Suppression of antiviral innate immunity by sunitinib enhances oncolytic virotherapy

Molecular Therapy

Volumn 21, Issue 9, 2013, Pages 1749-1757

  Jha, Babal K ^a   Dong, Beihua ^a   Nguyen, Carvell T ^a   Polyakova, Irina ^a   Silverman, Robert H ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INITIATION FACTOR 2ALPHA; ONCOLYTIC VESICULAR STOMATITIS VIRUS; ONCOLYTIC VIRUS; PROTEIN KINASE R; RIBONUCLEASE L; SODIUM CHLORIDE; SUNITINIB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER INHIBITION; CANCER REGRESSION; CANCER SIZE; CANCER TISSUE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; DRUG SELECTIVITY; DRUG TARGETING; EMBRYO; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOCOMPETENCE; INCUBATION TIME; INNATE IMMUNITY; KIDNEY CARCINOMA; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; TREATMENT DURATION; VIRUS IMMUNITY; VIRUS LOAD;

ANIMALIA; MUS; VESICULAR STOMATITIS VIRUS;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; EIF-2 KINASE; ENDORIBONUCLEASES; FEMALE; IMMUNITY, INNATE; INDOLES; KIDNEY NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, NUDE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROSTATIC NEOPLASMS; PYRROLES; VESICULOVIRUS;

EID: 84883741789     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.112     Document Type: Article

References (50)

