Oncolytic adenoviruses expressing interleukin: A novel antitumour approach

Expert Opinion on Biological Therapy

Volumn 10, Issue 6, 2010, Pages 917-926

  Pei, Dong Sheng ^a   Zheng, Jun Nian ^a  

^a XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Antitumour; Gene therapy; Interleukin; Oncolytic adenoviruses

Indexed keywords

ANTINEOPLASTIC AGENT; CG 0070; CISPLATIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 24; KH 901; ONCOLYTIC ADENOVIRUS; ONYX 015; RECOMBINANT INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 18; RECOMBINANT INTERLEUKIN 2; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; BLADDER CARCINOMA; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER GENE THERAPY; CANCER SURVIVAL; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM TUMOR; CLINICAL TRIAL; COLORECTAL CANCER; DRUG CONJUGATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; DRUG SPECIFICITY; DRUG TARGETING; DRUG TOLERABILITY; FLU LIKE SYNDROME; HEAD AND NECK CANCER; HEMATOLOGIC DISEASE; HUMAN; INFLAMMATION; KIDNEY CANCER; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; METABOLIC DISORDER; NONHUMAN; PROSTATE CANCER; REVIEW; SARCOMA; SEPTIC SHOCK; SINGLE DRUG DOSE; SKIN CANCER; SOLID TUMOR; SURVIVAL TIME; TUMOR SUPPRESSOR GENE; UNSPECIFIED SIDE EFFECT; UTERINE CERVIX CANCER; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANIMALS; HUMANS; INTERLEUKINS; NEOPLASMS; ONCOLYTIC VIRUSES;

EID: 77952222258     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2010.481668     Document Type: Review

References (104)

