Recent advances in oncolytic adenovirus therapies for cancer

Current Opinion in Virology

Volumn 21, Issue , 2016, Pages 9-15

  Rosewell Shaw, Amanda ^a,b   Suzuki, Masataka ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD137 LIGAND; CD40 LIGAND; CKS17 PROTEIN; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; CYCLOPHOSPHAMIDE; E1A PROTEIN; E1B PROTEIN; ENDOSTATIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 24; INTERLEUKIN 6; MEMBRANE COFACTOR PROTEIN; ONCOLYTIC ADENOVIRUS; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 3; ONCOLYTIC VIRUS;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTIGEN PRESENTING CELL; BREAST CANCER; CANCER CELL; CANCER GENE THERAPY; CARCINOMA CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN DEGRADATION; CYTOKINE PRODUCTION; CYTOLYSIS; DNA MODIFICATION; ENDOTHELIUM CELL; GLIOBLASTOMA; HUMAN; IMMUNE EVASION; IMMUNOCOMPETENT CELL; LUNG CANCER; MACROPHAGE; NASOPHARYNX CARCINOMA; NATURAL KILLER CELL; NONHUMAN; ONCOLYTIC VIROTHERAPY; OVARY CANCER; PANCREAS CARCINOMA; PANCREATIC CARCINOMA CELL; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; REVIEW; SEROTYPE; SOLID TUMOR; SUPPRESSOR CELL; TUMOR MICROENVIRONMENT; UPREGULATION; VIRAL TROPISM; VIRUS REPLICATION; ADENOVIRIDAE; GENE THERAPY; GENETIC TRANSDUCTION; GENETICS; NEOPLASMS; PHYSIOLOGY; PROCEDURES;

ADENOVIRIDAE; GENETIC THERAPY; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; TRANSDUCTION, GENETIC; VIRAL TROPISM;

EID: 84978500902     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2016.06.009     Document Type: Review

References (44)

