Oncolytic adenovirus and doxorubicin-based chemotherapy results in synergistic antitumor activity against soft-tissue sarcoma

International Journal of Cancer

Volumn 136, Issue 4, 2015, Pages 945-954

  Siurala, Mikko ^a   Bramante, Simona ^a   Vassilev, Lotta ^b   Hirvinen, Mari ^c   Parviainen, Suvi ^a   Tähtinen, Siri ^a   Guse, Kilian ^a   Cerullo, Vincenzo ^c   Kanerva, Anna ^a,d   Kipar, Anja ^e,f   Vähä Koskela, Markus ^a   Hemminki, Akseli ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Oncos Therapeutics Inc   (Finland)

^c Faculty of Pharmacy   (Finland)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e UNIVERSITY OF HELSINKI   (Finland)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Chemotherapy; GMCSF; Immunogenic cell death; Oncolytic adenovirus; Soft tissue sarcoma

Indexed keywords

CGTG 102; DOXORUBICIN; IFOSFAMIDE; ONCOLYTIC ADENOVIRUS; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; ONCOLYTIC VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL DEATH; CELL KILLING; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENCE; IMMUNOGENICITY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; SOFT TISSUE SARCOMA; SYRIAN HAMSTER; UPREGULATION; VIRUS REPLICATION; ADENOVIRIDAE; ANIMAL; C57BL MOUSE; CELL SURVIVAL; DRUG SCREENING; HAMSTER; IMMUNOLOGY; LEIOMYOSARCOMA; MELANOMA, EXPERIMENTAL; MESOCRICETUS; MULTIMODALITY CANCER THERAPY; NUDE MOUSE; SARCOMA; TUMOR CELL LINE;

ADENOVIRIDAE; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; CELL SURVIVAL; COMBINED MODALITY THERAPY; CRICETINAE; DOXORUBICIN; DRUG SYNERGISM; FEMALE; HUMANS; IFOSFAMIDE; LEIOMYOSARCOMA; MALE; MELANOMA, EXPERIMENTAL; MESOCRICETUS; MICE; MICE, INBRED C57BL; MICE, NUDE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; SARCOMA; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84919952624     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29048     Document Type: Article

References (46)

