Reovirus exerts potent oncolytic effects in head and neck cancer cell lines that are independent of signalling in the EGFR pathway

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Twigger, Katie ^a   Roulstone, Victoria ^a   Kyula, Joan ^a   Karapanagiotou, Eleni M ^a   Syrigos, Konstantinos N ^b   Morgan, Richard ^c   White, Christine ^a   Bhide, Shreerang ^a   Nuovo, Gerard ^d   Coffey, Matt ^e   Thompson, Brad ^e   Jebar, Adel ^f   Errington, Fiona ^f   Melcher, Alan A ^f   Vile, Richard G ^f,g   Pandha, Hardev S ^c   Harrington, Kevin J ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b SOTIRIA GENERAL HOSPITAL   (Greece)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d OHIO STATE UNIVERSITY   (United States)

^e ONCOLYTICS BIOTECH INC   (Canada)

^f UNIVERSITY OF LEEDS   (United Kingdom)

^g MAYO CLINIC   (United States)

Author keywords

Biomarker; Cancer; EGFR; Oncolytic virus; Ras; Reovirus

Indexed keywords

2 AMINOPURINE; ALPHA INTERFERON; BETA INTERFERON; CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; ONCOLYTIC REOVIRUS; ONCOLYTIC VIRUS; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE R; RAS PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL ASSAY; CELL KILLING; CELL SURVIVAL; CELL TRANSPORT; CHEMOSENSITIVITY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXICITY; ENZYME DEGRADATION; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; IC 50; INHIBITION KINETICS; ONCOLYTIC VIROTHERAPY; PREDICTION; REOVIRUS; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; VIROGENESIS; VIRUS PARTICLE; VIRUS VIRULENCE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE, TUMOR; FLOW CYTOMETRY; HEAD AND NECK NEOPLASMS; HUMANS; ONCOLYTIC VIRUSES; RECEPTOR, EPIDERMAL GROWTH FACTOR; REOVIRIDAE; REOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION;

EID: 84865287313     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-368     Document Type: Article

References (43)

