A.; Kemp, B.; Khuri, F.R.; Kurie, J.M.; Liao, Z.; McDonnell, T.J.; Morice, R.; Morello, F.; Munden, R.; Papadimitrakopoulou, V.; Pisters, K.M.; Putnam, J.B., Jr.; Sarabia, A.J.; Shelton, T.; Stevens, C.; Shin, D.M.; Smythe, W.R.; Vaporciyan, A.A.; Walsh, G.L.; Yin, M. Induction of p53-regulated genes and tumor regression in lung cancer patients after intratumoral delivery of adenoviral p53 (INGN 201) and radiation therapy. Clin. Cancer Res., 2003, 9 (1), 93-101.
12. Fujiwara, T.; Tanaka, N.; Kanazawa, S.; Ohtani, S.; Saijo, Y.; Nukiwa, T.; Yoshimura, K.; Sato, T.; Eto, Y.; Chada, S.; Nakamura, H.; Kato, H. Multicenter phase I study of repeated intratumoral delivery of adenoviral p53 in patients with advanced nonsmall-cell lung cancer. J. Clin. Oncol., 2006, 24 (11), 1689-1699.
13. Hawkins, L.K.; Lemoine, N.R.; Kirn, D. Oncolytic biotherapy: a novel therapeutic plafform. Lancet Oncol., 2002, 3 (1), 17-26.
14. Kawashima, T.; Kagawa, S.; Kobayashi, N.; Shirakiya, Y.; Umeoka, T.; Teraishi, F.; Taki, M.; Kyo, S.; Tanaka, N.; Fujiwara, T. Telomerase-specific replication-selective virotherapy for human cancer. Clin. Cancer Res., 2004, 10 (1 Pt 1), 285-292.
15. Umeoka, T.; Kawashima, T.; Kagawa, S.; Teraishi, F.; Taki, M.; Nishizaki, M.; Kyo, S.; Nagai, K.; Urata, Y.; Tanaka, N.; Fujiwara, T. Visualization of intrathoracically disseminated solid tumors in mice with optical imaging by telomerase-specific amplification of a transferred green fluorescent protein gene. Cancer Res., 2004, 64 (17), 6259-6265.
16. Taki, M.; Kagawa, S.; Nishizaki, M.; Mizuguchi, H.; Hayakawa, T.; Kyo, S.; Nagai, K.; Urata, Y.; Tanaka, N.; Fujiwara, T. Enhanced oncolysis by a tropism-modified telomerase-specific replication-selective adenoviral agent OBP-405 ('Telomelysin-RGD'). Oncogene, 2005, 24 (19), 3130-3140.
17. Shay, J.W.; Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer, 1997, 33 (5), 787-791.
18. Dong, C.K.; Masutomi, K.; Hahn, W.C. Telomerase: regulation, function and transformation. Crit Rev. Oncol. Hematol., 2005, 54 (2), 85-93.
19. Hiyama, K.; Hirai, Y.; Kyoizumi, S.; Akiyama, M.; Hiyama, E.; Piatyszek, M.A.; Shay, J.W.; Ishioka, S.; Yamakido, M. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J. Immunol., 1995, 155 (8), 3711-3715.
20. Tahara, H.; Yasui, W.; Tahara, E.; Fujimoto, J.; Ito, K.; Tamai, K.; Nakayama, J.; Ishikawa, F.; Tahara, E.; Ide, T. Immunohistochemical detection of human telomerase catalytic component, hTERT, in human colorectal tumor and non-tumor tissue sections. Oncogene, 1999, 18 (8), 1561-1567.
21. Shay, J.W.; Wright, W.E. Telomerase: a target for cancer therapeutics. Cancer Cell, 2002, 2 (4), 257-265.
22. Feng, J.; Funk, W.D.; Wang, S.S.; Weinrich, S.L.; Avilion, A.A.; Chiu, C.P.; Adams, R.R.; Chang, E.; Allsopp, R.C.; Yu, J.;. The RNA component of human telomerase. Science, 1995, 269 (5228), 1236-1241.
