Double trouble for tumours: Exploiting the tumour microenvironment to enhance anticancer effect of oncolytic viruses

Cytokine and Growth Factor Reviews

Volumn 21, Issue 2-3, 2010, Pages 135-141

  De Silva, Naomi ^a,b   Atkins, Harold ^b   Kirn, David H ^c   Bell, John C ^a,b,c   Breitbach, Caroline J ^c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c Jennerex Biotherapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; COLLAGENASE; CYCLOPHOSPHAMIDE; ENDOSTATIN; FIBROBLAST GROWTH FACTOR; GAMMA INTERFERON; GLYCOSAMINOGLYCAN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HISTONE DEACETYLASE INHIBITOR; HYALURONIDASE; INTERLEUKIN 15; INTERLEUKIN 18; JX 594; ONCOLYTIC VIRUS; SHORT HAIRPIN RNA; THROMBOCYTE FACTOR 4; THROMBOSPONDIN; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADENOVIRUS; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; CANCER CELL; CLINICAL TRIAL; CYTOKINE PRODUCTION; CYTOLYSIS; DRUG TARGETING; EXTRACELLULAR MATRIX; GLIOMA; HERPES SIMPLEX VIRUS 1; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LIVER CELL CARCINOMA; MALIGNANT NEOPLASTIC DISEASE; MEDICAL LITERATURE; MYXOMA VIRUS; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRUS TRANSMISSION; ANIMAL; CLINICAL TRIAL (TOPIC); GENETICS; IMMUNOLOGY; NEOPLASMS; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNITY, INNATE; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; TREATMENT OUTCOME;

EID: 77953543001     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2010.02.007     Document Type: Review

References (62)

1. Stanford M.M., Breitbach C.J., Bell J.C., McFadden G. Innate immunity, tumor microenvironment and oncolytic virus therapy: friends or foes?. Curr Opin Mol Ther 2008, 10(February (1)):32-37.
2. Power A.T., Bell J.C. Cell-based delivery of oncolytic viruses: a new strategic alliance for a biological strike against cancer. Mol Ther 2007, 15(April (4)):660-665.
3. Alemany R., Suzuki K., Curiel D.T. Blood clearance rates of adenovirus type 5 in mice. J Gen Virol 2000, 81(November (Pt 11)):2605-2609.
4. Shayakhmetov D.M., Li Z.Y., Ni S., Lieber A. Analysis of adenovirus sequestration in the liver, transduction of hepatic cells, and innate toxicity after injection of fiber-modified vectors. J Virol 2004, 78(May (10)):5368-5381.
5. Power A.T., Wang J., Falls T.J., Paterson J.M., Parato K.A., Lichty B.D., et al. Carrier cell-based delivery of an oncolytic virus circumvents antiviral immunity. Mol Ther 2007, 15(January (1)):123-130.
6. Dvorak H.F. Rous-Whipple Award Lecture. How tumors make bad blood vessels and stroma. Am J Pathol 2003, 162(June (6)):1747-1757.
7. Jain R.K., Munn L.L., Fukumura D. Dissecting tumour pathophysiology using intravital microscopy. Nat Rev Cancer 2002, 2(April (4)):266-276.
8. Vaha-Koskela M.J., Heikkila J.E., Hinkkanen A.E. Oncolytic viruses in cancer therapy. Cancer Lett 2007, 254(September (2)):178-216.
9. Stanford M.M., Shaban M., Barrett J.W., Werden S.J., Gilbert P.A., Bondy-Denomy J., et al. Myxoma virus oncolysis of primary and metastatic B16F10 mouse tumors in vivo. Mol Ther 2008, 16(January (1)):52-59.
10. Shayakhmetov D.M., Li Z.Y., Ni S., Lieber A. Targeting of adenovirus vectors to tumor cells does not enable efficient transduction of breast cancer metastases. Cancer Res 2002, 62(February (4)):1063-1068.
11. Valyi-Nagy K., Dosa S., Kovacs S.K., Bacsa S., Voros A., Shukla D., et al. Identification of virus resistant tumor cell subpopulations in three-dimensional uveal melanoma cultures. Cancer Gene Ther 2009, (November).
