Oncolytic virotherapy in veterinary medicine: Current status and future prospects for canine patients

Journal of Translational Medicine

Volumn 10, Issue 1, 2012, Pages

  Patil, Sandeep S ^a   Gentschev, Ivaylo ^a,b   Nolte, Ingo ^c   Ogilvie, Gregory ^d,e   Szalay, Aladar A ^a,b,e,f  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GENELUX CORPORATION   (United States)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d California Veterinary Specialists   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cancer; Canine cancer therapy; Oncolysis; Oncolytic virus; Target molecule, combination therapy

Indexed keywords

ADENOVIRUS VECTOR; CD40 LIGAND; GLV 1H68; JX 594; ONCOLYTIC VIRUS; PROTEIN P53; RECOMBITEK; UNCLASSIFIED DRUG;

ADENOVIRUS; ADVERSE OUTCOME; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER THERAPY; CANINE ADENOVIRUS; CANINE DISTEMPER MORBILLIVIRUS; CELL SPECIFICITY; CYTOLYSIS; DOG; DOUBLE STRANDED DNA BREAK; DRUG APPROVAL; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; IMMUNOCOMPROMISED PATIENT; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTOPENIA; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MOLECULARLY TARGETED THERAPY; NONHUMAN; ONCOLYTIC VIROTHERAPY; OSTEOSARCOMA; OUTCOME ASSESSMENT; REVIEW; SIGNAL TRANSDUCTION; VACCINIA VIRUS; VETERINARY MEDICINE; VIRUS MORPHOLOGY; VIRUS REPLICATION; WILD TYPE; ANIMAL; ANIMAL DISEASE; DOG DISEASE; HUMAN; MULTIMODALITY CANCER THERAPY; NEOPLASM; TRANSLATIONAL RESEARCH;

ANIMALS; COMBINED MODALITY THERAPY; DOG DISEASES; DOGS; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; TRANSLATIONAL MEDICAL RESEARCH; VETERINARY MEDICINE;

EID: 84855290113     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-10-3     Document Type: Review

References (124)

1. Merlo DF, Rossi L, Pellegrino C, Ceppi M, Cardellino U, Capurro C, Ratto A, Sambucco PL, Sestito V, Tanara G, Bocchini V. Cancer incidence in pet dogs: findings of the Animal Tumor Registry of Genoa, Italy. J Vet Intern Med 2008, 22:976-984. 10.1111/j.1939-1676.2008.0133.x, 18564221.
2. National Canine Cancer Foundation. , http://www.earethecure.org/
3. Kelsey JL, Moore AS, Glickman LT. Epidemiologic studies of risk factors for cancer in pet dogs. Epidemiol Rev 1998, 20:204-217.
4. Southam CM, Moore AE. Clinical studies of viruses as antineoplastic agents with particular reference to Egypt 101 virus. Cancer 1952, 5:1025-1034. 10.1002/1097-0142(195209)5:5<1025::AID-CNCR2820050518>3.0.CO;2-Q, 12988191.
5. Sinkovics JG. Viral oncolysates as human tumor vaccines. Int Rev Immunol 1991, 7:259-287. 10.3109/08830189109114875, 1663989.
6. Vaha-Koskela MJ, Heikkila JE, Hinkkanen AE. Oncolytic viruses in cancer therapy. Cancer Lett 2007, 254:178-216. 10.1016/j.canlet.2007.02.002, 17383089.
7. Moore AE. The destructive effect of the virus of Russian Far East encephalitis on the transplantable mouse sarcoma 180. Cancer 1949, 2:525-534. 10.1002/1097-0142(194905)2:3<525::AID-CNCR2820020317>3.0.CO;2-O, 18131412.
8. Phuangsab A, Lorence RM, Reichard KW, Peeples ME, Walter RJ. Newcastle disease virus therapy of human tumor xenografts: antitumor effects of local or systemic administration. Cancer Lett 2001, 172:27-36. 10.1016/S0304-3835(01)00617-6, 11595126.
9. Hirasawa K, Nishikawa SG, Norman KL, Coffey MC, Thompson BG, Yoon CS, Waisman DM, Lee PW. Systemic reovirus therapy of metastatic cancer in immune-competent mice. Cancer Res 2003, 63:348-353.