1. Clark MA, Fisher C, Judson I, et al. Soft-tissue sarcomas in adults. N Engl J Med 2005;353:701-11
2. Reed D, Altiok S. Metastatic soft tissue sarcoma chemotherapy: An opportunity for personalized medicine. Cancer Control 2011;18:188-95
3. Quesada J, Amato R. The molecular biology of soft-tissue sarcomas and current trends in therapy. Sarcoma 2012;2012:849456
4. Sokolowski E, Turina CB, Kikuchi K, et al. Proofof- concept rare cancers in drug development: The case for rhabdomyosarcoma. Oncogene 2014;33: 1877-89
5. Casares N, Pequignot MO, Tesniere A, et al. Caspase- dependent immunogenicity of doxorubicininduced tumor cell death. J Exp Med 2005;202: 1691-701
6. Obeid M, Tesniere A, Ghiringhelli F, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007;13:54-61
7. Galluzzi L, Senovilla L, Zitvogel L, et al. The secret ally: Immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012;11:215-33
8. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011;8:151-60
9. Kepp O, Galluzzi L, Martins I, et al. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Rev 2011;30:61-9
10. Inoue H, Tani K. Multimodal immunogenic cancer cell death as a consequence of anticancer cytotoxic treatments. Cell Death Differ 2014;21: 39-49
11. Raki M, Sarkioja M, Desmond RA, et al. Oncolytic adenovirus Ad5/3-delta24 and chemotherapy for treatment of orthotopic ovarian cancer. Gynecol Oncol 2008;108:166-72
12. Rajecki M, af Hallstrom T, Hakkarainen T, et al. Mre11 inhibition by oncolytic adenovirus associates with autophagy and underlies synergy with ionizing radiation. Int J Cancer 2009;125:2441-9
13. Ottolino-Perry K, Diallo JS, Lichty BD, et al. Intelligent design: combination therapy with oncolytic viruses. Mol Ther 2010;18:251-63
14. Fueyo J, Gomez-Manzano C, Alemany R, et al. A mutant oncolytic adenovirus targeting the rb pathway produces anti-glioma effect in vivo. Oncogene 2000;19:2-12
15. Sherr CJ. Cancer cell cycles. Science 1996;274: 1672-7
16. Koski A, Kangasniemi L, Escutenaire S, et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther 2010;18:1874-84
17. Arellano M, Lonial S. Clinical uses of GM-CSF, a critical appraisal and update. Biologics 2008;2:13-27
18. Cerullo V, Pesonen S, Diaconu I, et al. Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res 2010;70: 4297-309
19. Cerullo V, Diaconu I, Kangasniemi L, et al. Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus. Mol Ther 2011;19:1737-46
20. Kanerva A, Nokisalmi P, Diaconu I, et al. Antiviral and antitumor T-cell immunity in patients treated with GM-CSF-coding oncolytic adenovirus. Clin Cancer Res 2013;19:2734-44
21. Liikanen I, Ahtiainen L, Hirvinen ML, et al. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther 2013;21: 1212-23
22. van der Graaf W, Judson I, Verweij J. Results of a randomized phase III trial (EORTC 62012) of single agent doxorubicin versus doxorubicin plus ifosfamide as first line chemotherapy for patients with advanced or metastatic soft tissue sarcoma: A survival study by the EORTC soft tissue and bone sarcoma group. Presented at the 2012 ESMO Congress, Abstract LBA7, Vienna, Austria, October 1, 2012
23. Yokoyama Y, Dhanabal M, Griffioen AW, et al. Synergy between angiostatin and endostatin: Inhibition of ovarian cancer growth. Cancer Res 2000; 60:2190-6
24. Xu H, Niu X, Zhang Q, et al. Synergistic antitumor efficacy by combining adriamycin with recombinant human endostatin in an osteosarcoma model. Oncol Lett 2011;2:773-8
25. Webb J. Effect of more than one inhibitor, antagonism, summation, and synergism. In: Webb J, ed. Enzyme and metabolic inhibitors. New York: Academic Press, 1963. 488-512
26. Bramante S, Koski A, Kipar A, et al. Serotype chimeric oncolytic adenovirus coding for GMCSF for treatment of sarcoma in rodents and humans. Int J Cancer 2013;135:720-30
27. Raki M, Kanerva A, Ristimaki A, et al. Combination of gemcitabine and Ad5/3-Delta24, a tropism modified conditionally replicating adenovirus, for the treatment of ovarian cancer. Gene Ther 2005; 12:1198-205
28. Li Y, Yu DC, Chen Y, et al. A hepatocellular carcinoma-specific adenovirus variant, CV890, eliminates distant human liver tumors in combination with doxorubicin. Cancer Res 2001;61: 6428-36
29. Hoffmann D, Heim A, Nettelbeck DM, et al. Evaluation of twenty human adenoviral types and one infectivity-enhanced adenovirus for the therapy of soft tissue sarcoma. Hum Gene Ther 2007; 18:51-62
30. Thomas MA, Spencer JF, La Regina MC, et al. Syrian hamster as a permissive immunocompetent animal model for the study of oncolytic adenovirus vectors. Cancer Res 2006;66:1270-6
31. Wold WS, Toth K. Chapter three-Syrian hamster as an animal model to study oncolytic adenoviruses and to evaluate the efficacy of antiviral compounds. Adv Cancer Res 2012;115:69-92
32. Tascilar M, Loos WJ, Seynaeve C, et al. The pharmacologic basis of ifosfamide use in adult patients with advanced soft tissue sarcomas. Oncologist 2007;12:1351-60
33. Ghiringhelli F, Menard C, Puig PE, et al. Metronomic cyclophosphamide regimen selectively depletes CD41CD251 regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007;56:641-8
34. Yu DC, Chen Y, Dilley J, et al. Antitumor synergy of CV787, a prostate cancer-specific adenovirus, and paclitaxel and docetaxel. Cancer Res 2001;61:517-25
35. Weiland T, Lampe J, Essmann F, et al. Enhanced killing of therapy-induced senescent tumor cells by oncolytic measles vaccine viruses. Int J Cancer 2014;134:235-43
36. Kanerva A, Mikheeva GV, Krasnykh V, et al. Targeting adenovirus to the serotype 3 receptor increases gene transfer efficiency to ovarian cancer cells. Clin Cancer Res 2002;8: 275-80
37. Volk AL, Rivera AA, Kanerva A, et al. Enhanced adenovirus infection of melanoma cells by fibermodification: Incorporation of RGD peptide or Ad5/3 chimerism. Cancer Biol Ther 2003;2:511-15
38. Kangasniemi L, Kiviluoto T, Kanerva A, et al. Infectivity-enhanced adenoviruses deliver efficacy in clinical samples and orthotopic models of disseminated gastric cancer. Clin Cancer Res 2006; 12:3137-44
39. Guse K, Diaconu I, Rajecki M, et al. Ad5/3- 9HIF-Delta24-VEGFR-1-ig, an infectivity enhanced, dual-targeted and antiangiogenic oncolytic adenovirus for kidney cancer treatment. Gene Ther 2009;16:1009-20
40. Reid TR, Freeman S, Post L, et al. Effects of onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5- FU/leucovorin. Cancer Gene Ther 2005;12:673-81
41. Koski A, Ahtinen H, Liljenback H, et al. (18)F]- fluorodeoxyglucose positron emission tomography and computed tomography in response evaluation of oncolytic adenovirus treatments of patients with advanced cancer. Hum Gene Ther 2013;24: 1029-41
42. Ramakrishnan R, Gabrilovich DI. Novel mechanism of synergistic effects of conventional chemotherapy and immune therapy of cancer. Cancer Immunol Immunother 2013;62: 405-10
43. Hemminki O, Diaconu I, Cerullo V, et al. Ad3- hTERT-E1A, a fully serotype 3 oncolytic adenovirus, in patients with chemotherapy refractory cancer. Mol Ther 2012;20: 1821-30
44. Hirvinen M, Heiskanen R, Oksanen M, et al. Fcgamma receptor polymorphisms as predictive and prognostic factors in patients receiving oncolytic adenovirus treatment. J Transl Med 2013;11:193
45. Pesonen S, Diaconu I, Kangasniemi L, et al. Oncolytic immunotherapy of advanced solid tumors with a CD40L-expressing replicating adenovirus: Assessment of safety and immunologic responses in patients. Cancer Res 2012;72:1621-31
46. Nokisalmi P, Pesonen S, Escutenaire S, et al. Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors. Clin Cancer Res 2010;16:3035-43.