Antitumor activity of tumor-targeted RNA replicase-based plasmid that expresses interleukin-2 in a murine melanoma model

Molecular Pharmaceutics

Volumn 10, Issue 6, 2013, Pages 2404-2415

  Rodriguez, B Leticia ^a   Blando, Jorge M ^a   Lansakara P, Dharmika S P ^a   Kiguchi, Yuriko ^a   Digiovanni, John ^a   Cui, Zhengrong ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

anisamide; dsRNA therapy; IL2 therapy; melanoma; sigma receptor

Indexed keywords

INTERLEUKIN 2; LIPOSOME; RNA DIRECTED RNA POLYMERASE; SIGMA OPIATE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; GENE; GENE THERAPY; MELANOMA; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; SINDBIS VIRUS;

ANIMALS; CASPASE 3; CELL LINE; FEMALE; INTERLEUKIN-2; LIPOSOMES; MELANOMA; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PLASMIDS; RNA REPLICASE;

EID: 84878653944     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400033m     Document Type: Article

References (55)

1. Blank, C. U.; Hooijkaas, A. I.; Haanen, J. B.; Schumacher, T. N. Combination of targeted therapy and immunotherapy in melanoma Cancer Immunol. Immunother. 2011, 60 (10) 1359-71
2. Puzanov, I.; Flaherty, K. T. Targeted molecular therapy in melanoma Semin. Cutan. Med. Surg. 2010, 29 (3) 196-201
3. Foa, R.; Guarini, A.; Gansbacher, B. IL2 treatment for cancer: from biology to gene therapy Br. J. Cancer 1992, 66 (6) 992-8
4. Riker, A. I.; Radfar, S.; Liu, S.; Wang, Y.; Khong, H. T. Immunotherapy of melanoma: a critical review of current concepts and future strategies Expert Opin. Biol. Ther. 2007, 7 (3) 345-58
5. Rosenberg, S. A.; Yang, J. C.; White, D. E.; Steinberg, S. M. Durability of complete responses in patients with metastatic cancer treated with high-dose interleukin-2: identification of the antigens mediating response Ann. Surg. 1998, 228 (3) 307-19
6. Ali, G.; Boldrini, L.; Lucchi, M.; Picchi, A.; Dell'Omodarme, M.; Prati, M. C.; Mussi, A.; Corsi, V.; Fontanini, G. Treatment with interleukin-2 in malignant pleural mesothelioma: immunological and angiogenetic assessment and prognostic impact Br. J. Cancer 2009, 101 (11) 1869-75
7. Jackaman, C.; Bundell, C. S.; Kinnear, B. F.; Smith, A. M.; Filion, P.; van Hagen, D.; Robinson, B. W.; Nelson, D. J. IL-2 intratumoral immunotherapy enhances CD8+ T cells that mediate destruction of tumor cells and tumor-associated vasculature: a novel mechanism for IL-2 J. Immunol. 2003, 171 (10) 5051-63
8. West, W. H.; Tauer, K. W.; Yannelli, J. R.; Marshall, G. D.; Orr, D. W.; Thurman, G. B.; Oldham, R. K. Constant-infusion recombinant interleukin-2 in adoptive immunotherapy of advanced cancer N. Engl. J. Med. 1987, 316 (15) 898-905
9. Cortesina, G.; De Stefani, A.; Giovarelli, M.; Barioglio, M. G.; Cavallo, G. P.; Jemma, C.; Forni, G. Treatment of recurrent squamous cell carcinoma of the head and neck with low doses of interleukin-2 injected perilymphatically Cancer 1988, 62 (12) 2482-5
10. Belldegrun, A.; Tso, C. L.; Zisman, A.; Naitoh, J.; Said, J.; Pantuck, A. J.; Hinkel, A.; deKernion, J.; Figlin, R. Interleukin 2 gene therapy for prostate cancer: phase I clinical trial and basic biology Human Gene Ther. 2001, 12 (8) 883-92