10. De Palma M, Venneri MA, Naldini L. In vivo targeting of tumor endothelial cells by systemic delivery of lentiviral vectors. Hum Gene Ther 2003, 14:1193-1206. 10.1089/104303403322168028, 12908970.
11. Fu X, Zhang X. Delivery of herpes simplex virus vectors through liposome formulation. Mol Ther 2001, 4:447-453. 10.1006/mthe.2001.0474, 11708881.
12. Shafren DR, Au GG, Nguyen T, Newcombe NG, Haley ES, Beagley L, Johansson ES, Hersey P, Barry RD. Systemic therapy of malignant human melanoma tumors by a common cold-producing enterovirus, coxsackievirus a21. Clin Cancer Res 2004, 10:53-60. 10.1158/1078-0432.CCR-0690-3, 14734451.
13. Tseng JC, Levin B, Hurtado A, Yee H, Perez de Castro I, Jimenez M, Shamamian P, Jin R, Novick RP, Pellicer A, Meruelo D. Systemic tumor targeting and killing by Sindbis viral vectors. Nat Biotechnol 2004, 22:70-77. 10.1038/nbt917, 14647305.
14. Vaha-Koskela MJ, Kallio JP, Jansson LC, Heikkila JE, Zakhartchenko VA, Kallajoki MA, Kahari VM, Hinkkanen AE. Oncolytic capacity of attenuated replicative semliki forest virus in human melanoma xenografts in severe combined immunodeficient mice. Cancer Res 2006, 66:7185-7194. 10.1158/0008-5472.CAN-05-2214, 16849565.
15. Reddy PS, Burroughs KD, Hales LM, Ganesh S, Jones BH, Idamakanti N, Hay C, Li SS, Skele KL, Vasko AJ, et al. Seneca Valley virus, a systemically deliverable oncolytic picornavirus, and the treatment of neuroendocrine cancers. J Natl Cancer Inst 2007, 99:1623-1633. 10.1093/jnci/djm198, 17971529.
16. Dobbelstein M. Replicating adenoviruses in cancer therapy. Curr Top Microbiol Immunol 2004, 273:291-334.
17. Zhang Q, Yu YA, Wang E, Chen N, Danner RL, Munson PJ, Marincola FM, Szalay AA. Eradication of solid human breast tumors in nude mice with an intravenously injected light-emitting oncolytic vaccinia virus. Cancer Res 2007, 67:10038-10046. 10.1158/0008-5472.CAN-07-0146, 17942938.
18. Lun XQ, Yang WQ, Alain T, Shi ZQ, Muzik H, Barrett JW, McFadden G, John BH, Hamilton MG, Senger DL, Forsyth PA. Myxoma virus is a novel oncolytic virus with significant antitumor activity against experimental human gliomas. Cancer Res 2005, 65:9982-9990. 10.1158/0008-5472.CAN-05-1201, 16267023.
19. Evgin L, Vaha-Koskela M, Rintoul J, Falls T, Le Boeuf F, Barrett JW, Bell JC, Stanford MM. Potent Oncolytic Activity of Raccoonpox Virus in the Absence of Natural Pathogenicity. Molecular Therapy 2010, 18:896-902. 10.1038/mt.2010.14, 2890119, 20160706.
20. Russell SJ. RNA viruses as virotherapy agents. Cancer Gene Ther 2002, 9:961-966. 10.1038/sj.cgt.7700535, 12522435.
21. Parato KA, Senger D, Forsyth PA, Bell JC. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 2005, 5:965-976. 10.1038/nrc1750, 16294217.
22. Cattaneo R, Miest T, Shashkova EV, Barry MA. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat Rev Microbiol 2008, 6:529-540. 10.1038/nrmicro1927, 18552863.
23. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst 2006, 98:298-300. 10.1093/jnci/djj111, 16507823.
24. Nemunaitis J, Cunningham C. Emerging new therapies for chemotherapy-resistant cancer using adenoviral vectors. Drug Resist Updat 2002, 5:34-46. 10.1016/S1368-7646(02)00048-1, 12127862.
25. Yu W, Fang H. Clinical trials with oncolytic adenovirus in China. Curr Cancer Drug Targets 2007, 7:141-148. 10.2174/156800907780058817, 17346105.
26. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, Ng L, Nye JA, Sampson-Johannes A, Fattaey A, McCormick F. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996, 274:373-376. 10.1126/science.274.5286.373, 8832876.