1. 1 Lichty, B.D., Breitbach, C.J., Stojdl, D.F., Bell, J.C., Going viral with cancer immunotherapy. Nat Rev Cancer 14 (2014), 559–567.
2. 2 Jiang, H., Fueyo, J., Healing after death: antitumor immunity induced by oncolytic adenoviral therapy. Oncoimmunology, 3, 2014, e947872.
3. 3 Pol, J., Buqué, A., Aranda, F., Bloy, N., Cremer, I., Eggermont, A., Erbs, P., Fucikova, J., Galon, J., Limacher, J., et al. Trial watch-oncolytic viruses and cancer therapy. Oncoimmunology, 3, 2016, e1117740.
4. 4 Dolgin, E., Oncolytic viruses get a boost with first FDA-approval recommendation. Nat Rev Drug Discov 14 (2015), 369–371.
5. 5•• Andtbacka, R.H., Kaufman, H.L., Collichio, F., Amatruda, T., Senzer, N., Chesney, J., Delman, K.A., Spitler, L.E., Puzanov, I., Agarwala, S.S., et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol 33 (2015), 2780–2788 Results from the phase III clinical trial of T-VEC, the first oncolytic virus approved by the FDA, in patients with melanoma showing therapeutic benefit with a median overall survival of 23.3 months with T-VEC compared to 18.9 months in patients receiving only GM-CSF.
6. 6 Li, Y., Pong, R.C., Bergelson, J.M., Hall, M.C., Sagalowsky, A.I., Tseng, C.P., Wang, Z., Hsieh, J.T., Loss of adenoviral receptor expression in human bladder cancer cells: a potential impact on the efficacy of gene therapy. Cancer Res 59 (1999), 325–330.
7. 7 Shen, Y.H., Yang, F., Wang, H., Cai, Z.J., Xu, Y.P., Zhao, A., Su, Y., Zhang, G., Zhu, S.X., Arg-Gly-Asp (RGD)-modified E1A/E1B double mutant adenovirus enhances antitumor activity in prostate cancer cells in vitro and in mice. PLOS ONE, 11, 2016, e0147173.
8. 8 Bauerschmitz, G.J., Lam, J.T., Kanerva, A., Suzuki, K., Nettelbeck, D.M., Dmitriev, I., Krasnykh, V., Mikheeva, G.V., Barnes, M.N., Alvarez, R.D., et al. Treatment of ovarian cancer with a tropism modified oncolytic adenovirus. Cancer Res 62 (2002), 1271–1274.
9. 9 Tuve, S., Wang, H., Ware, C., Liu, Y., Gagger, A., Bernt, K., Shayakhmetov, D., Li, Z., Strauss, R., Stone, D., et al. A new group B adenovirus receptor is expressed at high levels on human stem and tumor cells. J Virol 80 (2006), 12109–12120.
10. 10 Thorsteinsson, L., O'Dowd, G.M., Harrington, P.M., Johnson, P.M., The complement regulatory proteins CD46 and CD59; but not CD55, are highly expressed by glandular epithelium of human breast and colorectal tumour tissues. APMIS 106 (1998), 869–879.
11. 11 Wang, H., Li, Z.Y., Liu, Y., Persson, J., Beyer, I., Möller, T., Koyuncu, D., Drescher, M.R., Strauss, R., Zhang, X.B., et al. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11, and 14. Nat Med 17 (2011), 96–104.
12. 12 Nevins, J.R., Transcriptional regulation. A closer look at E2F. Nature 358 (1992), 375–376.
13. 13 Fueyo, J., Gomez-Manzano, C., Alemany, R., Lee, P.S., McDonnell, T.J., Mitlianga, P., Shi, Y.X., Levin, V.A., Yung, W.K., Kyritsis, A.P., A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 19 (2000), 2–12.
14. 14 Rojas, J.J., Guedan, S., Searle, P.F., Martinez-Quintanilla, J., Gil-Hoyos, R., Alcayaga-Miranda, F., Cascallo, M., Alemany, R., Minimal RB-responsive E1A promoter modification to attain potency, selectivity, and transgene-arming capacity in oncolytic adenoviruses. Mol Ther 18 (2010), 1960–1971.
15. 15• Sarkar, S., Quinn, B.A., Shen, X.N., Dash, R., Das, S.K., Emdad, L., Klibanov, A.L., Wang, X.Y., Pellecchia, M., Sarkar, D., et al. Therapy of prostate cancer using a novel cancer terminator virus and a small molecule BH-3 mimetic. Oncotarget 6 (2015), 10712–10727 A dual regulated oncolytic Ad in which E1A is controlled by a prostate cancer specific promoter, tCCN1, and mda-7/IL-24 transgenes are controlled by the CMV promoter to generate cancer cell specific lysis and bystander anti-tumor effects. An ultrasound guided microbubble approach is used to enhance cancer targeting and avoid virus elimination by immune cells after systemic delivery.
