Clinical trials with oncolytic reovirus: Moving beyond phase I into combinations with standard therapeutics

Cytokine and Growth Factor Reviews

Volumn 21, Issue 2-3, 2010, Pages 91-98

  Harrington, K J ^a   Vile, R G ^b   Melcher, A ^c   Chester, J ^c   Pandha, H S ^d  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Chemotherapy; Clinical trial; Oncolytic virus; Radiotherapy; Reovirus

Indexed keywords

ANTINEOPLASTIC AGENT; CARBOPLATIN; CETUXIMAB; CISPLATIN; CYCLOPHOSPHAMIDE; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; FLUOROURACIL; MONOCLONAL ANTIBODY; ONCOLYTIC VIRUS; ONYX 015; PACLITAXEL; PLACEBO; PROTEIN KINASE R; PROTEIN SERINE THREONINE KINASE; VIRUS ANTIBODY;

CANCER CELL CULTURE; CANCER RADIOTHERAPY; CANCER RELAPSE; CLINICAL TRIAL; CYTOTOXICITY; DISEASE FREE SURVIVAL; DNA MODIFICATION; DRUG DOSE ESCALATION; DRUG MEGADOSE; DRUG POTENTIATION; DRUG RESEARCH; DRUG SAFETY; FATIGUE; FEVER; FLU LIKE SYNDROME; GENETIC ENGINEERING; HEAD AND NECK CANCER; HEADACHE; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; METASTASIS POTENTIAL; MULTIPLE CYCLE TREATMENT; NONHUMAN; ONCOLYTIC VIROTHERAPY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROSTATE CANCER; RADIATION DOSE; RECOMMENDED DRUG DOSE; REOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; TUMOR IMMUNITY; VIRUS REPLICATION; CLINICAL TRIAL (TOPIC); GENETICS; METHODOLOGY; NEOPLASMS; PHYSIOLOGY; REOVIRIDAE;

CLINICAL TRIALS AS TOPIC; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; REOVIRIDAE; RESEARCH DESIGN;

ORTHOREOVIRUS;

EID: 77953539465     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2010.02.006     Document Type: Review

References (48)