1. Rosen L, Evans HE, Spickard A. Reovirus infections in human volunteers. Am J Hyg 1963, 77:29-37.
2. Selb B, Weber B. A study of human reovirus IgG and IgA antibodies by ELISA and western blot. J Virol Methods 1994, 47:15-25. 10.1016/0166-0934(94)90062-0, 8051222.
3. Tai JH, Williams JV, Edwards KM, Wright PF, Crowe JE, et al. Prevalence of reovirus-specific antibodies in young children in Nashville, Tennessee. J Infect Dis 2005, 191:1221-1224. 10.1086/428911, 15776366.
4. Hashiro G, Loh PC, Yau YT. The preferential cytotoxicity of reovirus for certain transformed cell lines. Arch Virol 1977, 54:307-315. 10.1007/BF01314776, 562142.
5. Duncan MR, Stanish SM, Cox DC. Differential sensitivity of normal and transformed human cells to reovirus infection. J Virol 1978, 28:444-449. 354293, 214572.
6. Strong JE, Lee PWK. The v-erbB oncogene confers enhanced cellular susceptibility to reovirus infection. J Virol 1996, 70:612-616. 189854, 8523580.
7. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 1998, 17:3351-62. 10.1093/emboj/17.12.3351, 1170673, 9628872.
8. Coffey MC, Strong JE, Forsyth PA, Lee PW. Reovirus therapy of tumors with activated Ras pathway. Science 1998, 282:1332-1334.
9. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW. Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc Natl Acad Sci U S A 2004, 101:11099-11104. 10.1073/pnas.0404310101, 503746, 15263068.
10. Errington F, White CL, Twigger KR, Rose A, Scott K, et al. Inflammatory tumour cell killing by oncolytic reovirus for the treatment of melanoma. Gene Ther 2008, 15:1257-70. 10.1038/gt.2008.58, 18401435.
11. Smakman N, van den Wollenberg DJ, Borel Rinkes IH, Hoeben RC, Kranenburg O. Sensitization to apoptosis underlies KrasD12-dependent oncolysis of murine C26 colorectal carcinoma cells by reovirus T3D. J Virol 2005, 79:14981-14985. 10.1128/JVI.79.23.14981-14985.2005, 1287595, 16282499.
12. Marcato P, Shmulevitz M, Pan D, Stoltz D, Lee PW. Ras transformation mediates reovirus oncolysis by enhancing virus uncoating, particle infectivity, and apoptosis-dependent release. Mol Ther 2007, 15:1522-1530. 10.1038/sj.mt.6300179, 17457318.
13. Comins C, Heinemann L, Harrington K, Melcher A, De Bono J, et al. Reovirus: viral therapy for cancer " as nature intended" Clin Oncol (R. Coll. Radiol.) 2008, 20:548-554.
14. Yap TA, Brunetto A, Pandha H, Harrington K, De Bono JS. Reovirus to Reolysin: progress from the laboratory to the clinic. Exp Opin Investig Drugs 2008, 17:1925-1935.
15. Forsyth P, Roldan G, George D, Wallace C, Palmer CA, 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. 10.1038/sj.mt.6300403, 18253152.
16. Vidal L, Pandha HS, Yap TA, White CL, Twigger K, 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. 10.1158/1078-0432.CCR-08-0524, 18981012.
17. Gollamudi R, Ghalib MH, Desai KK, Chaudhary I, Wong B, et al. Intravenous administration of Reolysin, a live replication competent RNA virus is safe in patients with advanced solid tumors. Invest New Drugs 2010, 28:641-649. 10.1007/s10637-009-9279-8, 19572105.
18. Comins C, Spicer J, Protheroe A, Roulstone V, Twigger K, et al. REO-10: A phase I study of intravenous Reovirus and docetaxel in patients with advanced cancer. Clin Cancer Res 2010, 16:5564-5572. 10.1158/1078-0432.CCR-10-1233, 20926400.
19. Lolkema MP, Arkenau HT, Harrington K, Roxburgh P, Morrison R, et al. A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer. Clin Cancer Res 2011, 17:581-588. 10.1158/1078-0432.CCR-10-2159, 21106728.
20. Karapanagiotou E, et al. Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malihnancies. Clin Cancer Res 2012, [Epub ahead of print].
21. Harrington KJ, Karapanagiotou EM, Roulstone V, Twigger KR, White CL, et al. Two-stage phase I dose-escalation study of intratumoral reovirus type 3 dearing and palliative radiotherapy in patients with advanced cancers. Clin Cancer Res 2010, 16:3067-3077. 10.1158/1078-0432.CCR-10-0054, 20484020.
22. Rogers SJ, Harrington KJ, Rhys-Evans P, Eccles SA. Biological significance of c-erbB family oncogenes in head and neck cancer. Cancer Metast Rev 2005, 24:47-69.