16. 16 Lee, S.Y., Park, H.R., Rhee, J., Park, Y.M., Kim, S.H., Therapeutic effect of oncolytic adenovirus expressing relaxin in radioresistant oral squamous cell carcinoma. Oncol Res 20 (2013), 419–425.
17. 17•• Vera, B., Martinez-Vélez, N., Xipell, E., Acanda de la Rocha, A., Patiño-García, A., Saez-Castresana, J., Gonzalez-Huarriz, M., Cascallo, M., Alemany, R., Alonso, M.M., Characterization of the antiglioma effect of the oncolytic adenovirus VCN-01. PLOS ONE, 11, 2016, e0147211 A single intratumoral administration of VCN-01, an Onc.Ad expressing hyaluronidase, doubled animal survival in two orthotopic glioma models, eradicating tumors in long-term survivors.
18. 18 Ganesh, S., Gonzales, E.M., Idamakanti, N., Abramova, M., Vanroey, M., Robinson, M., Yun, C.O., Jooss, K., Relaxin-expressing, fiber chimeric oncolytic adenovirus prolongs survival of tumor-bearing mice. Cancer Res 67 (2007), 4399–4407.
19. 19 Yang, S.W., Cody, J.J., Rivera, A.A., Waehler, R., Wang, M., Kimball, K.J., Alvarez, R.A., Siegal, G.P., Douglas, J.T., Ponnazhagan, S., Conditionally replicating adenovirus expressing TIMP2 for ovarian cancer therapy. Clin Cancer Res 17 (2011), 538–549.
20. 20•• Lucas, T., Benihoud, K., Vigant, F., Schmidt, C.Q., Wortmann, A., Bachem, M.G., Simmet, T., Kochanek, S., Hexon modification to improve the activity of oncolytic adenovirus vectors against neoplastic and stromal cells in pancreatic cancer. PLOS ONE, 18, 2015, e0117254 Insertion of a targeting peptide, CKS17, into the Ad hexon protein enhanced Onc.Ad transduction to both malignant cells and pancreatic stellate cells while decreasing liver uptake and increases cytotoxicity of complex co-cultures.
21. 21 Thaci, B., Ulasov, I.V., Ahmed, A.U., Ferguson, S.D., Han, Y., Lesniak, M.S., Anti-angiogenic therapy increases intratumoral adenovirus distribution by inducing collagen degradation. Gene Ther 20 (2013), 318–327.
22. 22 Choi, I.K., Shin, H., Oh, E., Yoo, J.Y., Hwang, J.K., Shin, K., Yu, D.C., Yun, C.O., Potent and long-term antiangiogenic efficacy mediated by FP3-expressing oncolytic adenovirus. Int J Cancer 137 (2015), 2253–2269.
23. 23 Bazan-Peregrino, M., Sainson, R.C., Carlisle, R.C., Thoma, C., Waters, R.A., Arvanitis, C., Harris, A.L., Hernandez-Alcoceba, R., Seymour, L.W., Combining virotherapy and angiotherapy for the treatment of breast cancer. Cancer Gene Ther 20 (2013), 461–468.
24. 24 Li, H.L., Li, S., Shao, J.Y., Lin, X.B., Cao, Y., Jiang, W.Q., Liu, R.Y., Zhao, P., Zhu, X.F., Zeng, M.S., et al. Pharmacokinetic and pharmacodynamics study of intratumoral injection of an adenovirus encoding endostatin in patients with advanced tumors. Gene Ther 15 (2008), 247–256.
25. 25 Lin, X., Huang, H., Li, S., Li, H., Li, Y., Cao, Y., Zhang, D., Xia, Y., Guo, Y., Huang, W., et al. A phase I clinical trial of an adenovirus-mediated endostatin gene (E10A) in patients with solid tumors. Cancer Biol Ther 6 (2007), 648–653.
26. 26 Li, L.X., Zhang, Y.L., Zhou, L., Ke, M.L., Chen, J.M., Fu, X., Ye, C.L., Wu, J.X., Liu, R.Y., Huang, W., Antitumor efficacy of a recombinant adenovirus encoding endostatin combined with an E1B55KD-deficient adenovirus in gastric cancer cells. J Transl Med, 11, 2013, 257.
27. 27 Cuevas, Y., Hernández-Alcoceba, R., Aragones, J., Naranjo-Suárez, S., Castellanos, M.C., Esteban, M.A., Martin-Puig, S., Landazuri, M.O., del Peso, L., Specific oncolytic effect of a new hypoxia-inducible factor dependent replicative adenovirus on von Hippel–Lindau-defective renal cell carcinoma. Cancer Res 63 (2003), 6877–6884.
28. 28 Post, D.E., Devi, N.S., Li, Z., Brat, D.J., Kaur, B., Nicholson, A., Olson, J.J., Zhang, Z., Van Meir, E.G., Cancer therapy with a replicating oncolytic adenovirus targeting the hypoxic microenvironment of tumors. Clin Cancer Res 10 (2004), 8603–8612.
29. 29 Loskog, A., Immunostimulatory gene therapy using oncolytic viruses as vehicles. Viruses 6 (2015), 5780–5791.
30. 30 Ostuni, R., Kratochvill, F., Murray, P.J., Natoli, G., Macrophages and cancer: from mechanisms to therapeutic implications. Trends Immunol 36 (2015), 229–239.