23. Harrington, L.; McPhail, T.; Mar, V.; Zhou, W.; Oulton, R.; Bass, M.B.; Arruda, I.; Robinson, M.O. A mammalian telomeraseassociated protein. Science, 1997, 275 (5302), 973-977.
24. Meyerson, M.; Counter, C.M.; Eaton, E.N.; Ellisen, L.W.; Steiner, P.; Caddle, S.D.; Ziaugra, L.; Beijersbergen, R.L.; Davidoff, M.J.; Liu, Q.; Bacchetti, S.; Haber, D.A.; Weinberg, R.A. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell, 1997, 90 (4), 785-795.
25. Nakamura, T.M.; Morin, G.B.; Chapman, K.B.; Weinrich, S.L.; Andrews, W.H.; Lingner, J.; Harley, C.B.; Cech, T.R. Telomerase catalytic subunit homologs from fission yeast and human. Science, 1997, 277 (5328), 955-959.
26. Nakayama, J.; Tahara, H.; Tahara, E.; Saito, M.; Ito, K.; Nakamura, H.; Nakanishi, T.; Tahara, E.; Ide, T.; Ishikawa, F. Telomerase activation by hTRT in human normal fibroblasts and hepatocellular carcinomas. Nat. Genet., 1998, 18 (1), 65-68.
27. Beattie, T.L.; Zhou, W.; Robinson, M.O.; Harrington, L. Reconstitution of human telomerase activity in vitro. Curr. Biol., 1998, 8 (3), 177-180.
28. Wirth, T.; Zender, L.; Schulte, B.; Mundt, B.; Plentz, R.; Rudolph, K.L.; Manns, M.; Kubicka, S.; Kuhnel, F. A telomerase-dependent conditionally replicating adenovirus for selective treatment of cancer. Cancer Res., 2003, 63 (12), 3181-3188.
29. Lanson, N.A., Jr.; Friedlander, P.L.; Schwarzenberger, P.; Kolls, J.K.; Wang, G. Replication of an adenoviral vector controlled by the human telomerase reverse transcriptase promoter causes tumorselective tumor lysis. Cancer Res., 2003, 63 (22), 7936-7941.
30. Irving, J.; Wang, Z.; Powell, S.; O'Sullivan, C.; Mok, M.; Murphy, B.; Cardoza, L.; Lebkowski, J.S.; Majumdar, A.S. Conditionally replicative adenovirus driven by the human telomerase promoter provides broad-spectrum antitumor activity without liver toxicity. Cancer Gene Ther., 2004, 11 (3), 174-185.
31. Kim, E.; Kim, J.H.; Shin, H.Y.; Lee, H.; Yang, J.M.; Kim, J.; Sohn, J.H.; Kim, H.; Yun, C.O. Ad-mTERT-delta19, a conditional replication-competent adenovirus driven by the human telomerase promoter, selectively replicates in and elicits cytopathic effect in a cancer cellspecific manner. Hum. Gene Ther., 2003, 14 (15), 1415-1428.
32. Li, Y.; Yu, D.C.; Chen, Y.; Amin, P.; Zhang, H.; Nguyen, N.; Henderson, D.R. A hepatocellular carcinoma-specific adenovirus variant, CV890, eliminates distant human liver tumors in combination with doxorubicin. Cancer Res., 2001, 61 (17), 6428-6436.
33. Hashimoto, Y.; Watanabe, Y.; Shirakiya, Y.; Uno, F.; Kagawa, S.; Kawamura, H.; Nagai, K.; Tanaka, N.; Kumon, H.; Urata, Y.; Fujiwara, T. Establishment of biological and pharmacokinetic assays of telomerase-specific replication-selective adenovirus. Cancer Sci., 2008, 99 (2), 385-390.
34. Fujiwara, T.; Urata, Y.; Tanaka, N. Telomerase-specific oncolytic virotherapy for human cancer with the hTERT promoter. Curr. Cancer Drug Targets, 2007, 7 (2), 191-201.