1. Harrington K.J., Epenetos A.A. Recent developments in radioimmunotherapy. Clin Oncol (R Coll Radiol) 1994, 6:391-398.
2. Kohler G., Milstein C. Continuous culture of fused cells secreting antibodies of predefined specificity. Nature 1975, 256:495-497.
3. Jain R.K. Physiological barriers to delivery of monoclonal antibodies and other macromolecules in tumours. Cancer Res 1990, 50(Suppl.):814s-819s.
4. Courtenay-Luck N.S., Epenetos A.A., Moore R., Larche M., Pectasides D., Dhokia B., et al. Development of primary and secondary immune responses to mouse monoclonal antibodies used in the diagnosis and therapy of malignant neoplasms. Cancer Res 1986, 46:6489-6493.
5. Forni L., Coutinho A., Köhler G., Jerne N.K. IgM antibodies induce the production of antibodies of the same specificity. Proc Natl Acad Sci USA 1980, 77:1125-1128.
6. Ledermann J.A., Begent R.H., Bagshawe K.D. Cyclosporin A prevents the anti-murine antibody response to a monoclonal anti-tumour antibody in rabbits. Br J Cancer 1988, 58:562-566.
7. Ledermann J.A., Begent R.H., Massof C., Kelly A.M., Adam T., Bagshawe K.D. A phase-I study of repeated therapy with radiolabelled antibody to carcinoembryonic antigen using intermittent or continuous administration of cyclosporin A to suppress the immune response. Int J Cancer 1991, 47:659-664.
8. Prestwich R.J., Errington F., Diaz R.M., Pandha H., Harrington K.J., Melcher A.A., et al. The case of oncolytic viruses versus the immune system: waiting on the judgment of Solomon. Hum Gene Ther 2009, 20:1119-1132.
9. Ikeda K., Ichikawa T., Wakimoto H., Silver J.S., Deisboeck T.S., Finkelstein D., et al. Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses. Nat Med 1999, 5:881-887.
10. Kambara H., Saeki Y., Chiocca E.A. Cyclophosphamide allows for in vivo dose reduction of a potent oncolytic virus. Cancer Res 2005, 65:11255-11258.
11. Thomas M.A., Spencer J.F., Toth K., Sagartz J.E., Phillips N.J., Wold W.S. Immunosuppression enhances oncolytic adenovirus replication and antitumor efficacy in the Syrian hamster model. Mol Ther 2008, 16:1665-1673.
12. Qiao J., Wang H., Kottke T., White C., Twigger K., Diaz R.M., et al. Cyclophosphamide facilitates anti-tumor efficacy against subcutaneous tumors following intravenous delivery of reovirus. Clin Cancer Res 2008, 14:259-269.
13. Argyriou A.A., Kalofonos H.P. Recent advances relating to the clinical application of naked monoclonal antibodies in solid tumors. Mol Med 2009, 15:183-191.
14. Harrington K., Alvarez-Vallina L., Crittenden M., Gough M., Chong H., Diaz R.M., et al. Cells as vehicles for cancer gene therapy: the missing link between targeted vectors and systemic delivery?. Hum Gene Ther 2002, 13:1263-1280.
15. Willmon C., Harrington K., Kottke T., Prestwich R., Melcher A., Vile R. Cell carriers for oncolytic viruses: Fed Ex for cancer therapy. Mol Ther 2009, 17:1667-1676.
16. Fisher K.D., Seymour L.W. HPMA copolymers for masking and retargeting of therapeutic viruses. Adv Drug Deliv Rev 2010, 62:240-245.
17. Van Glabbeke M., Verweij J., Casali P.G., Le Cesne A., Hohenberger P., Ray-Coquard I., et al. Initial and late resistance to imatinib in advanced gastrointestinal stromal tumors are predicted by different prognostic factors: a European Organisation for Research and Treatment of Cancer-Italian Sarcoma Group-Australasian Gastrointestinal Trials Group study. J Clin Oncol 2005, 23:5795-5804.
18. Ottolino-Perry K., Diallo J.S., Lichty B.D., Bell J.C., McCart J.A. Intelligent design: combination therapy with oncolytic viruses. Mol Ther 2010, 18:251-263.
19. Bonner J.A., Harari P.M., Giralt J., Azarnia N., Shin D.M., Cohen R.B., et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med 2006, 354:567-578.
20. Bonner J.A., Harari P.M., Giralt J., Cohen R.B., Jones C.U., Sur R.K., et al. Radiotherapy plus cetuximab for locoregionally advanced head and neck cancer: 5-year survival data from a phase 3 randomised trial, and relation between cetuximab-induced rash and survival. Lancet Oncol 2010, 11:21-28.
21. Adams D.J., Ridinger D.N., Spendlove R.S., Barnett B.B. Protamine precipitation of two reovirus particle types from polluted waters. Appl Environ Microbiol 1982, 44:589-596.
22. Ridinger D.N., Spendlove R.S., Barnett B.B., George D.B., Roth J.C. Evaluation of cell lines and immunofluorescence and plaque assay procedures for quantifying reoviruses in sewage. Appl Environ Microbiol 1982, 43:740-746.
