Oncolytic virotherapy for treatment of breast cancer, including triple-negative breast cancer

OncoImmunology

Volumn 5, Issue 2, 2016, Pages

  Bramante, Simona ^a   Koski, Anniina ^a   Liikanen, Ilkka ^a   Vassilev, Lotta ^b   Oksanen, Minna ^a   Siurala, Mikko ^a,c   Heiskanen, Raita ^b   Hakonen, Tiina ^b   Joensuu, Timo ^d   Kanerva, Anna ^a,e   Pesonen, Sari ^a,b   Hemminki, Akseli ^a,c,e  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Oncos Therapeutics   (Finland)

^c TILT Biotherapeutics Ltd   (Finland)

^d Docrates Oncology Clinic   (Finland)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Breast cancer; combination therapies; cyclophosphamide; GM CSF; oncolytic adenovirus; oncolytic virotherapy; triple negative breast cancer

Indexed keywords

EID: 84959374267     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1078057     Document Type: Article

References (52)

1. American Cancer Society: Cancer Facts and Figures 2015. Atlanta, Ga: American Cancer Society, 2015. http://www.cancer.org/research/cancerfactsstatistics/cancerfactsfigures2015/
2. R.Sandhu, J.S.Parker, W.D.Jones, C.A.Livasy, W.B.Coleman. Microarray-Based gene expression profiling for molecular classification of breast cancer and identification of new targets for therapy. Lab Medicine 2010; 41:364-72; http://dx.doi.org/10.1309/LMLIK0VIE3CJK0WD
3. http://www.cancer.gov/types/breast/patient/breast-treatment-pdq
4. P.Kern, A.Kalisch, H.C.Kolberg, R.Kimmig, F.Otterbach, G.von Minckwitz, W.M.Sikov, D.Pott, C.Kurbacher. Neoadjuvant, anthracycline-free chemotherapy with carboplatin and docetaxel in triple-negative, early-stage breast cancer: a multicentric analysis of feasibility and rates of pathologic complete response. Chemotherapy 2013; 59:387-94; PMID:24852315; http://dx.doi.org/10.1159/000362756
5. T.Browder, C.E.Butterfield, B.M.Kraling, B.Shi, B.Marshall, M.S.O'Reilly, J.Folkman. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 2000; 60:1878-86; PMID:10766175
6. E.Pasquier, M.Kavallaris, N.Andre. Metronomic chemotherapy: new rationale for new directions. Nat Rev Clin Oncol 2010; 7:455-65; PMID:20531380; http://dx.doi.org/10.1038/nrclinonc.2010.82
7. D.Loven, E.Hasnis, F.Bertolini, Y.Shaked. Low-dose metronomic chemotherapy: from past experience to new paradigms in the treatment of cancer. Drug Discov Today 2013; 18:193-201; PMID:22868084; http://dx.doi.org/10.1016/j.drudis.2012.07.015
8. M.Colleoni, A.Rocca, M.T.Sandri, L.Zorzino, G.Masci, F.Nole, G.Peruzzotti, C.Robertson, L.Orlando, S.Cinieri et al. Low-dose oral methotrexate and cyclophosphamide in metastatic breast cancer: antitumor activity and correlation with vascular endothelial growth factor levels. Ann Oncol 2002; 13:73-80; PMID:11863115; http://dx.doi.org/10.1093/annonc/mdf013
9. http://clinicaltrials.gov/.