35. Kurihara, Y.; Watanabe, Y.; Onimatsu, H.; Kojima, T.; Shirota, T.; Hatori, M.; Liu, D.; Kyo, S.; Mizuguchi, H.; Urata, Y.; Shintani, S.; Fujiwara, T. Telomerase-specific virotheranostics for human head and neck cancer. Clin. Cancer Res., 2009, 15 (7), 2335-2343.
36. Fujiwara, T. Telomerase-specific virotherapy for human squamous cell carcinoma. Expert. Opin. Biol. Ther., 2009, 9 (3), 321-329.
37. Nemunaitis, J.; Tong, A.W.; Nemunaitis, M.; Senzer, N.; Phadke, A.P.; Bedell, C.; Adams, N.; Zhang, Y.A.; Maples, P.B.; Chen, S.; Pappen, B.; Burke, J.; Ichimaru, D.; Urata, Y.; Fujiwara, T. A phase I study of telomerase-specific replication competent oncolytic adenovirus (telomelysin) for various solid tumors. Mol. Ther., 2010, 18 (2), 429-434.
38. DeWeese, T.L.; van der, P.H.; Li, S.; Mikhak, B.; Drew, R.; Goemann, M.; Hamper, U.; DeJong, R.; Detorie, N.; Rodriguez, R.; Haulk, T.; DeMarzo, A.M.; Piantadosi, S.; Yu, D.C.; Chen, Y.; Henderson, D.R.; Carducci, M.A.; Nelson, W.G.; Simons, J.W. A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res., 2001, 61 (20), 7464-7472.
39. Small, E.J.; Carducci, M.A.; Burke, J.M.; Rodriguez, R.; Fong, L.; van, U.L.; Yu, D.C.; Aimi, J.; Ando, D.; Working, P.; Kirn, D.; Wilding, G. A Phase I Trial of Intravenous CG7870, a Replicationselective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol. Ther., 2006.
40. Bischoff, J.R.; Kirn, D.H.; Williams, A.; Heise, C.; Horn, S.; Muna, M.; Ng, L.; Nye, J.A.; Sampson-Johannes, A.; Fattaey, A.; McCormick, F. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science, 1996, 274 (5286), 373-376.
41. Rodriguez, R.; Schuur, E.R.; Lim, H.Y.; Henderson, G.A.; Simons, J.W.; Henderson, D.R. Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostatespecific antigen-positive prostate cancer cells. Cancer Res., 1997, 57 (13), 2559-2563.
42. Kirn, D.; Martuza, R.L.; Zwiebel, J. Replication-selective virotherapy for cancer: Biological principles, risk management and future directions. Nat. Med., 2001, 7 (7), 781-787.
43. Heise, C.; Sampson-Johannes, A.; Williams, A.; McCormick, F.; Von Hoff, D.D.; Kirn, D.H. ONYX-015, an E1B gene-attenuated adenovirus, causes tumor-specific cytolysis and antitumoral efficacy that can be augmented by standard chemotherapeutic agents. Nat. Med., 1997, 3 (6), 639-645.
44. You, L.; Yang, C.T.; Jablons, D.M. ONYX-015 works synergistically with chemotherapy in lung cancer cell lines and primary cultures freshly made from lung cancer patients. Cancer Res., 2000, 60 (4), 1009-1013.
45. Toyoizumi, T.; Mick, R.; Abbas, A.E.; Kang, E.H.; Kaiser, L.R.; Molnar-Kimber, K.L. Combined therapy with chemotherapeutic agents and herpes simplex virus type 1 ICP34.5 mutant (HSV-1716) in human non-small cell lung cancer. Hum. Gene Ther., 1999, 10 (18), 3013-3029.
46. Khuri, F.R.; Nemunaitis, J.; Ganly, I.; Arseneau, J.; Tannock, I.F.; Romel, L.; Gore, M.; Ironside, J.; MacDougall, R.H.; Heise, C.; Randlev, B.; Gillenwater, A.M.; Bruso, P.; Kaye, S.B.; Hong, W.K.; Kirn, D.H. a controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat. Med., 2000, 6 (8), 879-885.