1. Barker DD, Berk AJ. Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection. Virology 1987;156:107-121
2. Bischoff JR, Kirn DH, Williams A, et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996;274:373-376
3. Hallenbeck PL, Chang YN, Hay C, et al. A novel tumor-specific replication-restricted adenoviral vector for gene therapy of hepatocellular carcinoma. Hum Gene Ther 1999;10:1721-1733
4. Yu D, Sakamoto G, Henderson DR. Identification of the transcriptional regulatory sequences of human kallikrein 2 and their use in the construction of calydon virus 764, an attenuated replication competent adenovirus for prostate cancer therapy. Cancer Res 1999;59:1498-1504
5. Yu D, Chen Y, Seng M, et al. The additionof adenovirus region E3 enables calydon virus 787 to eliminatedistant prostate tumor xenografts. Cancer Res 1999;59:4200-4203
6. Ries SJ, Brandts CH, Chung AS, et al. Loss of p14ARF in tumor cells facilitates replication of the adenovirus mutant dl1520 (ONYX-015). Nat Med 2000;6:1128-1133
7. O'Shea CC, Johnson L, Bagus B, et al. Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell 2004;6:611-623
8. Fueyo J, Gomez MC, Alemany R, et al. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 2000;19:2-12
9. Piao Y, Jiang H, Alemany R, et al. Oncolytic adenovirus retargeted to Delta-EGFR induces selective antiglioma activity. Cancer Gene Ther 2009;16:256-265
10. Nemunaitis J, Ganly I, Khuri F, et al. 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;60:6359-6366
11. Ganly I, Kirn D, Eckhardt S, et al. A Phase I study of Onyx-015, an E1B attenuated adenovirus, administered intratumorally to patients with recurrent head and neck cancer. Clin Cancer Res 2000;6:798-806
12. Reid TR, Freeman S, Post L, et al. Effects of Onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5-FU/leucovorin. Cancer Gene Ther 2005;12:673-681
13. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006;24:657-679
14. Gaffen SL, Liu KD. Overview of interleukin-2 function, production and clinical applications. Cytokine 2004;28(3):109-123
15. Fehérvari Z, Yamaguchi T, Sakaguchi S. The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol 2006;27(3):109-111
16. Antony PA, Paulos CM, Ahmadzadeh M, et al. Interleukin-2-dependent mechanisms of tolerance and immunity in vivo. J Immunol 2006;176(9):5255-5266
17. Jaleco S, Swainson L, Dardalhon V, et al. Homeostasis of naive and memory CD4+ T cells: IL-2 and IL-7 differentially regulate the balance between proliferation and Fas-mediated apoptosis. J Immunol 2003;171(1):61-68
18. Atkins MB, Kunkel L, Sznol M, et al. High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J Sci Am 2000;6(Suppl 1):S11-14
19. Tsao H, Atkins MB, Sober AJ. Management of cutaneous melanoma. N Engl J Med 2004;351:998-1012
20. Curtsinger JM, Lins DC, Mescher MF. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 2003;197:1141-1151
21. Kalinski P, Hilkens CM, Wierenga EA, et al. T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today 1999;20:561-567
22. Yoo JK, Cho JH, Lee SW, et al. IL-12 provides proliferation and survival signals to murine CD4+T cells through phosphatidylinositol 3-kinase/Akt signaling pathway. J Immunol 2002;169:3637-3643
23. Wesa A, Kalinski P, Tatsumi T, et al. Polarized type-1 dendritic cells (DC1) producing high levels of IL-12 family members rescue patient TH1-type anti-melanoma CD4+ T cell responses in vitro. J Immunother 2007;30:75-82
24. Trinchieri G, Pflanz S, Kastelein RA. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003;19:641-644
25. Rakhit A, Yeon MM, Ferrante J, et al. Down-regulation of the pharmacokinetic-pharmacodynamic response to interleukin-12 during long-term administration to patients with renal cell carcinoma and evaluation of the mechanism of this "adaptive response" in mice. Clin Pharmacol Ther 1999;65:615-629
26. Beyer M, Schultze JL. Regulatory T cells in cancer. Blood 2006;108:804-811
27. Okamura H, Tsutsi H, Komatsu T, et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995;378:88-91
28. Smyth MJ, Taniguchi M, Street SE. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol 2000;165:2665-2670
29. Okamoto I, Kohno K, Tanimoto T, et al. Development of CD8+ effector T cells is differentially regulated by IL-18 and IL-12. J Immunol 1999;162:3202-3211
30. Dao T, Ohashi K, Kayano T, et al. Interferon-gamma-inducing factor, a novel cytokine, enhances Fas ligand-mediated cytotoxicity of murine T helper 1 cells. Cell Immunol 1996;173:230-235