11. Galanis, E.; Burch, P. A.; Richardson, R. L.; Lewis, B.; Pitot, H. C.; Frytak, S.; Spier, C.; Akporiaye, E. T.; Peethambaram, P. P.; Kaur, J. S.; Okuno, S. H.; Unni, K. K.; Rubin, J. Intratumoral administration of a 1,2-dimyristyloxypropyl-3-dimethylhydroxyethyl ammonium bromide/ dioleoylphosphatidylethanolamine formulation of the human interleukin-2 gene in the treatment of metastatic renal cell carcinoma Cancer 2004, 101 (11) 2557-66
12. Galanis, E.; Hersh, E. M.; Stopeck, A. T.; Gonzalez, R.; Burch, P.; Spier, C.; Akporiaye, E. T.; Rinehart, J. J.; Edmonson, J.; Sobol, R. E.; Forscher, C.; Sondak, V. K.; Lewis, B. D.; Unger, E. C.; O'Driscoll, M.; Selk, L.; Rubin, J. Immunotherapy of advanced malignancy by direct gene transfer of an interleukin-2 DNA/DMRIE/DOPE lipid complex: phase I/II experience J. Clin. Oncol. 1999, 17 (10) 3313-23
13. Fearon, E. R.; Pardoll, D. M.; Itaya, T.; Golumbek, P.; Levitsky, H. I.; Simons, J. W.; Karasuyama, H.; Vogelstein, B.; Frost, P. Interleukin-2 production by tumor cells bypasses T helper function in the generation of an antitumor response Cell 1990, 60 (3) 397-403
14. Zier, K. S.; Gansbacher, B. IL-2 gene therapy of solid tumors: an approach for the prevention of signal transduction defects in T cells J. Mol. Med. (Berlin) 1996, 74 (3) 127-34
15. Fujimura, T.; Nakagawa, S.; Ohtani, T.; Ito, Y.; Aiba, S. Inhibitory effect of the polyinosinic-polycytidylic acid/cationic liposome on the progression of murine B16F10 melanoma Eur. J. Immunol. 2006, 36 (12) 3371-80
16. Absher, M.; Stinebring, W. R. Toxic properties of a synthetic double-stranded RNA. Endotoxin-like properties of poly I. poly C, an interferon stimulator Nature 1969, 223 (5207) 715-7
17. Chawla-Sarkar, M.; Lindner, D. J.; Liu, Y. F.; Williams, B. R.; Sen, G. C.; Silverman, R. H.; Borden, E. C. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis Apoptosis 2003, 8 (3) 237-49
18. Friedrich, I.; Shir, A.; Klein, S.; Levitzki, A. RNA molecules as anti-cancer agents Semin. Cancer Biol. 2004, 14 (4) 223-30
19. Schulz, O.; Diebold, S. S.; Chen, M.; Naslund, T. I.; Nolte, M. A.; Alexopoulou, L.; Azuma, Y. T.; Flavell, R. A.; Liljestrom, P.; Reis e Sousa, C. Toll-like receptor 3 promotes cross-priming to virus-infected cells Nature 2005, 433 (7028) 887-92
20. Cui, Z.; Le, U. M.; Qiu, F.; Shaker, D. S. Learning from viruses: the necrotic bodies of tumor cells with intracellular synthetic dsRNA induced strong anti-tumor immune responses Pharm. Res. 2007, 24 (9) 1645-52
21. McBride, S.; Hoebe, K.; Georgel, P.; Janssen, E. Cell-associated double-stranded RNA enhances antitumor activity through the production of type I IFN J. Immunol. 2006, 177 (9) 6122-8
22. Rodriguez, B. L.; Yu, Z.; Chung, W. G.; Weiss, R.; Cui, Z. Replicase-based plasmid DNA shows anti-tumor activity BMC Cancer 2011, 11, 110
23. Rodriguez, B. L.; Li, X.; Kiguchi, K.; DiGiovanni, J.; Unger, E. C.; Cui, Z. Control of solid tumor growth in mice using EGF receptor-targeted RNA replicase-based plasmid DNA Nanomedicine (London) 2012, 7 (4) 475-91
24. Vilner, B. J.; John, C. S.; Bowen, W. D. Sigma-1 and sigma-2 receptors are expressed in a wide variety of human and rodent tumor cell lines Cancer Res. 1995, 55 (2) 408-13
25. Hou, C.; Tu, Z.; Mach, R.; Kung, H. F.; Kung, M. P. Characterization of a novel iodinated sigma-2 receptor ligand as a cell proliferation marker Nucl. Med. Biol. 2006, 33 (2) 203-9