47. Reid, T.; Galanis, E.; Abbruzzese, J.; Sze, D.; Wein, L.M.; Andrews, J.; Randlev, B.; Heise, C.; Uprichard, M.; Hatfield, M.; Rome, L.; Rubin, J.; Kirn, D. Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): phase II viral, immunologic, and clinical endpoints. Cancer Res., 2002, 62 (21), 6070-6079.
48. Hecht, J.R.; Bedford, R.; Abbruzzese, J.L.; Lahoti, S.; Reid, T.R.; Soetikno, R.M.; Kirn, D.H.; Freeman, S.M. A phase I/II trial of intratumoral endoscopic ultrasound injection of ONYX-015 with intravenous gemcitabine in unresectable pancreatic carcinoma. Clin. Cancer Res., 2003, 9 (2), 555-561.
49. Galanis, E.; Okuno, S.H.; Nascimento, A.G.; Lewis, B.D.; Lee, R.A.; Oliveira, A.M.; Sloan, J.A.; Atherton, P.; Edmonson, J.H.; Erlichman, C.; Randlev, B.; Wang, Q.; Freeman, S.; Rubin, J. Phase I-II trial of ONYX-015 in combination with MAP chemotherapy in patients with advanced sarcomas. Gene Ther., 2005, 12 (5), 437-445.
50. Nemunaitis, J.; Ganly, I.; Khuri, F.; Arseneau, J.; Kuhn, J.; McCarty, T.; Landers, S.; Maples, P.; Romel, L.; Randlev, B.; Reid, T.; Kaye, S.; Kirn, D. Selective replication and oncolysis in p53 mutant tumors with ONYX-015, an E1B-55kD gene-deleted adenovirus, in patients with advanced head and neck cancer: a phase II trial. Cancer Res., 2000, 60 (22), 6359-6366.
51. Jacobs, C.; Lyman, G.; Velez-Garcia, E.; Sridhar, K.S.; Knight, W.; Hochster, H.; Goodnough, L.T.; Mortimer, J.E.; Einhorn, L.H.; Schacter, L. A phase III randomized study comparing cisplatin and fluorouracil as single agents and in combination for advanced squamous cell carcinoma of the head and neck. J. Clin. Oncol., 1992, 10 (2), 257-263.
52. Vokes, E.E. Chemotherapy and integrated treatment approaches in head and neck cancer. Curr. Opin. Oncol., 1991, 3 (3), 529-534.
53. Jordan, M.A.; Toso, R.J.; Thrower, D.; Wilson, L. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. USA, 1993, 90 (20), 9552-9556.
54. Dumontet, C.; Sikic, B.I. Mechanisms of action of and resistance to antitubulin agents: microtubule dynamics, drug transport, and cell death. J. Clin. Oncol., 1999, 17 (3), 1061-1070.
55. Nielsen, L.L.; Lipari, P.; Dell, J.; Gurnani, M.; Hajian, G. Adenovirus-mediated p53 gene therapy and paclitaxel have synergistic efficacy in models of human head and neck, ovarian, prostate, and breast cancer. Clin. Cancer Res., 1998, 4 (4), 835-846.
56. Yu, D.C.; Chen, Y.; Dilley, J.; Li, Y.; Embry, M.; Zhang, H.; Nguyen, N.; Amin, P.; Oh, J.; Henderson, D.R. Antitumor synergy of CV787, a prostate cancer-specific adenovirus, and paclitaxel and docetaxel. Cancer Res., 2001, 61 (2), 517-525.
57. Fujiwara, T.; Kagawa, S.; Kishimoto, H.; Endo, Y.; Hioki, M.; Ikeda, Y.; Sakai, R.; Urata, Y.; Tanaka, N.; Fujiwara, T. Enhanced antitumor efficacy of telomerase-selective oncolytic adenoviral agent OBP-401 with docetaxel: Preclinical evaluation of chemovirotherapy. Int. J. Cancer, 2006, 119 (2), 432-440.