1. Parato, KA, Senger, D, Forsyth, PA and Bell, JC (2005). Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 5: 965-976. (Pubitemid 41766784)
2. Russell, SJ, Peng, KW and Bell, JC (2012). Oncolytic virotherapy. Nat Biotechnol 30: 658-670.
3. Wennier, ST, Liu, J and McFadden, G (2012). Bugs and drugs: oncolytic virotherapy in combination with chemotherapy. Curr Pharm Biotechnol 13: 1817-1833.
4. Echchgadda, I, Chang, TH, Sabbah, A, Bakri, I, Ikeno, Y, Hubbard, GB et al. (2011). Oncolytic targeting of androgen-sensitive prostate tumor by the respiratory syncytial virus (RSV): consequences of deficient interferon-dependent antiviral defense. BMC Cancer 11: 43.
5. Dunn, GP, Sheehan, KC, Old, LJ and Schreiber, RD (2005). IFN unresponsiveness in LNCaP cells due to the lack of JAK1 gene expression. Cancer Res 65: 3447-3453. (Pubitemid 40524631)
6. Cripe, TP, Wang, PY, Marcato, P, Mahller, YY and Lee, PW (2009). Targeting cancer-initiating cells with oncolytic viruses. Mol Ther 17: 1677-1682.
7. Mahller, YY, Williams, JP, Baird, WH, Mitton, B, Grossheim, J, Saeki, Y et al. (2009). Neuroblastoma cell lines contain pluripotent tumor initiating cells that are susceptible to a targeted oncolytic virus. PLoS ONE 4: e4235.
8. Aghi, MK, Liu, TC, Rabkin, S and Martuza, RL (2009). Hypoxia enhances the replication of oncolytic herpes simplex virus. Mol Ther 17: 51-56.
9. DeWeese, TL, van der Poel, H, Li, S, Mikhak, B, Drew, R, Goemann, M et al. (2001). A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res 61: 7464-7472. (Pubitemid 32995035)
10. Freytag, SO, Stricker, H, Pegg, J, Paielli, D, Pradhan, DG, Peabody, J et al. (2003). Phase I study of replication-competent adenovirus-mediated double-suicide gene therapy in combination with conventional-dose three-dimensional conformal radiation therapy for the treatment of newly diagnosed, intermediate-to high-risk prostate cancer. Cancer Res 63: 7497-7506. (Pubitemid 37413494)
11. Vidal, L, Pandha, HS, Yap, TA, White, CL, Twigger, K, Vile, RG et al. (2008). A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer. Clin Cancer Res 14: 7127-7137.
12. Freytag, SO, Stricker, H, Peabody, J, Pegg, J, Paielli, D, Movsas, B et al. (2007). Fiveyear follow-up of trial of replication-competent adenovirus-mediated suicide gene therapy for treatment of prostate cancer. Mol Ther 15: 636-642.
13. Lichty, BD, Power, AT, Stojdl, DF and Bell, JC (2004). Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 10: 210-216. (Pubitemid 38581793)
14. Lyles DS and Rupprecht, CE (2007). Rhabdoviridae, in Field's Virology, 5th edn., Lippincott Williams and Wilkins: Philadelphia, PA. pp. 1364-1408.
15. Stojdl, DF, Lichty, BD, tenOever, BR, Paterson, JM, Power, AT, Knowles, S et al. (2003). VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4: 263-275. (Pubitemid 37329791)
16. Ahmed, M, McKenzie, MO, Puckett, S, Hojnacki, M, Poliquin, L and Lyles, DS (2003). Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J Virol 77: 4646-4657. (Pubitemid 36402814)
17. Chang, CL, Ma, B, Pang, X, Wu, TC and Hung, CF (2009). Treatment with cyclooxygenase-2 inhibitors enables repeated administration of vaccinia virus for control of ovarian cancer. Mol Ther 17: 1365-1372.
18. Prestwich, RJ, Ilett, EJ, Errington, F, Diaz, RM, Steele, LP, Kottke, T et al. (2009). Immune-mediated antitumor activity of reovirus is required for therapy and is independent of direct viral oncolysis and replication. Clin Cancer Res 15: 4374-4381.
19. Gujar, SA, Pan, DA, Marcato, P, Garant, KA and Lee, PW (2011). Oncolytic virusinitiated protective immunity against prostate cancer. Mol Ther 19: 797-804.
20. Sadler, AJ and Williams, BR (2008). Interferon-inducible antiviral effectors. Nat Rev Immunol 8: 559-568. (Pubitemid 351913674)
21. Chakrabarti, A, Jha, BK and Silverman, RH (2011). New insights into the role of RNase L in innate immunity. J Interferon Cytokine Res 31: 49-57.
22. Jha, BK, Polyakova, I, Kessler, P, Dong, B, Dickerman, B, Sen, GC et al. (2011). Inhibition of RNase L and RNA-dependent protein kinase (PKR) by sunitinib impairs antiviral innate immunity. J Biol Chem 286: 26319-26326.
23. Kerbel, RS (2006). Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science 312: 1171-1175. (Pubitemid 43801134)
24. Silverman, RH, Skehel, JJ, James, TC, Wreschner, DH and Kerr, IM (1983). rRNA cleavage as an index of ppp(A2'p)nA activity in interferon-treated encephalomyocarditis virus-infected cells. J Virol 46: 1051-1055. (Pubitemid 13092515)
25. Motzer, RJ, Rini, BI, Bukowski, RM, Curti, BD, George, DJ, Hudes, GR et al. (2006). Sunitinib in patients with metastatic renal cell carcinoma. JAMA 295: 2516-2524. (Pubitemid 43854967)