31. Micallef MJ, Ohtsuki T, Kohno K, et al. Interferon-gamma-inducing factor enhances T helper 1 cytokine production by stimulated human T cells: synergism with interleukin-12 for interferon-gamma production. Eur J Immunol 1996;26:1647-1651
32. Swain SL. Interleukin 18: tipping the balance towards a T helper cell 1 response. J Exp Med 2001;194:F11-14
33. Okano F, Yamada K. Canine interleukin-18 induces apoptosis and enhances Fas ligand mRNA expression in a canine carcinoma cell line. Anticancer Res 2000;20:3411-3415
34. Coughlin CM, Salhany KE, Wysocka M, et al. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J Clin Invest 1998;101:1441-1452
35. Torigoe K, Ushio S, Okura T, et al. Purification and characterization of the human interleukin-18 receptor. Am Soc Biochem Mol Biol 1997;272:25737-25742
36. Hoshino K, Tsutsui H, Kawai T, et al. Cutting edge: generation of IL-18 receptor-deficient mice: evidence for IL-1 receptor-related protein as an essential IL-18 binding receptor. J Immunol 1999;162:5041-5044
37. Nakanishi K, Yoshimoto T, Tsutsui H, et al. Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol 2001;19:423-474
38. Gerdes N, Sukhova GK, Libby P, et al. Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for atherogenesis. J Exp Med 2002;195:245-257
39. Leung BP, Culshaw S, Gracie JA, et al. A role for IL-18 in neutrophil activation. J Immunol 2001;167:2879-2886
40. Leung W, Iyengar R, Turner V, et al. Determinants of antileukemia effects of allogeneic NK cells. J Immunol 2004;172:644-650
41. Azam T, Novick D, Bufler P, et al. Identification of a critical Ig-like domain in IL-18 receptor alpha and characterization of a functional IL-18 receptor complex. J Immunol 2003;171:6574-6580
42. Micallef MJ, Tanimoto T, Kohno K, et al. Interleukin 18 induces the sequential activation of natural killer cells and cytotoxic T lymphocytes to protect syngeneic mice from transplantation with Meth A sarcoma. Cancer Res 1997;57:4557-4563
43. Osaki T, Péron JM, Cai Q, et al. IFN-gamma-inducing factor/IL-18 administration mediates IFN-gamma-and IL-12-independent antitumor effects. J Immunol 1998;160:1742-1749
44. Hashimoto W, Osaki T, Okamura H, et al. Differential antitumor effects of administration of recombinant IL-18 or recombinant IL-12 are mediated primarily by Fas--Fas ligand-and perforin-induced tumor apoptosis, respectively. J Immunol 1999;163:583-589
45. Wigginton JM, Lee JK, Wiltrout TA, et al. Synergistic engagement of an ineffective endogenous anti-tumor immune response and induction of IFN-gamma and Fas-ligand-dependent tumor eradication by combined administration of IL-18 and IL-2. J Immunol 2002;169:4467-4474
46. Akamatsu S, Arai N, Hanaya T, et al. Antitumor activity of interleukin-18 against the murine T-cell leukemia/lymphoma EL-4 in syngeneic mice. J Immunother 2002;25:S28-34
47. Wang Q, Yu H, Ju DW, et al. Intratumoral IL-18 gene transfer improves therapeutic efficacy of antibody-targeted superantigen in established murine melanoma. Gene Ther 2001;8:542-550
48. Ju DW, Yang Y, Tao Q, et al. Interleukin-18 gene transfer increases antitumor effects of suicide gene therapy through efficient induction of antitumor immunity. Gene Ther 2000;7:1672-1679
49. Robertson MJ, Mier JW, Logan T, et al. Clinical and biological effects of recombinant human interleukin-18 administered by intravenous infusion to patients with advanced cancer. Clin Cancer Res 2006;12:4265-4273
50. Tsutsui H, Matsui K, Kawada N, et al. IL-18 accounts for both TNF-alpha-and Fas ligand-mediated hepatotoxic pathways in endotoxin-induced liver injury in mice. J Immunol 1997;159:3961-3967
51. Son Y, Dallal RM, Mailliard RB, et al. Interleukin-18 (IL-18) synergizes with IL-2 to enhance cytotoxicity, interferon-gamma production, and expansion of natural killer cells. Cancer Res 2001;61:884-888
52. Son Y, Dallal RM, Lotze MT. Combined treatment with interleukin-18 and low-dose interleukin-2 induced regression of a murine sarcoma and memory response. J Immunother 2003;25:234-240
53. Li Q, Car AL, Donald EJ, et al. Synergistic effects of IL-12 and IL-18 in skewing tumor-reactive T-Cell responses towards a type 1 pattern. Cancer Res 2005;65:1063-1070
54. Motzer RJ, Rakhit A, Schwartz LH, et al. Phase I trial of subcutaneous recombinant human interleukin-12 in patients with advanced renal cell carcinoma. Clin Cancer Res 1998;4:1183-1191