12. Kaur B., Cripe T.P., Chiocca E.A. Buy one get one free": armed viruses for the treatment of cancer cells and their microenvironment. Curr Gene Ther 2009, 9(October (5)):341-355.
13. Mok W., Boucher Y., Jain R.K. Matrix metalloproteinases-1 and -8 improve the distribution and efficacy of an oncolytic virus. Cancer Res 2007, 67(November (22)):10664-10668.
14. McKee T.D., Grandi P., Mok W., Alexandrakis G., Insin N., Zimmer J.P., et al. Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 2006, 66(March (5)):2509-2513.
15. Ganesh S., Gonzalez-Edick M., Gibbons D., Van Roey M., Jooss K. Intratumoral coadministration of hyaluronidase enzyme and oncolytic adenoviruses enhances virus potency in metastatic tumor models. Clin Cancer Res 2008, 14(June (12)):3933-3941.
16. Kim J.H., Lee Y.S., Kim H., Huang J.H., Yoon A.R., Yun C.O. Relaxin expression from tumor-targeting adenoviruses and its intratumoral spread, apoptosis induction, and efficacy. J Natl Cancer Inst 2006, 98(October (20)):1482-1493.
17. Nagano S., Perentes J.Y., Jain R.K., Boucher Y. Cancer cell death enhances the penetration and efficacy of oncolytic herpes simplex virus in tumors. Cancer Res 2008, 68(May (10)):3795-3802.
18. Tong R.T., Boucher Y., Kozin S.V., Winkler F., Hicklin D.J., Jain R.K. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res 2004, 64(June (11)):3731-3736.
19. Libertini S., Iacuzzo I., Perruolo G., Scala S., Ierano C., Franco R., et al. Bevacizumab increases viral distribution in human anaplastic thyroid carcinoma xenografts and enhances the effects of E1A-defective adenovirus dl922-947. Clin Cancer Res 2008, 14(October (20)):6505-6514.
20. Kurozumi K., Hardcastle J., Thakur R., Yang M., Christoforidis G., Fulci G., et al. Effect of tumor microenvironment modulation on the efficacy of oncolytic virus therapy. J Natl Cancer Inst 2007, 99(December (23)):1768-1781.
21. Kurozumi K., Hardcastle J., Thakur R., Shroll J., Nowicki M., Otsuki A., et al. Oncolytic HSV-1 infection of tumors induces angiogenesis and upregulates CYR61. Mol Ther 2008, 16(August (8)):1382-1391.
22. Aghi M., Rabkin S.D., Martuza R.L. Angiogenic response caused by oncolytic herpes simplex virus-induced reduced thrombospondin expression can be prevented by specific viral mutations or by administering a thrombospondin-derived peptide. Cancer Res 2007, 67(January (2)):440-444.
23. Tseng J.C., Granot T., Digiacomo V., Levin B., Meruelo D. Enhanced specific delivery and targeting of oncolytic Sindbis viral vectors by modulating vascular leakiness in tumor. Cancer Gene Ther 2009, (October).
24. Mahller Y.Y., Vaikunth S.S., Ripberger M.C., Baird W.H., Saeki Y., Cancelas J.A., et al. Tissue inhibitor of metalloproteinase-3 via oncolytic herpesvirus inhibits tumor growth and vascular progenitors. Cancer Res 2008, 68(February (4)):1170-1179.
25. Kang Y.A., Shin H.C., Yoo J.Y., Kim J.H., Kim J.S., Yun C.O. Novel cancer antiangiotherapy using the VEGF promoter-targeted artificial zinc-finger protein and oncolytic adenovirus. Mol Ther 2008, 16(June (6)):1033-1040.
26. Yoo J.Y., Kim J.H., Kwon Y.G., Kim E.C., Kim N.K., Choi H.J., et al. VEGF-specific short hairpin RNA-expressing oncolytic adenovirus elicits potent inhibition of angiogenesis and tumor growth. Mol Ther 2007, 15(February (2)):295-302.
27. Su C., Na M., Chen J., Wang X., Liu Y., Wang W., et al. Gene-viral cancer therapy using dual-regulated oncolytic adenovirus with antiangiogenesis gene for increased efficacy. Mol Cancer Res 2008, 6(April (4)):568-575.