10. P.P.Gor, H.I.Su, R.J.Gray, P.A.Gimotty, M.Horn, R.Aplenc, W.P.Vaughan, M.S.Tallman, T.R.Rebbeck, A.DeMichele. Cyclophosphamide-metabolizing enzyme polymorphisms and survival outcomes after adjuvant chemotherapy for node-positive breast cancer: a retrospective cohort study. Breast Cancer Res 2010; 12:R26; PMID:20459744; http://dx.doi.org/10.1186/bcr2570
11. A.Nicolini, P.Mancini, P.Ferrari, L.Anselmi, G.Tartarelli, V.Bonazzi, A.Carpi, R.Giardino. Oral low-dose cyclophosphamide in metastatic hormone refractory prostate cancer (MHRPC). Biomed Pharmacother 2004; 58:447-50; PMID:15464874; http://dx.doi.org/10.1016/j.biopha.2004.08.006
12. K.Lien, S.Georgsdottir, L.Sivanathan, K.Chan, U.Emmenegger. Low-dose metronomic chemotherapy: a systematic literature analysis. Eur J Cancer 2013; 49:3387-95; PMID:23880474; http://dx.doi.org/10.1016/j.ejca.2013.06.038
13. S.Man, G.Bocci, G.Francia, S.K.Green, S.Jothy, D.Hanahan, P.Bohlen, D.J.Hicklin, G.Bergers, R.S.Kerbel. Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 2002; 62:2731-5; PMID:12019144
14. R.Wang, S.Qin, Y.Chen, Y.Li, C.Chen, Z.Wang, R.Zheng, Q.Wu. Enhanced antitumor and anti-angiogenic effects of metronomic cyclophosphamide combined with Endostar in a xenograft model of human lung cancer. Oncol Rep 2012; 28:439-45; PMID:22641525; http://dx.doi.org/10.3892/or.2012.1828
15. F.Ghiringhelli, C.Menard, P.E.Puig, S.Ladoire, S.Roux, F.Martin, E.Solary, A.Le Cesne, L.Zitvogel, B.Chauffert. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007; 56:641-8; PMID:16960692; http://dx.doi.org/10.1007/s00262-006-0225-8
16. Y.Ge, C.Domschke, N.Stoiber, S.Schott, J.Heil, J.Rom, M.Blumenstein, J.Thum, C.Sohn, A.Schneeweiss et al. Metronomic cyclophosphamide treatment in metastasized breast cancer patients: immunological effects and clinical outcome. Cancer Immunol Immunother 2012; 61:353-62; PMID:21915801; http://dx.doi.org/10.1007/s00262-011-1106-3
17. V.Cerullo, I.Diaconu, L.Kangasniemi, M.Rajecki, S.Escutenaire, A.Koski, V.Romano, N.Rouvinen, T.Tuuminen, L.Laasonen et al. Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus. Mol Ther 2011; 19:1737-46; PMID:21673660; http://dx.doi.org/10.1038/mt.2011.113
18. I.Liikanen, L.Ahtiainen, M.L.Hirvinen, S.Bramante, V.Cerullo, P.Nokisalmi, O.Hemminki, I.Diaconu, S.Pesonen, A.Koski et al. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther 2013; 21:1212-23; PMID:23546299; http://dx.doi.org/10.1038/mt.2013.51
19. S.Bramante, J.K.Kaufmann, V.Veckman et al. Treatment of melanoma with a serotype 5/3 Chimeric oncolytic adenovirus coding for GM-CSF: results in vitro, in rodents and in humans. Int J Cancer 2015 Oct 1; 137(7):1775-83; PMID:25821063; http://dx.doi.org/10.1002/ijc.29536
20. A.Koski, L.Kangasniemi, S.Escutenaire, S.Pesonen, V.Cerullo, I.Diaconu, P.Nokisalmi, M.Raki, M.Rajecki, K.Guse et al. Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther 2010; 18:1874-84; PMID:20664527; http://dx.doi.org/10.1038/mt.2010.161
21. S.Bramante, A.Koski, A.Kipar, I.Diaconu, I.Liikanen, O.Hemminki, L.Vassilev, S.Parviainen, V.Cerullo, S.K.Pesonen et al. Serotype chimeric oncolytic adenovirus coding for GM-CSF for treatment of sarcoma in rodents and humans. In J Cancer 2014; 135:720-30; PMID:24374597; http://dx.doi.org/10.1002/ijc.28696