58. Shaked, Y.; Emmenegger, U.; Francia, G.; Chen, L.; Lee, C.R.; Man, S.; Paraghamian, A.; Ben-David, Y.; Kerbel, R.S. Low-dose metronomic combined with intermittent bolus-dose cyclophosphamide is an effective long-term chemotherapy treatment strategy. Cancer Res., 2005, 65 (16), 7045-7051.
59. Kitazono, M.; Goldsmith, M.E.; Aikou, T.; Bates, S.; Fojo, T. Enhanced adenovirus transgene expression in malignant cells treated with the histone deacetylase inhibitor FR901228. Cancer Res., 2001, 61 (17), 6328-6330.
60. Goldsmith, M.E.; Kitazono, M.; Fok, P.; Aikou, T.; Bates, S.; Fojo, T. The histone deacetylase inhibitor FK228 preferentially enhances adenovirus transgene expression in malignant cells. Clin. Cancer Res., 2003, 9 (14), 5394-5401.
61. Pong, R.C.; Lai, Y.J.; Chen, H.; Okegawa, T.; Frenkel, E.; Sagalowsky, A.; Hsieh, J.T. Epigenetic regulation of coxsackie and adenovirus receptor (CAR) gene promoter in urogenital cancer cells. Cancer Res., 2003, 63 (24), 8680-8686.
62. Hemminki, A.; Kanerva, A.; Liu, B.; Wang, M.; Alvarez, R.D.; Siegal, G.P.; Curiel, D.T. Modulation of coxsackie-adenovirus receptor expression for increased adenoviral transgene expression. Cancer Res., 2003, 63 (4), 847-853.
63. Watanabe, T.; Hioki, M.; Fujiwara, T.; Nishizaki, M.; Kagawa, S.; Taki, M.; Kishimoto, H.; Endo, Y.; Urata, Y.; Tanaka, N.; Fujiwara, T. Histone deacetylase inhibitor FR901228 enhances the antitumor effect of telomerase-specific replication-selective adenoviral agent OBP-301 in human lung cancer cells. Exp. Cell Res., 2006, 312 (3), 256-265.
64. Marshall, J.L.; Rizvi, N.; Kauh, J.; Dahut, W.; Figuera, M.; Kang, M.H.; Figg, W.D.; Wainer, I.; Chaissang, C.; Li, M.Z.; Hawkins, M.J. A phase I trial of depsipeptide (FR901228) in patients with advanced cancer. J. Exp. Ther. Oncol., 2002, 2 (6), 325-332.
65. Byrd, J.C.; Marcucci, G.; Parthun, M.R.; Xiao, J.J.; Klisovic, R.B.; Moran, M.; Lin, T.S.; Liu, S.; Sklenar, A.R.; Davis, M.E.; Lucas, D.M.; Fischer, B.; Shank, R.; Tejaswi, S.L.; Binkley, P.; Wright, J.; Chan, K.K.; Grever, M.R. A phase 1 and pharmacodynamic study of depsipeptide (FK228) in chronic lymphocytic leukemia and acute myeloid leukemia. Blood, 2005, 105 (3), 959-967.
66. Heinemann, V.; Quietzsch, D.; Gieseler, F.; Gonnermann, M.; Schonekas, H.; Rost, A.; Neuhaus, H.; Haag, C.; Clemens, M.; Heinrich, B.; Vehling-Kaiser, U.; Fuchs, M.; Fleckenstein, D.; Gesierich, W.; Uthgenannt, D.; Einsele, H.; Holstege, A.; Hinke, A.; Schalhorn, A.; Wilkowski, R. Randomized phase III trial of gemcitabine plus cisplatin compared with gemcitabine alone in advanced pancreatic cancer. J. Clin. Oncol., 2006, 24 (24), 3946-3952.