28. Mullen J.T., Donahue J.M., Chandrasekhar S., Yoon S.S., Liu W., Ellis L.M., et al. Oncolysis by viral replication and inhibition of angiogenesis by a replication-conditional herpes simplex virus that expresses mouse endostatin. Cancer 2004, 101(August (4)):869-877.
29. Liu T.C., Zhang T., Fukuhara H., Kuroda T., Todo T., Canron X., et al. Dominant-negative fibroblast growth factor receptor expression enhances antitumoral potency of oncolytic herpes simplex virus in neural tumors. Clin Cancer Res 2006, 12(November (22)):6791-6799.
30. Liu T.C., Zhang T., Fukuhara H., Kuroda T., Todo T., Martuza R.L., et al. Oncolytic HSV armed with platelet factor 4, an antiangiogenic agent, shows enhanced efficacy. Mol Ther 2006, 14(December (6)):789-797.
31. Hardcastle J., Kurozumi K., Dmitrieva N., Sayers M.P., Ahmad S., Waterman P., et al. Enhanced antitumor efficacy of vasculostatin (Vstat120) expressing oncolytic HSV-1. Mol Ther 2009, (October).
32. Frentzen A., Yu Y.A., Chen N., Zhang Q., Weibel S., Raab V., et al. Anti-VEGF single-chain antibody GLAF-1 encoded by oncolytic vaccinia virus significantly enhances antitumor therapy. Proc Natl Acad Sci USA 2009, 106(August (31)):12915-12920.
33. Breitbach C.J., Paterson J.M., Lemay C.G., Falls T.J., McGuire A., Parato K.A., et al. Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow. Mol Ther 2007, 15(September (9)):1686-1693.
34. Fulci G., Dmitrieva N., Gianni D., Fontana E.J., Pan X., Lu Y., et al. Depletion of peripheral macrophages and brain microglia increases brain tumor titers of oncolytic viruses. Cancer Res 2007, 67(October (19)):9398-9406.
35. Shashkova E.V., Doronin K., Senac J.S., Barry M.A. Macrophage depletion combined with anticoagulant therapy increases therapeutic window of systemic treatment with oncolytic adenovirus. Cancer Res 2008, 68(July (14)):5896-5904.
36. Tao N., Gao G.P., Parr M., Johnston J., Baradet T., Wilson J.M., et al. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol Ther 2001, 3(January (1)):28-35.
37. Altomonte J., Wu L., Chen L., Meseck M., Ebert O., Garcia-Sastre A., et al. Exponential enhancement of oncolytic vesicular stomatitis virus potency by vector-mediated suppression of inflammatory responses in vivo. Mol Ther 2008, 16(January (1)):146-153.
38. Altomonte J., Wu L., Meseck M., Chen L., Ebert O., Garcia-Sastre A., et al. Enhanced oncolytic potency of vesicular stomatitis virus through vector-mediated inhibition of NK and NKT cells. Cancer Gene Ther 2008, (October).
39. Fulci G., Breymann L., Gianni D., Kurozomi K., Rhee S.S., Yu J., et al. Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses. Proc Natl Acad Sci USA 2006, 103(August (34)):12873-12878.
40. Wakimoto H., Fulci G., Tyminski E., Chiocca E.A. Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis. Gene Ther 2004, 11(January (2)):214-223.
41. Qiao J., Wang H., Kottke T., White C., Twigger K., Diaz R.M., et al. Cyclophosphamide facilitates antitumor efficacy against subcutaneous tumors following intravenous delivery of reovirus. Clin Cancer Res 2008, 14(January (1)):259-269.
42. Currier M.A., Gillespie R.A., Sawtell N.M., Mahller Y.Y., Stroup G., Collins M.H., et al. Efficacy and safety of the oncolytic herpes simplex virus rRp450 alone and combined with cyclophosphamide. Mol Ther 2008, 16(May (5)):879-885.
43. Kirn D.H., Wang Y., Le Boeuf F., Bell J., Thorne S.H. Targeting of interferon-beta to produce a specific, multi-mechanistic oncolytic vaccinia virus. PLoS Med 2007, 4(December (12)):e353.
44. Benencia F., Courreges M.C., Conejo-Garcia J.R., Mohamed-Hadley A., Zhang L., Buckanovich R.J., et al. HSV oncolytic therapy upregulates interferon-inducible chemokines and recruits immune effector cells in ovarian cancer. Mol Ther 2005, 12(November (5)):789-802.