23. Bonner JA, Harari PM, Giralt J, Cohen RB, Jones CU, 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. 10.1016/S1470-2045(09)70311-0, 19897418.
24. Vermorken JB, Mesia R, Rivera F, Remenar E, Kawecki A, et al. Platinum-based chemotherapy plus cetuximab in head and neck cancer. N Engl J Med 2008, 359:1116-1127. 10.1056/NEJMoa0802656, 18784101.
25. O-Charoenrat P, Rhys-Evans P, Eccles S. Characterization of ten newly-derived human head and neck squamous carcinoma cell lines with special reference to c-erbB proto-oncogene expression. Anticancer Res 2001, 21(3B):1953-63.
26. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, et al. Junction adhesion molecule is a receptor for reovirus. Cell 2001, 104:441-451. 10.1016/S0092-8674(01)00231-8, 11239401.
27. Chandran K, Walker SB, Chen Y, Contreras CM, Schiff LA, et al. In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins mu1 and sigma3. J Virol 1999, 73:3941-3950. 104172, 10196289.
28. Alain T, Kim TS, Lun X, Liacini A, Schiff LA, et al. Proteolytic disassembly is a critical determinant for reovirus oncolysis. Mol Ther 2007, 15:1512-1521. 10.1038/sj.mt.6300207, 17519890.
29. Modjtahedi H, Eccles SA, Box G, Styles J, Dean CJ. Antitumor activity of combinations of antibodies directed against different epitopes on the extracellular domain of the human EGF receptor. Cell Biophys 1993, 22:129-146.
30. Rogers SJ, Box C, Chambers P, Barbachano Y, Nutting CM, et al. Determinants of response to gefitinib in squamous cell carcinoma of the head and neck. J Path 2009, 218:122-130. 10.1002/path.2515, 19197951.
31. Sebolt-Leopold JS, Dudley DT, Herrera R, Van Becelaere K, Wiland A, et al. Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat Med 1999, 5:810-816. 10.1038/10533, 10395327.
32. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 1998, 273:18623-18632. 10.1074/jbc.273.29.18623, 9660836.
33. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994, 269:5241-5248.
34. Young PR, McLaughlin MM, Kumar S, Kassis S, Doyle ML, et al. Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site. J Biol Chem 1997, 272:12116-12121. 10.1074/jbc.272.18.12116, 9115281.
35. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
36. Errington F, White CL, Twigger KR, Rose A, Scott K, Steele L, Ilett LJ, Prestwich R, Pandha HS, Coffey M, Selby P, Vile R, Harrington KJ, Melcher AA. Inflammatory tumour cell killing by oncolytic reovirus for the treatment of melanoma. Gene Ther 2008, 15:1257-70. 10.1038/gt.2008.58, 18401435.
37. Harrington KJ, Vile RG, Melcher A, Chester J, Pandha HS. Clinical trials with oncolytic reovirus: Moving beyond phase I into combinations with standard therapeutics. Cytokine Growth Factor Rev 2010, 21:91-98. 10.1016/j.cytogfr.2010.02.006, 20223697.
38. Sei S, Mussio JK, Yang QE, Nagashima K, Parchment RE, et al. Synergistic antitumor activity of oncolytic reovirus and chemotherapeutic agents in non-small cell lung cancer cells. Mol Cancer 2009, 8:47. 10.1186/1476-4598-8-47, 2723073, 19594950.
39. Pandha HS, Heinemann L, Simpson GR, Melcher A, Prestwich R, et al. Synergistic effects of oncolytic reovirus and cisplatin chemotherapy in murine malignant melanoma. Clin Cancer Res. 2009, 15:6158-6166. 10.1158/1078-0432.CCR-09-0796, 19773377.
40. Twigger K, Vidal L, White CL, De Bono JS, Bhide S, et al. Enhanced in vitro and in vivo cytotoxicity of combined reovirus and radiotherapy. Clin Cancer Res 2008, 14:912-923. 10.1158/1078-0432.CCR-07-1400, 18245555.
41. Ries SJ, Brandts CH, Chung AS, Biederer CH, Hann BC, et al. Loss of p14ARF in tumor cells facilitates replication of the adenovirus mutant dl1520 (ONYX-015). Nat Med 2000, 6:1128-1133. 10.1038/80466, 11017144.
42. Prestwich RJ, Errington F, Diaz RM, Pandha HS, Harrington KJ, Melcher AA, Vile RG. The case of oncolytic viruses versus the immune system: waiting on the judgment of Solomon. Hum Gene Ther 2009, 20:1119-1132. 10.1089/hum.2009.135, 2829276, 19630549.
43. Cassell A, Grandis JR. Investigational EGFR-targeted therapy in head and neck squamous cell carcinoma. Expert Opin Investig Drugs 2010, 19:709-722. 10.1517/13543781003769844, 2947445, 20415598.