23. Rosen L., Evans H.E., Spickard A. Reovirus infections in human volunteers. Am J Hyg 1963, 77:29-37.
24. Tai J.H., Williams J.V., Edwards K.M., Wright P.F., Crowe J.E., Dermody T.S. Prevalence of reovirus-specific antibodies in young children in Nashville, Tennessee. J Infect Dis 2005, 191:1221-1224.
25. Rosen L., Hovis J.F., Mastrota F.M., Bell J.A., Huebner R.J. Observations on a newly recognized virus (Abney) of the reovirus family. Am J Hyg 1960, 71:258-265.
26. van den Wollenberg D.J., van den Hengel S.K., Dautzenberg I.J., Cramer S.J., Kranenburg O., Hoeben R.C. A strategy for genetic modification of the spike-encoding segment of human reovirus T3D for reovirus targeting. Gene Ther 2008, 15:1567-1578.
27. Hashiro G., Loh P.C., Yau J.T. The preferential cytotoxicity of reovirus for certain transformed cell lines. Arch Virol 1977, 54:307-315.
28. Strong J.E., Lee P.W. The v-erbB oncogene confers enhanced cellular susceptibility to reovirus infection. J Virol 1996, 70:612-616.
29. Coffey M.C., Strong J.E., Forsyth P.A., Lee P.W. Reovirus therapy of tumors with activated Ras pathway. Science 1998, 282:1332-1334.
30. Strong J.E., Coffey M.C., Tang D., Sabinin P., Lee P.W. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 1998, 17:3351-3362.
31. Bos J.L. ras oncogenes in human cancer: a review. Cancer Res 1989, 49:4682-4689.
32. Vorburger S.A., Pataer A., Swisher S.G., Hunt K.K. Genetically targeted cancer therapy: tumor destruction by PKR activation. Am J Pharmacogenomics 2004, 4:189-198.
33. Meurs E., Chong K., Galabru J., Thomas N.S., Kerr I.M., Williams B.R., et al. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 1990, 62:379-390.
34. Comins C., Heinemann L., Harrington K., Melcher A., De Bono J., Pandha H. Reovirus: viral therapy for cancer " as nature intended" Clin Oncol (R Coll Radiol) 2008, 20:548-554.
35. Galanis E., Hartmann L.C., Cliby W.A., Long H.J., Peethambaram P.P., Barrette B.A., et al. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res 2010, 70:875-882.
36. Morris D.G., Forsyth P.A., Paterson A.H., et al. A phase I clinical trial evaluating intralesional reolysin (reovirus) in histologically confirmed malignancies. Proc Am Soc Clin Oncol 2002.
37. Forsyth P., Roldán G., George D., Wallace C., Palmer C.A., Morris D., et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008, 16:627-632.
38. Vidal L., Pandha H.S., Yap T.A., White C.L., Twigger K., Vile R.G., et al. A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer. Clin Cancer Res 2008, 14:7127-7137.
39. White C.L., Twigger K.R., Vidal L., De Bono J.S., Coffey M., Heinemann L., et al. Characterisation of the innate, humoral and cellular immune response to intravenous oncolytic reovirus (Dearing Type 3) during a phase I clinical trial. Gene Ther 2008, 15:911-920.
40. Harrington K.J., Melcher A., Vassaux G., Pandha H.S., Vile R.G. Exploiting synergies between radiation and oncolytic viruses. Curr Opin Mol Ther 2008, 10:362-370.
41. Kumar S., Gao L., Yeagy B., Reid T. Virus combinations and chemotherapy for the treatment of human cancers. Curr Opin Mol Ther 2008, 10:371-379.
42. Zhang M., Li S., Li J., Ensminger W.D., Lawrence T.S. Ionizing radiation increases adenovirus uptake and improves transgene expression in intrahepatic colon cancer xenografts. Mol Ther 2003, 8:21-28.
43. Qian J., Yang J., Dragovic A.F., Abu-Isa E., Lawrence T.S., Zhang M. Ionizing radiation-induced adenovirus infection is mediated by Dynamin 2. Cancer Res 2005, 65:5493-5497.
44. Twigger K., Vidal L., White C.L., De Bono J.S., Bhide S., Coffey M., et al. Enhanced in vitro and in vivo cytotoxicity of combined reovirus and radiotherapy. Clin Cancer Res 2008, 14:912-923.
45. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
46. Vidal L., Twigger K., White C.L., Ahmed M., Pandha H.S., Nutting C.M., et al. Phase I trial of intratumoral administration of reovirus type 3 (Reolysin) in combination with radiation in patients with advanced malignancies. Proc Am Assoc Cancer Res 2005.
47. Khuri F.R., Nemunaitis J., Ganly I., Arseneau J., Tannock I.F., Romel L., et al. 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, 6:879-885.
48. Pandha H.S., Heinemann L., Simpson G.R., Melcher A., Prestwich R., Errington F., et al. Synergistic effects of oncolytic reovirus and cisplatin chemotherapy in murine malignant melanoma. Clin Cancer Res 2009, 15:6158-6166.