55. Portielje JE, Kruit WH, Schuler M, et al. Phase I study of subcutaneously administered recombinant human interleukin 12 in patients with advanced renal cell cancer. Clin Cancer Res 1999;5:3983-3989
56. Carson WE, Dierksheide JE, Jabbour S, et al. Coadministration of interleukin-18 and interleukin-12 induces a fatal inflammatory response in mice: critical role of natural killer cell interferon-gamma production and STAT-mediated signal transduction. Blood 2000;96:1465-1473
57. Jiang H, Lin JJ, Su ZZ, et al. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 1995;11:2477-2486
58. Jiang H, Su ZZ, Lin JJ, et al. The melanoma differentiation associated gene mda-7 suppresses cancer cell growth. Proc Natl Acad Sci USA 1996;93:9160-9165
59. Pestka S, Krause CD, Sarkar D, et al. Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 2004;22:929-979
60. Huang EY, Madireddi MT, Gopalkrishnan RV, et al. Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogene 2001;20:7051-7063
61. Fisher PB, Sarkar D, Lebedeva IV, et al. Melanoma differentiation associated gene-7/interleukin-24 (mda-7/IL-24): novel gene therapeutic for metastatic melanoma. Toxicol Appl Pharmacol 2007;224(3):300-307
62. Fisher PB. Is mda-7/IL-24 a "magic bullet" for cancer? Cancer Res 2005;65:10128-10138
63. Gupta P, Su Z-Z, Lebedeva IV, et al. mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther 2006;111:596-628
64. Lebedeva IV, Sauane M, Gopalkrishnan RV, et al. mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 2005;11:4-18
65. Cunningham CC, Chada S, Merritt JA, et al. Clinical and local biological effects of an intratumoral injection of mda-7 (IL24; INGN 241) in patients with advanced carcinoma: a Phase I study. Mol Ther 2005;11:149-159
66. Tong AW, Nemunaitis J, Su D, et al. Intratumoral injection of INGN 241, a nonreplicating adenovector expressing the melanoma-differentiation associated gene-7 (mda-7/IL24): biologic outcome in advanced cancer patients. Mol Ther 2005;11:160-172
67. Fisher PB. Is mda7/IL24 a 'magic bullet' for cancer? Cancer Res 2005;65:10128-10138
68. Su ZZ, Madireddi MT, Lin JJ, et al. The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc Natl Acad Sci USA 1998;95:14400-14405
69. Gopalan B, Shanker M, Chada S, et al. MDA-7/IL-24 suppresses human ovarian carcinoma growth in vitro and in vivo. Mol Cancer 2007;6:11
70. Saeki T, Mhashilkar A, Chada S, et al. Tumor suppressive effects by adenovirus-mediated mda-7 gene transfer in nonsmall cell lung cancer in vitro. Gene Therapy 2000;7:2051-2057
71. Saeki T, Mhashilkar A, Swanson X, et al. Inhibition of human lung cancer growth following adenovirus mediated mda-7 gene expression in vivo. Oncogene 2002;21:4558-4566
72. Zhao L, Dong A, Gu J, et al. The antitumor activity of TRAIL and IL-24 with replicating oncolytic adenovirus in colorectal cancer. Cancer Gene Ther 2006;13:1011-1022
73. Qian W, Liu J, Tong Y, et al. Enhanced antitumor activity by a selective conditionally replicating adenovirus combining with MDA-7/interleukin-24 for B-lymphoblastic leukemia via induction of apoptosis. Leukemia 2008;22(2):361-369
74. Zhao L, Gu J, Dong A, et al. Potent antitumor activity of oncolytic adenovirus expressing mda-7/IL-24 for colorectal cancer. Hum Gene Ther 2005;16(7):845-858
75. Wu YM, Zhang KJ, Yue XT, et al. Enhancement of tumor cell death by combining cisplatin with an oncolytic adenovirus carrying MDA-7/IL-24. Acta Pharmacol Sin 2009;30(4):467-477
76. Zhang KJ, Wang YG, Cao X, et al. Potent antitumor effect of interleukin-24 gene in the survivin promoter and retinoblastoma double-regulated oncolytic adenovirus. Hum Gene Ther 2009;20(8):818-830
77. Luo J, Xia Q, Zhang R, et al. Treatment of cancer with a novel dual-targeted conditionally replicative adenovirus armed with mda-7/IL-24 gene. Clin Cancer Res 2008;14(8):2450-2457
78. Robertson MJ, Mier JW, Logan T, et al. Clinical and biological effects of recombinant human interleukin-18 administered by intravenous infusion to patients with advanced cancer. Clin Cancer Res 2006;12:4265-4273
79. Nakamura S, Otani T, Ijiri Y, et al. IFN-gamma-dependent and-independent mechanisms in adverse effects caused by concomitant administration of IL-18 and IL-12. J Immunol 2000;164:3330-3336
80. Zheng JN, Pei DS, Mao LJ, et al. Oncolytic adenovirus expressing interleukin-18 induces significant antitumor effects against melanoma in mice through inhibition of angiogenesis. Cancer Gene Ther 2010;17(1):28-36