67. Paz-Ares, L.; Douillard, J.Y.; Koralewski, P.; Manegold, C.; Smit, E.F.; Reyes, J.M.; Chang, G.C.; John, W.J.; Peterson, P.M.; Obasaju, C.K.; Lahn, M.; Gandara, D.R. Phase III study of gemcitabine and cisplatin with or without aprinocarsen, a protein kinase C-alpha antisense oligonucleotide, in patients with advanced-stage nonsmall-cell lung cancer. J. Clin. Oncol., 2006, 24 (9), 1428-1434.
68. Halloran, C.M.; Ghaneh, P.; Shore, S.; Greenhalf, W.; Zumstein, L.; Wilson, D.; Neoptolemos, J.P.; Costello, E. 5-Fluorouracil or gemcitabine combined with adenoviral-mediated reintroduction of p16INK4A greatly enhanced cytotoxicity in Panc-1 pancreatic adenocarcinoma cells. J. Gene Med., 2004, 6 (5), 514-525.
69. Lee, W.P.; Tai, D.I.; Tsai, S.L.; Yeh, C.T.; Chao, Y.; Lee, S.D.; Hung, M.C. Adenovirus type 5 E1A sensitizes hepatocellular carcinoma cells to gemcitabine. Cancer Res., 2003, 63 (19), 6229-6236.
70. Liu, D.; Kojima, T.; Ouchi, M.; Kuroda, S.; Watanabe, Y.; Hashimoto, Y.; Onimatsu, H.; Urata, Y.; Fujiwara, T. Preclinical evaluation of synergistic effect of telomerase-specific oncolytic virotherapy and gemcitabine for human lung cancer. Mol. Cancer Ther., 2009, 8 (4): 980-987.
71. Huang, P.; Chubb, S.; Hertel, L.W.; Grindey, G.B.; Plunkett, W. Action of 2',2'-difluorodeoxycytidine on DNA synthesis. Cancer Res., 1991, 51 (22), 6110-6117.
72. Wang, H.G.; Draetta, G.; Moran, E. E1A induces phosphorylation of the retinoblastoma protein independently of direct physical association between the E1A and retinoblastoma products. Mol. Cell Biol., 1991, 11 (8), 4253-4265.
73. Hollyoake, M.; Stuhler, A.; Farrell, P.; Gordon, J.; Sinclair, A. The normal cell cycle activation program is exploited during the infection of quiescent B lymphocytes by Epstein-Barr virus. Cancer Res., 1995, 55 (21), 4784-4787.
74. Morozov, A.; Shiyanov, P.; Barr, E.; Leiden, J.M.; Raychaudhuri, P. Accumulation of human papillomavirus type 16 E7 protein bypasses G1 arrest induced by serum deprivation and by the cell cycle inhibitor p21. J. Virol., 1997, 71 (5), 3451-3457.
75. Nahle, Z.; Polakoff, J.; Davuluri, R.V.; McCurrach, M.E.; Jacobson, M.D.; Narita, M.; Zhang, M.Q.; Lazebnik, Y.; Bar-Sagi, D.; Lowe, S.W. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol., 2002, 4 (11), 859-864.
76. Kuroda, S.; Fujiwara, T.; Shirakawa, Y.; Yamasaki, Y.; Yano, S.; Uno, F.; Tazawa, H.; Hashimoto, Y.; Watanabe, Y.; Noma, K.; Urata, Y.; Kagawa, S.; Fujiwara, T. Telomerase-dependent oncolytic adenovirus sensitizes human cancer cells to ionizing radiation via inhibition of DNA repair machinery. Cancer Res., 2010, 70 (22): 9339-9348.
77. Kojima, T.; Watanabe, Y.; Hashimoto, Y.; Kuroda, S.; Yamasaki, Y.; Yano, S.; Ouchi, M.; Tazawa, H.; Uno, F.; Kagawa, S.; Kyo, S.; Mizuguchi, H.; Urata, Y.; Tanaka, N.; Fujiwara, T. In vivo biological purging for lymph node metastasis of human colorectal cancer by telomerase-specific oncolytic virotherapy. Ann. Surg., 2010, 251 (6),1079-1086.