26. Banerjee, R.; Tyagi, P.; Li, S.; Huang, L. Anisamide-targeted stealth liposomes: a potent carrier for targeting doxorubicin to human prostate cancer cells Int. J. Cancer 2004, 112 (4) 693-700
27. Chen, Y.; Bathula, S. R.; Yang, Q.; Huang, L. Targeted nanoparticles deliver siRNA to melanoma J. Invest. Dermatol. 2010, 130 (12) 2790-8
28. Le, U. M.; Cui, Z. Long-circulating gadolinium-encapsulated liposomes for potential application in tumor neutron capture therapy Int. J. Pharmaceutics 2006, 312 (1-2) 105-12
29. Scheiblhofer, S.; Weiss, R.; Gabler, M.; Leitner, W. W.; Thalhamer, J. Replicase-based DNA vaccines for allergy treatment Methods Mol. Med. 2006, 127, 221-35
30. Sloat, B. R.; Sandoval, M. A.; Li, D.; Chung, W. G.; Lansakara, P. D.; Proteau, P. J.; Kiguchi, K.; DiGiovanni, J.; Cui, Z. In vitro and in vivo anti-tumor activities of a gemcitabine derivative carried by nanoparticles Int. J. Pharmaceutics 2011, 409 (1-2) 278-88
31. Cui, Z.; Qiu, F. Synthetic double-stranded RNA poly(I:C) as a potent peptide vaccine adjuvant: therapeutic activity against human cervical cancer in a rodent model Cancer Immunol. Immunother. 2006, 55 (10) 1267-79
32. Festing, M. F.; Altman, D. G. Guidelines for the design and statistical analysis of experiments using laboratory animals ILAR J. 2002, 43 (4) 244-58
33. Ziegler, S. F.; Ramsdell, F.; Alderson, M. R. The activation antigen CD69 Stem Cells 1994, 12 (5) 456-65
34. Hirabayashi, K.; Yano, J.; Inoue, T.; Yamaguchi, T.; Tanigawara, K.; Smyth, G. E.; Ishiyama, K.; Ohgi, T.; Kimura, K.; Irimura, T. Inhibition of cancer cell growth by polyinosinic-polycytidylic acid/cationic liposome complex: a new biological activity Cancer Res. 1999, 59 (17) 4325-33
35. Le, U. M.; Kaurin, D. G.; Sloat, B. R.; Yanasarn, N.; Cui, Z. Localized irradiation of tumors prior to synthetic dsRNA therapy enhanced the resultant anti-tumor activity Radiother. Oncol. 2009, 90 (2) 273-9
36. Le, U. M.; Yanasarn, N.; Lohr, C. V.; Fischer, K. A.; Cui, Z. Tumor chemo-immunotherapy using gemcitabine and a synthetic dsRNA Cancer Biol. Ther 2008, 7 (3) 440-7
37. Okada, C.; Akbar, S. M.; Horiike, N.; Onji, M. Early development of primary biliary cirrhosis in female C57BL/6 mice because of poly I:C administration Liver Int. 2005, 25 (3) 595-603
38. Pimm, M. V.; Baldwin, R. W. Treatment of transplanted rat tumours with double-stranded RNA(BRL 5907). II. Treatment of pleural and peritoneal growths Br. J. Cancer 1976, 33 (2) 166-71
39. Meier, H.; Myers, D. D.; Huebner, R. J. Ineffectiveness of poly rI:rC on transplanted tumors induced by methylcholanthrene Naturwissenschaften 1970, 57 (5) 248-9
40. Shimizu, J.; Yamazaki, S.; Sakaguchi, S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity J. Immunol. 1999, 163 (10) 5211-8
41. Tanaka, H.; Tanaka, J.; Kjaergaard, J.; Shu, S. Depletion of CD4+ CD25+ regulatory cells augments the generation of specific immune T cells in tumor-draining lymph nodes J. Immunother. 2002, 25 (3) 207-17
42. Yao, H.; Ng, S. S.; Huo, L. F.; Chow, B. K.; Shen, Z.; Yang, M.; Sze, J.; Ko, O.; Li, M.; Yue, A.; Lu, L. W.; Bian, X. W.; Kung, H. F.; Lin, M. C. Effective melanoma immunotherapy with interleukin-2 delivered by a novel polymeric nanoparticle Mol. Cancer Ther. 2011, 10 (6) 1082-92