27. Liu TC, Wang Y, Hallden G, Brooks G, Francis J, Lemoine NR, Kirn D. Functional interactions of antiapoptotic proteins and tumor necrosis factor in the context of a replication-competent adenovirus. Gene Ther 2005, 12:1333-1346. 10.1038/sj.gt.3302555, 15920462.
28. Ternovoi VV, Le LP, Belousova N, Smith BF, Siegal GP, Curiel DT. Productive replication of human adenovirus type 5 in canine cells. J Virol 2005, 79:1308-1311. 10.1128/JVI.79.2.1308-1311.2005, 538546, 15613357.
29. Smith BF, Curiel DT, Ternovoi VV, Borovjagin AV, Baker HJ, Cox N, Siegal GP. Administration of a conditionally replicative oncolytic canine adenovirus in normal dogs. Cancer Biother Radiopharm 2006, 21:601-606. 10.1089/cbr.2006.21.601, 17257075.
30. Le LP, Rivera AA, Glasgow JN, Ternovoi VV, Wu H, Wang M, Smith BF, Siegal GP, Curiel DT. Infectivity enhancement for adenoviral transduction of canine osteosarcoma cells. Gene Ther 2006, 13:389-399. 10.1038/sj.gt.3302674, 16292351.
31. von Euler H, Sadeghi A, Carlsson B, Rivera P, Loskog A, Segall T, Korsgren O, Totterman TH. Efficient adenovector CD40 ligand immunotherapy of canine malignant melanoma. J Immunother 2008, 31:377-384. 10.1097/CJI.0b013e31816a812d, 18391758.
32. International Committee on Taxonomy of Viruses., Van Regenmortel MHV, International Union of Microbiological Societies. Virology Division Virus taxonomy: classification and nomenclature of viruses: seventh report of the International Committee on Taxonomy of Viruses 2000, San Diego: Academic Press, International Committee on Taxonomy of Viruses., Van Regenmortel MHV, International Union of Microbiological Societies. Virology Division.
33. Suter SE, Chein MB, von Messling V, Yip B, Cattaneo R, Vernau W, Madewell BR, London CA. In vitro canine distemper virus infection of canine lymphoid cells: a prelude to oncolytic therapy for lymphoma. Clin Cancer Res 2005, 11:1579-1587. 10.1158/1078-0432.CCR-04-1944, 15746063.
34. Bluming AZ, Ziegler JL. Regression of Burkitt's lymphoma in association with measles infection. Lancet 1971, 2:105-106.
35. Gross S. Measles and leukaemia. Lancet 1971, 1:397-398.
36. Tatsuo H, Ono N, Tanaka K, Yanagi Y. SLAM (CDw150) is a cellular receptor for measles virus. Nature 2000, 406:893-897. 10.1038/35022579, 10972291.
37. Tatsuo H, Ono N, Yanagi Y. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 2001, 75:5842-5850. 10.1128/JVI.75.13.5842-5850.2001, 114299, 11390585.
38. Shchelkunov SN, Totmenin AV, Babkin IV, Safronov PF, Ryazankina OI, Petrov NA, Gutorov VV, Uvarova EA, Mikheev MV, Sisler JR, et al. Human monkeypox and smallpox viruses: genomic comparison. FEBS Lett 2001, 509:66-70. 10.1016/S0014-5793(01)03144-1, 11734207.
39. Moss B, Earl PL. Overview of the vaccinia virus expression system. Curr Protoc Protein Sci 2001, Chapter 5. Unit5 11.
40. Fenner F. Smallpox and its eradication. World Health Organization, Geneva 1988,
41. Dranoff G. GM-CSF-based cancer vaccines. Immunol Rev 2002, 188:147-154. 10.1034/j.1600-065X.2002.18813.x, 12445288.
42. Clinical Trail Govt Database. , http://clinicaltrialsgov/ct2/show/NCT00794131
43. Park BH, Hwang T, Liu TC, Sze DY, Kim JS, Kwon HC, Oh SY, Han SY, Yoon JH, Hong SH, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol 2008, 9:533-542. 10.1016/S1470-2045(08)70107-4, 18495536.
44. Gentschev I, Ehrig K, Donat U, Hess M, Rudolph S, Chen N, Yu YA, Zhang Q, Bullerdiek J, Nolte I, et al. Significant Growth Inhibition of Canine Mammary Carcinoma Xenografts following Treatment with Oncolytic Vaccinia Virus GLV-1h68. J Oncol 2010, 2010:736907. 2902752, 20631910.