31. 31 Koski, A., Kangasniemi, L., Escutenaire, S., Pesonen, S., Cerullo, V., Diaconu, I., Nokisalmi, P., Raki, M., Rajecki, M., Guse, K., et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther 18 (2010), 1874–1884.
32. 32• Ranki, T., Pesonen, S., Hemminki, A., Partanen, K., Kairemo, K., Alanko, T., Lundin, J., Linder, N., Turkki, R., Ristimäki, A., et al. Phase I study with ONCOS-102 for the treatment of solid tumors — an evaluation of clinical response and exploratory analyses of immune markers. J Immunother Cancer, 4, 2016, 17 A GM-CSF expressing Onc.Ad (ONCOS-102) was safely administered to 12 patients with refractory solid tumors, 40% of evaluable patients had stable disease at 3 months with 11 of 12 patients having evidence of TILs post treatment.
33. 33 Vassilev, L., Ranki, T., Joensuu, T., Jäger, E., Karbach, J., Wahle, C., Partanen, K., Kairemo, K., Alanko, T., Turkki, R., et al. Repeated intratumoral administration of ONCOS-102 leads to systemic antitumor CD8+ T-cell response and robust cellular and transcriptional immune activation at tumor site in a patient with ovarian cancer. Oncoimmunology, 4, 2015, e1017702.
34. 34• Hirvinen, M., Rajecki, M., Kapanen, M., Parviainen, S., Rouvinen-Lagerström, N., Diaconu, I., Nokisalmi, P., Tenhunen, M., Hemminki, A., Cerullo, V., Immunological effects of a tumor necrosis factor alpha-armed oncolytic adenovirus. Hum Gene Ther 26 (2015), 134–144 An Onc.Ad expressing TNFα provides enhanced anti-tumor effect in a xenograft prostate cancer model and increased CD8+ T cell infiltration to B16-OVA syngeneic mouse model.
35. 35 LaRocca, C.J., Han, J., Gavrikova, T., Armstrong, L., Oliveira, A.R., Shanley, R., Vickers S.M., Yamamoto, M., Davydova, J., Oncolytic adenovirus expressing interferon alpha in a syngeneic Syrian hamster model for the treatment of pancreatic cancer. Surgery 157 (2015), 888–898.
36. 36 Suzuki, M., Bertin, T.K., Rogers, G.L., Cela, R.G., Zolotukhin, I., Palmer, D., Ng, P., Herzog, R.W., Lee, B., Differential type I interferon-dependent transgene silencing of helper-dependent adenoviral vs adeno-associated viral vectors in vivo. Mol Ther 21 (2013), 796–805.
37. H cells. J Exp Med 177 (1993), 1199–1204.
38. 38 Freytag, S.O., Barton, K.N., Zhang, Y., Efficacy of oncolytic adenovirus expressing suicide genes and interleukin-12 in preclinical model of prostate cancer. Gene Ther 20 (2013), 1131–1139.
39. 39 Fretag, S.O., Zhang, Y., Siddiqui, F., Preclinical toxicology of oncolytic adenovirus-mediated cytotoxic and interleukin-12 gene therapy for prostate cancer. Mol Ther Oncolytics, 2, 2015, 15006.
40. 40 Zhao, L., Gu, J., Dong, A., Zhang, Y., Zhong, L., He, L., Wang, Y., Zhang, J., Zhang, Z., Huiwang, J., et al. Potent antitumor activity of oncolytic adenovirus expressing mda-7/IL-24 for colorectal cancer. Hum Gene Ther 16 (2005), 845–858.
41. 41 He, B., Huang, X., Liu, X., Xu, B., Cancer targeting gene-viro-therapy for pancreatic cancer using oncolytic adenovirus ZD55-IL-24 in immune-competent mice. Mol Biol Rep 40 (2013), 5397–5405.
42. 42 Malmstrom, P.U., Loskog, A.S., Lindqvist, C.A., Mangsbo, S.M., Fransson, M., Wanders, A., Gårdmark, T., Tötterman, T.H., AdCD40L immunogene therapy for bladder carcinoma — the first phase I/IIa trial. Clin Cancer Res 16 (2010), 3279–3287.
43. 43 Pesonen, S., Diaconu, I., Kangasniemi, L., Ranki, T., Kanerva, A., Pesonen, S.K., Gerdemann, U., Leen, A.M., Kairemo, K., Oksanen, M., et al. Oncolytic immunotherapy of advanced solid tumors with a CD40L-expressing replicating adenovirus: assessment of safety and immunologic responses in patients. Cancer Res 72 (2012), 1621–1631.
44. 44 Farzad, L., Cerullo, V., Yagyu, S., Bertin, T., Hemminki, A., Rooney, C., Lee, B., Suzuki, M., Combinatorial treatment with oncolytic adenovirus and helper-dependent adenovirus augments adenoviral cancer gene therapy. Mol Ther Oncolytics, 1, 2014, 14008.