81. Zheng JN, Pei DS, Sun FH, et al. Potent antitumor efficacy of interleukin-18 delivered by conditionally replicative adenovirus vector in renal cell carcinoma-bearing nude mice via inhibition of angiogenesis. Cancer Biol Ther 2009;8(7):599-606
82. Trinchieri G. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv Immunol 1998;70:83-243
83. Linsley PS, Ledbetter JA. The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol 1993;11:191-212
84. Hathcock KS, Laszlo G, Pucillo C, et al. Comparative analysis of B7-1and B7-2 costimulatory ligands: expression and function. J Exp Med 1994;180:631-640
85. Chamberlain RS, Carroll MW, Bronte V, et al. Costimulation enhancest he active immunotherapy effect of recombinant anticancer vaccines. Cancer Res 1996;56:2832-2836
86. Tatsumi T, Takehara T, Kanto T, et al. B7-1 (CD80)-gene transfer combined with interleukin-12 administration elicitsp rotective and therapeutic immunity against mouse hepatocellular carcinoma. Hepatology 1999;30:422-429
87. Lee YS, Kim JH, Choi KJ, et al. Enhanced antitumor effect of oncolytic adenovirus expressing interleukin-12 and B7-1 in an immunocompetent murine model. Clin Cancer Res 2006;12(19):5859-5868
88. Bortolanza S, Bunuales M, Otano I, et al. Treatment of pancreatic cancer with an oncolytic adenovirus expressing interleukin-12 in Syrian hamsters. Mol Ther 2009;17(4):614-622
89. Post DE, Sandberg EM, Kyle MM, et al. Targeted cancer gene therapy using a hypoxia inducible factor dependent oncolytic adenovirus armed with interleukin-4. Cancer Res 2007;67(14):6872-6881
90. Dranoff G, Jaffee E, Lazenby A, et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent,specific,and longlasting anti-tumor immunity. Proc Natl Acad Sci USA 1993;90:3539-3543
91. Bristol JA, Zhu M, Ji H, et al. In vitro and in vivo activities of an oncolytic adenoviral vector designed to express GM-CSF. Mol Ther 2003;7(6):755-764
92. Ramesh N, Ge Y, Ennist DL, et al. CG0070, a conditionally replicating granulocyte macrophage colony-stimulating factor-armed oncolytic adenovirus for the treatment of bladder cancer. Clin Cancer Res 2006;12(1):305-313
93. Choi KJ, Kim JH, Lee YS, et al. Concurrent delivery of GM-CSF and B7-1 using an oncolytic adenovirus elicits potent antitumor effect. Gene Ther 2006;13(13):1010-1020
94. Lei N, Shen FB, Chang JH, et al. An oncolytic adenovirus expressing granulocyte macrophage colony-stimulating factor shows improved specificity and efficacy for treating human solid tumors. Cancer Gene Ther 2009;16(1):33-43
95. Chang J, Zhao X, Wu X, et al. A Phase I study of KH901, a conditionally replicating granulocyte-macrophage colony-stimulating factor: armed oncolytic adenovirus for the treatment of head and neck cancers. Cancer Biol Ther 2009;8(8):676-682
96. Steel JC, Morrison BJ, Mannan P, et al. Immunocompetent syngeneic cotton rat tumor models for the assessment of replication-competent oncolytic adenovirus. Virology 2007;369:131-142
97. Thomas MA, Spencer JF, La Regina MC, et al. Syrian hamster as a permissive immunocompetent animal model for the study of oncolytic adenovirus vectors. Cancer Res 2006;66:1270-1276
98. Wildner O, Hoffmann D, Jogler C, et al. Comparison of HSV-1 thymidine kinase-dependent and--independent inhibition of replication-competent adenoviral vectors by a panel of drugs. Cancer Gene Ther 2003;10:791-802
99. Kirn D, Martuza RL, Zwiebel J. Replication-selective virotherapy for cancer: biological principles, risk management and future directions. Nat Med 2001;7:781-787
100. Shayakhmetov DM, Papayannopoulou T, Stamatoyannopoulos G, et al. Efficient gene transfer into human CD34+ cells by a retargeted adenovirus vector. J Virol 2000;74(6):2567-2583
101. Qiao J, Kottke T, Willmon C, et al. Purging metastases in lymphoid organs using a combination of antigen-nonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat Med 2008;14:37-44
102. Iankov ID, Blechacz B, Liu C, et al. Infected cell carriers: a new strategy for systemic delivery of oncolytic measles viruses in cancer virotherapy. Mol Ther 2007;15:114-122
103. Power AT, Wang J, Falls TJ, et al. Carrier cell-based delivery of an oncolytic virus circumvents antiviral immunity. Mol Ther 2007;15:123-130
104. Hermiston TW, Kuhn I. Armed therapeutic viruses: strategies and challenges to arming oncolytic viruses with therapeutic genes. Cancer Gene Ther 2002;9:1022-1035