45. Gentschev I, Stritzker J, Hofmann E, Weibel S, Yu YA, Chen N, Zhang Q, Bullerdiek J, Nolte I, Szalay AA. Use of an oncolytic vaccinia virus for the treatment of canine breast cancer in nude mice: preclinical development of a therapeutic agent. Cancer Gene Ther 2009, 16:320-328. 10.1038/cgt.2008.87, 18949014.
46. Kelly KJ, Brader P, Woo Y, Li S, Chen N, Yu YA, Szalay AA, Fong Y. Real-time intraoperative detection of melanoma lymph node metastases using recombinant vaccinia virus GLV-1h68 in an immunocompetent animal model. Int J Cancer 2009, 124:911-918. 10.1002/ijc.24037, 2677523, 19035444.
47. Perkus ME, Taylor J, Tartaglia J, Pincus S, Kauffman EB, Tine JA, Paoletti E. Live attenuated vaccinia and other poxviruses as delivery systems: public health issues. Ann N Y Acad Sci 1995, 754:222-233. 10.1111/j.1749-6632.1995.tb44454.x, 7625655.
48. Jourdier TM, Moste C, Bonnet MC, Delisle F, Tafani JP, Devauchelle P, Tartaglia J, Moingeon P. Local immunotherapy of spontaneous feline fibrosarcomas using recombinant poxviruses expressing interleukin 2 (IL2). Gene Ther 2003, 10:2126-2132. 10.1038/sj.gt.3302124, 14625567.
49. Hasegawa K, Nakamura T, Harvey M, Ikeda Y, Oberg A, Figini M, Canevari S, Hartmann LC, Peng KW. The use of a tropism-modified measles virus in folate receptor-targeted virotherapy of ovarian cancer. Clin Cancer Res 2006, 12:6170-6178. 10.1158/1078-0432.CCR-06-0992, 17062694.
50. Hashiro G, Loh PC, Yau JT. The preferential cytotoxicity of reovirus for certain transformed cell lines. Arch Virol 1977, 54:307-315. 10.1007/BF01314776, 562142.
51. Lorence RM, Reichard KW, Katubig BB, Reyes HM, Phuangsab A, Mitchell BR, Cascino CJ, Walter RJ, Peeples ME. Complete regression of human neuroblastoma xenografts in athymic mice after local Newcastle disease virus therapy. J Natl Cancer Inst 1994, 86:1228-1233. 10.1093/jnci/86.16.1228, 8040891.
52. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N, Bell JC. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 2000, 6:821-825. 10.1038/77558, 10888934.
53. Yew PR, Berk AJ. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 1992, 357:82-85. 10.1038/357082a0, 1533443.
54. Zhang J, Chen X, Kent MS, Rodriguez CO. Establishment of a dog model for the p53 family pathway and identification of a novel isoform of p21 cyclin-dependent kinase inhibitor. Mol Cancer Res 2009, 7:67-78. 10.1158/1541-7786.MCR-08-0347, 2653090, 19147538.
55. Chu LL, Rutteman GR, Kong JM, Ghahremani M, Schmeing M, Misdorp W, van Garderen E, Pelletier J. Genomic organization of the canine p53 gene and its mutational status in canine mammary neoplasia. Breast Cancer Res Treat 1998, 50:11-25. 10.1023/A:1006010526813, 9802616.
56. Queiroga FL, Raposo T, Carvalho MI, Prada J, Pires I. Canine mammary tumours as a model to study human breast cancer: most recent findings. In Vivo 2011, 25:455-465.
57. Levine RA, Fleischli MA. Inactivation of p53 and retinoblastoma family pathways in canine osteosarcoma cell lines. Vet Pathol 2000, 37:54-61. 10.1354/vp.37-1-54, 10643981.
58. Rungsipipat A, Tateyama S, Yamaguchi R, Uchida K, Miyoshi N, Hayashi T. Immunohistochemical analysis of c-yes and c-erbB-2 oncogene products and p53 tumor suppressor protein in canine mammary tumors. J Vet Med Sci 1999, 61:27-32. 10.1292/jvms.61.27, 10027159.
59. Carrasco V, Canfran S, Rodriguez-Franco F, Benito A, Sainz A, Rodriguez-Bertos A. Canine gastric carcinoma: immunohistochemical expression of cell cycle proteins (p53, p21, and p16) and heat shock proteins (Hsp27 and Hsp70). Vet Pathol 2011, 48:322-329. 10.1177/0300985810375050, 20587688.
60. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009, 9:64-71. 10.1038/nrc2545, 19104515.
61. Liu L, Chavan R, Feinberg MB. Dendritic cells are preferentially targeted among hematolymphocytes by Modified Vaccinia Virus Ankara and play a key role in the induction of virus-specific T cell responses in vivo. BMC Immunol 2008, 9:15. 10.1186/1471-2172-9-15, 2359732, 18412969.
62. Thorne SH, Contag CH. Combining immune cell and viral therapy for the treatment of cancer. Cell Mol Life Sci 2007, 64:1449-1451. 10.1007/s00018-007-6550-z, 17404689.
63. Nakamura N, Momoi Y, Watari T, Yoshino T, Tsujimoto H, Hasegawa A. Plasma thymidine kinase activity in dogs with lymphoma and leukemia. J Vet Med Sci 1997, 59:957-960. 10.1292/jvms.59.957, 9362053.
64. von Euler H, Einarsson R, Olsson U, Lagerstedt AS, Eriksson S. Serum thymidine kinase activity in dogs with malignant lymphoma: a potent marker for prognosis and monitoring the disease. J Vet Intern Med 2004, 18:696-702.
65. Von Euler HP, Rivera P, Aronsson AC, Bengtsson C, Hansson LO, Eriksson SK. Monitoring therapy in canine malignant lymphoma and leukemia with serum thymidine kinase 1 activity--evaluation of a new, fully automated non-radiometric assay. Int J Oncol 2009, 34:505-510.
66. Selting KA, Thamm DH. Serum thymidine kinase concentrations in normal versus tumor-bearing dogs. Journal of Veterinary Internal Medicine 2008, 22:704-704.
67. Gama A, Gartner F, Alves A, Schmitt F. Immunohistochemical expression of Epidermal Growth Factor Receptor (EGFR) in canine mammary tissues. Res Vet Sci 2009, 87:432-437. 10.1016/j.rvsc.2009.04.016, 19464036.
68. Higgins RJ, Dickinson PJ, LeCouteur RA, Bollen AW, Wang H, Corely LJ, Moore LM, Zang W, Fuller GN. Spontaneous canine gliomas: overexpression of EGFR, PDGFRalpha and IGFBP2 demonstrated by tissue microarray immunophenotyping. J Neurooncol 2010, 98:49-55. 10.1007/s11060-009-0072-5, 19967449.
69. Grabarevic Z, Coric M, Seiwerth S, Dzaja P, Artukovic B, Kurilj AG, Beck A, Hohsteter M, Sostaric-Zuckermann IC, Brcic L, Hrstic I. Comparative analysis of hepatocellular carcinoma in men and dogs. Coll Antropol 2009, 33:811-814.
70. Shiomitsu K, Johnson CL, Malarkey DE, Pruitt AF, Thrall DE. Expression of epidermal growth factor receptor and vascular endothelial growth factor in malignant canine epithelial nasal tumours. Vet Comp Oncol 2009, 7:106-114. 10.1111/j.1476-5829.2009.00178.x, 19453364.
71. Kirn DH, Wang Y, Le Boeuf F, Bell J, Thorne SH. Targeting of interferon-beta to produce a specific, multi-mechanistic oncolytic vaccinia virus. PLoS Med 2007, 4:e353. 10.1371/journal.pmed.0040353, 2222946, 18162040.
72. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006, 6:836-848. 10.1038/nri1961, 17063185.
73. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006, 25:373-381. 10.1016/j.immuni.2006.08.007, 16979569.
74. Xu L, Rothman P. IFN-gamma represses epsilon germline transcription and subsequently down-regulates switch recombination to epsilon. Int Immunol 1994, 6:515-521. 10.1093/intimm/6.4.515, 8018593.
75. Heise CC, Williams A, Olesch J, Kirn DH. Efficacy of a replication-competent adenovirus (ONYX-015) following intratumoral injection: intratumoral spread and distribution effects. Cancer Gene Ther 1999, 6:499-504. 10.1038/sj.cgt.7700071, 10608346.
76. Altomonte J, Marozin S, Schmid RM, Ebert O. Engineered newcastle disease virus as an improved oncolytic agent against hepatocellular carcinoma. Mol Ther 2010, 18:275-284. 10.1038/mt.2009.231, 2839313, 19809404.