45. Errington F., White C.L., Twigger K.R., Rose A., Scott K., Steele L., et al. Inflammatory tumour cell killing by oncolytic reovirus for the treatment of melanoma. Gene Ther 2008, 15(September (18)):1257-1270.
46. Post D.E., Sandberg E.M., Kyle M.M., Devi N.S., Brat D.J., Xu Z., et al. Targeted cancer gene therapy using a hypoxia inducible factor dependent oncolytic adenovirus armed with interleukin-4. Cancer Res 2007, 67(July (14)):6872-6881.
47. Shin E.J., Wanna G.B., Choi B., Aguila D., Ebert O., Genden E.M., et al. Interleukin-12 expression enhances vesicular stomatitis virus oncolytic therapy in murine squamous cell carcinoma. Laryngoscope 2007, 117(February (2)):210-214.
48. Stanford M.M., Barrett J.W., Gilbert P.A., Bankert R., McFadden G. Myxoma virus expressing human interleukin-12 does not induce myxomatosis in European rabbits. J Virol 2007, 81(November (22)):12704-12708.
49. Varghese S., Rabkin S.D., Nielsen P.G., Wang W., Martuza R.L. Systemic oncolytic herpes virus therapy of poorly immunogenic prostate cancer metastatic to lung. Clin Cancer Res 2006, 12(May (9)):2919-2927.
50. Wong R.J., Chan M.K., Yu Z., Ghossein R.A., Ngai I., Adusumilli P.S., et al. Angiogenesis inhibition by an oncolytic herpes virus expressing interleukin 12. Clin Cancer Res 2004, 10(July (13)):4509-4516.
51. Varghese S., Rabkin S.D., Nielsen G.P., MacGarvey U., Liu R., Martuza R.L. Systemic therapy of spontaneous prostate cancer in transgenic mice with oncolytic herpes simplex viruses. Cancer Res 2007, 67(October (19)):9371-9379.
52. Ramesh N., Ge Y., Ennist D.L., Zhu M., Mina M., Ganesh S., 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(January (1)):305-313.
53. Grote D., Cattaneo R., Fielding A.K. Neutrophils contribute to the measles virus-induced antitumor effect: enhancement by granulocyte macrophage colony-stimulating factor expression. Cancer Res 2003, 63(October (19)):6463-6468.
54. Janke M., Peeters B., de Leeuw O., Moorman R., Arnold A., Fournier P., et al. Recombinant Newcastle disease virus (NDV) with inserted gene coding for GM-CSF as a new vector for cancer immunogene therapy. Gene Ther 2007, 14(December (23)):1639-1649.
55. Prestwich R.J., Errington F., Steele L.P., Ilett E.J., Morgan R.S., Harrington K.J., et al. Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J Immunol 2009, 183(October (7)):4312-4321.
56. Nguyen T.L., Abdelbary H., Arguello M., Breitbach C., Leveille S., Diallo J.S., et al. Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc Natl Acad Sci USA 2008, 105(September (39)):14981-14986.
57. Liu T.C., Castelo-Branco P., Rabkin S.D., Martuza R.L. Trichostatin A and oncolytic HSV combination therapy shows enhanced antitumoral and antiangiogenic effects. Mol Ther 2008, 16(June (6)):1041-1047.
58. Liu T.C., Galanis E., Kirn D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol 2007, 4(February (2)):101-117.
59. Park B.H., Hwang T., Liu T.C., Sze D.Y., Kim J.S., Kwon H.C., 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(June (6)):533-542.
60. Senzer N.N., Kaufman H.L., Amatruda T., Nemunaitis M., Reid T., Daniels G., et al. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol 2009, 27(December (34)):5763-5771.
61. Liu T.C., Hwang T., Park B.H., Bell J., Kirn D.H. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther 2008, 16(September (9)):1637-1642.
62. Ruegg C., Yilmaz A., Bieler G., Bamat J., Chaubert P., Lejeune F.J. Evidence for the involvement of endothelial cell integrin alphaVbeta3 in the disruption of the tumor vasculature induced by TNF and IFN-gamma. Nat Med 1998, 4(April (4)):408-414.