43. Lal, G.; Zhang, N.; van der Touw, W.; Ding, Y.; Ju, W.; Bottinger, E. P.; Reid, S. P.; Levy, D. E.; Bromberg, J. S. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation J. Immunol. 2009, 182 (1) 259-73
44. Korn, T.; Mitsdoerffer, M.; Croxford, A. L.; Awasthi, A.; Dardalhon, V. A.; Galileos, G.; Vollmar, P.; Stritesky, G. L.; Kaplan, M. H.; Waisman, A.; Kuchroo, V. K.; Oukka, M. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+ regulatory T cells Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (47) 18460-5
45. Di Giacomo, A. M.; Ascierto, P. A.; Pilla, L.; Santinami, M.; Ferrucci, P. F.; Giannarelli, D.; Marasco, A.; Rivoltini, L.; Simeone, E.; Nicoletti, S. V.; Fonsatti, E.; Annesi, D.; Queirolo, P.; Testori, A.; Ridolfi, R.; Parmiani, G.; Maio, M. Ipilimumab and fotemustine in patients with advanced melanoma (NIBIT-M1): an open-label, single-arm phase 2 trial Lancet Oncol. 2012, 13 (9) 879-86
46. Bem, W. T.; Thomas, G. E.; Mamone, J. Y.; Homan, S. M.; Levy, B. K.; Johnson, F. E.; Coscia, C. J. Overexpression of sigma receptors in nonneural human tumors Cancer Res. 1991, 51 (24) 6558-62
47. John, C. S.; Bowen, W. D.; Saga, T.; Kinuya, S.; Vilner, B. J.; Baumgold, J.; Paik, C. H.; Reba, R. C.; Neumann, R. D.; Varma, V. M. A malignant melanoma imaging agent: synthesis, characterization, in vitro binding and biodistribution of iodine-125-(2-piperidinylaminoethyl)4-iodobenzamide J. Nucl. Med. 1993, 34 (12) 2169-75
48. Caveliers, V.; Everaert, H.; John, C. S.; Lahoutte, T.; Bossuyt, A. Sigma receptor scintigraphy with N-[2-(1′-piperidinyl)ethyl]-3-(123)I-iodo-4- methoxybenzamide of patients with suspected primary breast cancer: first clinical results J. Nucl. Med. 2002, 43 (12) 1647-9
49. John, C. S.; Vilner, B. J.; Geyer, B. C.; Moody, T.; Bowen, W. D. Targeting sigma receptor-binding benzamides as in vivo diagnostic and therapeutic agents for human prostate tumors Cancer Res. 1999, 59 (18) 4578-83
50. Kashiwagi, H.; McDunn, J. E.; Simon, P. O., Jr.; Goedegebuure, P. S.; Xu, J.; Jones, L.; Chang, K.; Johnston, F.; Trinkaus, K.; Hotchkiss, R. S.; Mach, R. H.; Hawkins, W. G. Selective sigma-2 ligands preferentially bind to pancreatic adenocarcinomas: applications in diagnostic imaging and therapy Mol. Cancer 2007, 6, 48
51. Megalizzi, V.; Le Mercier, M.; Decaestecker, C. Sigma receptors and their ligands in cancer biology: overview and new perspectives for cancer therapy Med. Res. Rev. 2012, 32 (2) 410-27
52. Everaert, H.; Flamen, P.; Franken, P. R.; Verhaeghe, W.; Bossuyt, A. Sigma-receptor imaging by means of I123-IDAB scintigraphy: clinical application in melanoma and non-small cell lung cancer Anticancer Res. 1997, 17 (3B) 1577-82
53. Brown, D. M.; Fisher, T. L.; Wei, C.; Frelinger, J. G.; Lord, E. M. Tumours can act as adjuvants for humoral immunity Immunology 2001, 102 (4) 486-97
54. Li, S. D.; Chono, S.; Huang, L. Efficient oncogene silencing and metastasis inhibition via systemic delivery of siRNA Mol. Ther. 2008, 16 (5) 942-6
55. Leitner, W. W.; Hwang, L. N.; Bergmann-Leitner, E. S.; Finkelstein, S. E.; Frank, S.; Restifo, N. P. Apoptosis is essential for the increased efficacy of alphaviral replicase-based DNA vaccines Vaccine 2004, 22 (11-12) 1537-44