77. Hong CS, Fellows W, Niranjan A, Alber S, Watkins S, Cohen JB, Glorioso JC, Grandi P. Ectopic matrix metalloproteinase-9 expression in human brain tumor cells enhances oncolytic HSV vector infection. Gene Ther 2010, 17:1200-1205. 10.1038/gt.2010.66, 3228315, 20463757.
78. Ganesh S, Gonzalez Edick M, Idamakanti N, Abramova M, Vanroey M, Robinson M, Yun CO, Jooss K. Relaxin-expressing, fiber chimeric oncolytic adenovirus prolongs survival of tumor-bearing mice. Cancer Res 2007, 67:4399-4407. 10.1158/0008-5472.CAN-06-4260, 17483354.
79. Guedan S, Rojas JJ, Gros A, Mercade E, Cascallo M, Alemany R. Hyaluronidase expression by an oncolytic adenovirus enhances its intratumoral spread and suppresses tumor growth. Mol Ther 2010, 18:1275-1283. 10.1038/mt.2010.79, 2911260, 20442708.
80. Kuriyama N, Kuriyama H, Julin CM, Lamborn K, Israel MA. Pretreatment with protease is a useful experimental strategy for enhancing adenovirus-mediated cancer gene therapy. Hum Gene Ther 2000, 11:2219-2230. 10.1089/104303400750035744, 11084679.
81. McKee TD, Grandi P, Mok W, Alexandrakis G, Insin N, Zimmer JP, Bawendi MG, Boucher Y, Breakefield XO, Jain RK. Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 2006, 66:2509-2513. 10.1158/0008-5472.CAN-05-2242, 16510565.
82. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000, 60:2497-2503.
83. Fujiwara S, Nawa A, Luo C, Kamakura M, Goshima F, Kondo C, Kiyono T, Kikkawa F, Nishiyama Y. Carrier cell-based delivery of replication-competent HSV-1 mutants enhances antitumor effect for ovarian cancer. Cancer Gene Ther 2011, 18:77-86. 10.1038/cgt.2010.53, 3025316, 20885447.
84. Komarova S, Kawakami Y, Stoff-Khalili MA, Curiel DT, Pereboeva L. Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol Cancer Ther 2006, 5:755-766. 10.1158/1535-7163.MCT-05-0334, 16546991.
85. Thorne SH, Contag CH. Integrating the biological characteristics of oncolytic viruses and immune cells can optimize therapeutic benefits of cell-based delivery. Gene Ther 2008, 15:753-758. 10.1038/gt.2008.42, 18356814.
86. Ong HT, Hasegawa K, Dietz AB, Russell SJ, Peng KW. Evaluation of T cells as carriers for systemic measles virotherapy in the presence of antiviral antibodies. Gene Ther 2007, 14:324-333. 10.1038/sj.gt.3302880, 17051248.
87. Hakkarainen T, Sarkioja M, Lehenkari P, Miettinen S, Ylikomi T, Suuronen R, Desmond RA, Kanerva A, Hemminki A. Human mesenchymal stem cells lack tumor tropism but enhance the antitumor activity of oncolytic adenoviruses in orthotopic lung and breast tumors. Hum Gene Ther 2007, 18:627-641. 10.1089/hum.2007.034, 17604566.
88. Stoff-Khalili MA, Rivera AA, Mathis JM, Banerjee NS, Moon AS, Hess A, Rocconi RP, Numnum TM, Everts M, Chow LT, et al. Mesenchymal stem cells as a vehicle for targeted delivery of CRAds to lung metastases of breast carcinoma. Breast Cancer Res Treat 2007, 105:157-167. 10.1007/s10549-006-9449-8, 17221158.
89. Coukos G, Makrigiannakis A, Kang EH, Caparelli D, Benjamin I, Kaiser LR, Rubin SC, Albelda SM, Molnar-Kimber KL. Use of carrier cells to deliver a replication-selective herpes simplex virus-1 mutant for the intraperitoneal therapy of epithelial ovarian cancer. Clin Cancer Res 1999, 5:1523-1537.
90. Power AT, Bell JC. Cell-based delivery of oncolytic viruses: a new strategic alliance for a biological strike against cancer. Mol Ther 2007, 15:660-665.