26. George, S, Blay, JY, Casali, PG, Le Cesne, A, Stephenson, P, Deprimo, SE et al. (2009). Clinical evaluation of continuous daily dosing of sunitinib malate in patients with advanced gastrointestinal stromal tumour after imatinib failure. Eur J Cancer 45: 1959-1968.
27. Raymond, E, Dahan, L, Raoul, JL, Bang, YJ, Borbath, I, Lombard-Bohas, C et al. (2011). Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 364: 501-513.
28. Kottke, T, Hall, G, Pulido, J, Diaz, RM, Thompson, J, Chong, H et al. (2010). Antiangiogenic cancer therapy combined with oncolytic virotherapy leads to regression of established tumors in mice. J Clin Invest 120: 1551-1560.
29. Russell, SJ and Peng, KW (2007). Viruses as anticancer drugs. Trends Pharmacol Sci 28: 326-333. (Pubitemid 47016683)
30. Breitbach, CJ, De Silva, NS, Falls, TJ, Aladl, U, Evgin, L, Paterson, J et al. (2011). Targeting tumor vasculature with an oncolytic virus. Mol Ther 19: 886-894.
31. Heo, J, Breitbach, CJ, Moon, A, Kim, CW, Patt, R, Kim, MK et al. (2011). Sequential therapy with JX-594, a targeted oncolytic poxvirus, followed by sorafenib in hepatocellular carcinoma: preclinical and clinical demonstration of combination efficacy. Mol Ther 19: 1170-1179.
32. Carey, BL, Ahmed, M, Puckett, S and Lyles, DS (2008). Early steps of the virus replication cycle are inhibited in prostate cancer cells resistant to oncolytic vesicular stomatitis virus. J Virol 82: 12104-12115.
33. Xiang, Y, Condit, RC, Vijaysri, S, Jacobs, B, Williams, BR and Silverman, RH (2002). Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J Virol 76: 5251-5259. (Pubitemid 34441727)
34. Kaighn, ME, Narayan, KS, Ohnuki, Y, Lechner, JF and Jones, LW (1979). Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 17: 16-23. (Pubitemid 9239413)
35. Gravina, GL, Marampon, F, Piccolella, M, Biordi, L, Ficorella, C, Motta, M et al. (2011). Antitumor effects of carnertinib in castration resistant prostate cancer models: a Comparative study with erlotinib. Prostate 71: 1481-1491.
36. Harding, HP, Zhang, Y and Ron, D (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274. (Pubitemid 29051178)
37. Shi, Y, Vattem, KM, Sood, R, An, J, Liang, J, Stramm, L et al. (1998). Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18: 7499-7509. (Pubitemid 28533068)
38. Carpten, J, Nupponen, N, Isaacs, S, Sood, R, Robbins, C, Xu, J et al. (2002). Germline mutations in the ribonuclease L gene in families showing linkage with HPC1. Nat Genet 30: 181-184.
39. Silverman, RH (2003). Implications for RNase L in prostate cancer biology. Biochemistry 42: 1805-1812. (Pubitemid 36258654)
40. Dong, B, Niwa, M, Walter, P and Silverman, RH (2001). Basis for regulated RNA cleavage by functional analysis of RNase L and Ire1p. RNA 7: 361-373. (Pubitemid 32381912)
41. Mahoney, DJ, Lefebvre, C, Allan, K, Brun, J, Sanaei, CA, Baird, S et al. (2011). Virustumor interactome screen reveals ER stress response can reprogram resistant cancers for oncolytic virus-triggered caspase-2 cell death. Cancer Cell 20: 443-456.
42. Ali, MM, Bagratuni, T, Davenport, EL, Nowak, PR, Silva-Santisteban, MC, Hardcastle, A et al. (2011). Structure of the Ire1 autophosphorylation complex and implications for the unfolded protein response. EMBO J 30: 894-905.
43. Balachandran, S, Roberts, PC, Brown, LE, Truong, H, Pattnaik, AK, Archer, DR et al. (2000). Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13: 129-141.
44. Malathi, K, Dong, B, Gale, M Jr and Silverman, RH (2007). Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448: 816-819. (Pubitemid 47266340)
45. Faria, PA, Chakraborty, P, Levay, A, Barber, GN, Ezelle, HJ, Enninga, J et al. (2005). VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol Cell 17: 93-102. (Pubitemid 40075368)
46. Farsaci, B, Higgins, JP and Hodge, JW (2012). Consequence of dose scheduling of sunitinib on host immune response elements and vaccine combination therapy. Int J Cancer 130: 1948-1959.
47. Faivre, S, Raymond, E, Boucher, E, Douillard, J, Lim, HY, Kim, JS et al. (2009). Safety and efficacy of sunitinib in patients with advanced hepatocellular carcinoma: an openlabel, multicentre, phase II study. Lancet Oncol 10: 794-800.
48. Dong, B and Silverman, RH (1995). 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J Biol Chem 270: 4133-4137.
49. Kopecky, SA, Willingham, MC and Lyles, DS (2001). Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J Virol 75: 12169-12181. (Pubitemid 33115890)
50. Black, BL, Rhodes, RB, McKenzie, M and Lyles, DS (1993). The role of vesicular stomatitis virus matrix protein in inhibition of host-directed gene expression is genetically separable from its function in virus assembly. J Virol 67: 4814-4821. (Pubitemid 23215962)