91. Hamada K, Desaki J, Nakagawa K, Zhang T, Shirakawa T, Gotoh A, Tagawa M. Carrier cell-mediated delivery of a replication-competent adenovirus for cancer gene therapy. Mol Ther 2007, 15:1121-1128.
92. Iankov ID, Blechacz B, Liu C, Schmeckpeper JD, Tarara JE, Federspiel MJ, Caplice N, Russell SJ. Infected cell carriers: a new strategy for systemic delivery of oncolytic measles viruses in cancer virotherapy. Mol Ther 2007, 15:114-122. 10.1038/sj.mt.6300020, 17164782.
93. Alcayaga-Miranda F, Cascallo M, Rojas JJ, Pastor J, Alemany R. Osteosarcoma cells as carriers to allow antitumor activity of canine oncolytic adenovirus in the presence of neutralizing antibodies. Cancer Gene Ther 2010, 17:792-802. 10.1038/cgt.2010.36, 20671769.
94. MacTavish H, Diallo JS, Huang B, Stanford M, Le Boeuf F, De Silva N, Cox J, Simmons JG, Guimond T, Falls T, et al. Enhancement of vaccinia virus based oncolysis with histone deacetylase inhibitors. PLoS One 2010, 5:e14462. 10.1371/journal.pone.0014462, 3012680, 21283510.
95. Advani SJ, Markert JM, Sood RF, Samuel S, Gillespie GY, Shao MY, Roizman B, Weichselbaum RR. Increased oncolytic efficacy for high-grade gliomas by optimal integration of ionizing radiation into the replicative cycle of HSV-1. Gene Ther 2011,
96. Le Boeuf F, Diallo JS, McCart JA, Thorne S, Falls T, Stanford M, Kanji F, Auer R, Brown CW, Lichty BD, et al. Synergistic interaction between oncolytic viruses augments tumor killing. Mol Ther 2010, 18:888-895. 10.1038/mt.2010.44, 2890112, 20234341.
97. Breitbach CJ, De Silva NS, Falls TJ, Aladl U, Evgin L, Paterson J, Sun YY, Roy DG, Rintoul JL, Daneshmand M, et al. Targeting tumor vasculature with an oncolytic virus. Mol Ther 2011, 19:886-894. 10.1038/mt.2011.26, 21364541.
98. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 2005, 23:1011-1027.
99. Guse K, Sloniecka M, Diaconu I, Ottolino-Perry K, Tang N, Ng C, Le Boeuf F, Bell JC, McCart JA, Ristimaki A, et al. Antiangiogenic arming of an oncolytic vaccinia virus enhances antitumor efficacy in renal cell cancer models. J Virol 2010, 84:856-866. 10.1128/JVI.00692-09, 2798339, 19906926.
100. Frentzen A, Yu YA, Chen N, Zhang Q, Weibel S, Raab V, Szalay AA. Anti-VEGF single-chain antibody GLAF-1 encoded by oncolytic vaccinia virus significantly enhances antitumor therapy. Proc Natl Acad Sci USA 2009, 106:12915-12920. 10.1073/pnas.0900660106, 2722284, 19617539.
101. Qiu CW, Lin DG, Wang JQ, Li CY, Deng GZ. Expression and significance of PTEN and VEGF in canine mammary gland tumours. Vet Res Commun 2008, 32:463-472. 10.1007/s11259-008-9049-7, 18461467.
102. Platt SR, Scase TJ, Adams V, Wieczorek L, Miller J, Adamo F, Long S. Vascular endothelial growth factor expression in canine intracranial meningiomas and association with patient survival. J Vet Intern Med 2006, 20:663-668. 10.1111/j.1939-1676.2006.tb02912.x, 16734105.
103. Al-Dissi AN, Haines DM, Singh B, Kidney BA. Immunohistochemical expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 in canine simple mammary gland adenocarcinomas. Can Vet J 2010, 51:1109-1114. 2942048, 21197202.
104. Mederle O, Mederle N, Bocan EV, Ceausu R, Raica M. VEGF expression in dog mastocytoma. Rev Med Chir Soc Med Nat Iasi 2010, 114:185-188.
105. Amorim RL, Pinczowski P, Neto RT, Rahal SC. Immunohistochemical evaluation of prostaglandin E2 and vascular endothelial growth factor in canine cutaneous mast cell tumours. Vet Comp Oncol 2010, 8:23-27. 10.1111/j.1476-5829.2009.00202.x, 20230578.
106. de Queiroz GF, Dagli ML, Fukumasu H, Zavala AA, Matera JM. Vascular endothelial growth factor expression and microvascular density in soft tissue sarcomas in dogs. J Vet Diagn Invest 2010, 22:105-108. 10.1177/104063871002200121, 20093695.
107. Blackwood L, O'Shaughnessy PJ, Reid SW, Argyle DJ. E. coli nitroreductase/CB1954: in vitro studies into a potential system for feline cancer gene therapy. Vet J 2001, 161:269-279. 10.1053/tvjl.2000.0557, 11352484.
108. Hlavaty J, Jandl G, Liszt M, Petznek H, Konig-Schuster M, Sedlak J, Egerbacher M, Weissenberger J, Salmons B, Gunzburg WH, Renner M. Comparative evaluation of preclinical in vivo models for the assessment of replicating retroviral vectors for the treatment of glioblastoma. J Neurooncol 2011, 102:59-69. 10.1007/s11060-010-0295-5, 20623247.
109. Touchefeu Y, Vassaux G, Harrington KJ. Oncolytic viruses in radiation oncology. Radiother Oncol 2011, 99:262-270. 10.1016/j.radonc.2011.05.078, 21704402.
110. Wennier ST, Liu J, McFadden G. Bugs and Drugs: Oncolytic Virotherapy in Combination with Chemotherapy. Curr Pharm Biotechnol 2011,
111. Woo Y, Adusumilli PS, Fong Y. Advances in oncolytic viral therapy. Curr Opin Investig Drugs 2006, 7:549-559.
112. Vile R, Ando D, Kirn D. The oncolytic virotherapy treatment platform for cancer: unique biological and biosafety points to consider. Cancer Gene Ther 2002, 9:1062-1067. 10.1038/sj.cgt.7700548, 12522445.
113. Khanna C, Lindblad-Toh K, Vail D, London C, Bergman P, Barber L, Breen M, Kitchell B, McNeil E, Modiano JF, et al. The dog as a cancer model. Nat Biotechnol 2006, 24:1065-1066.
114. Vail DM, MacEwen EG. Spontaneously occurring tumors of companion animals as models for human cancer. Cancer Invest 2000, 18:781-792. 10.3109/07357900009012210, 11107448.
115. Hansen K, Khanna C. Spontaneous and genetically engineered animal models; use in preclinical cancer drug development. Eur J Cancer 2004, 40:858-880. 10.1016/j.ejca.2003.11.031, 15120042.
116. Genelhu MC, Cardoso SV, Gobbi H, Cassali GD. A comparative study between mixed-type tumours from human salivary and canine mammary glands. BMC Cancer 2007, 7:218. 10.1186/1471-2407-7-218, 2233636, 18045453.
117. Hayes HM, Fraumeni JF. Epidemiological features of canine renal neoplasms. Cancer Res 1977, 37:2553-2556.
118. Bukowski JA, Wartenberg D, Goldschmidt M. Environmental causes for sinonasal cancers in pet dogs, and their usefulness as sentinels of indoor cancer risk. J Toxicol Environ Health A 1998, 54:579-591. 10.1080/009841098158719, 9726781.
119. Rivera P, von Euler H. Molecular biological aspects on canine and human mammary tumors. Vet Pathol 2011, 48:132-146. 10.1177/0300985810387939, 21147766.
120. Wildner O, Hoffmann D, Jogler C, Uberla K. 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. 10.1038/sj.cgt.7700638, 14502232.
121. Hallden G, Hill R, Wang Y, Anand A, Liu TC, Lemoine NR, Francis J, Hawkins L, Kirn D. Novel immunocompetent murine tumor models for the assessment of replication-competent oncolytic adenovirus efficacy. Mol Ther 2003, 8:412-424. 10.1016/S1525-0016(03)00199-0, 12946314.
122. Wang Y, Hallden G, Hill R, Anand A, Liu TC, Francis J, Brooks G, Lemoine N, Kirn D. E3 gene manipulations affect oncolytic adenovirus activity in immunocompetent tumor models. Nat Biotechnol 2003, 21:1328-1335. 10.1038/nbt887, 14555956.
123. Withrow SJ, Powers BE, Straw RC, Wilkins RM. Comparative aspects of osteosarcoma. Dog versus man. Clin Orthop Relat Res 1991, 159-168.
124. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ, Zody MC, et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 2005, 438:803-819. 10.1038/nature04338, 16341006.