22. A.Kanerva, P.Nokisalmi, I.Diaconu, A.Koski, V.Cerullo, I.Liikanen, S.Tahtinen, M.Oksanen, R.Heiskanen, S.Pesonen et al. Antiviral and antitumor T-cell immunity in patients treated with GM-CSF-coding oncolytic adenovirus. Clin Cancer Res 2013; 19:2734-44; PMID:23493351; http://dx.doi.org/10.1158/1078-0432.CCR-12-2546
23. M.Siurala, S.Bramante, L.Vassilev, M.Hirvinen, S.Parviainen, S.Tahtinen, K.Guse, V.Cerullo, A.Kanerva, A.Kipar et al. Oncolytic adenovirus and doxorubicin-based chemotherapy results in synergistic antitumor activity against soft-tissue sarcoma. Int J Cancer 2015; 136:945-54; PMID:24975392; http://dx.doi.org/10.1002/ijc.29048
24. A.B.Shanafelt, K.E.Johnson, R.A.Kastelein. Identification of critical amino acid residues in human and mouse granulocyte-macrophage colony-stimulating factor and their involvement in species specificity. J Biol Chem 1991; 266:13804-10; PMID:1856212
25. O.Hemminki, I.Diaconu, V.Cerullo, S.K.Pesonen, A.Kanerva, T.Joensuu, K.Kairemo, L.Laasonen, K.Partanen, L.Kangasniemi et al. Ad3-hTERT-E1A, a fully serotype 3 oncolytic adenovirus, in patients with chemotherapy refractory cancer. Mol Ther 2012; 20:1821-30; PMID:22871667; http://dx.doi.org/10.1038/mt.2012.115
26. O.Hemminki, S.Parviainen, J.Juhila, R.Turkki, N.Linder, J.Lundin, M.Kankainen, A.Ristimaki, A.Koski, I.Liikanen et al. Immunological data from cancer patients treated with Ad5/3 E2F Delta24 GMCSF suggests utility for tumor immunotherapy. Oncotarget 2015; 6:4467-81; PMID:25714011; http://dx.doi.org/10.18632/oncotarget.2901
27. A.Koski, H.Ahtinen, H.Liljenback, A.Roivainen, A.Koskela, M.Oksanen, K.Partanen, L.Laasonen, K.Kairemo, T.Joensuu 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; PMID:24099555; http://dx.doi.org/10.1089/hum.2013.123
28. E.A.Eisenhauer, P.Therasse, J.Bogaerts, L.H.Schwartz, D.Sargent, R.Ford, J.Dancey, S.Arbuck, S.Gwyther, M.Mooney et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009; 45:228-47; PMID:19097774; http://dx.doi.org/10.1016/j.ejca.2008.10.026
29. V.Cerullo, S.Pesonen, I.Diaconu, S.Escutenaire, P.T.Arstila, M.Ugolini, P.Nokisalmi, M.Raki, L.Laasonen, M.Sarkioja et al. Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res 2010; 70:4297-309; PMID:20484030; http://dx.doi.org/10.1158/0008-5472.CAN-09-3567
30. J.J.Rojas, M.Cascallo, S.Guedan, A.Gros, J.Martinez-Quintanilla, A.Hemminki, R.Alemany. A modified E2F-1 promoter improves the efficacy to toxicity ratio of oncolytic adenoviruses. Gene Ther 2009; 16:1441-51; PMID:19710704; http://dx.doi.org/10.1038/gt.2009.103
31. P.Nokisalmi, S.Pesonen, S.Escutenaire, M.Sarkioja, M.Raki, V.Cerullo, L.Laasonen, R.Alemany, J.Rojas, M.Cascallo et al. Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors. Clin Cancer Res 2010; 16:3035-43; PMID:20501623; http://dx.doi.org/10.1158/1078-0432.CCR-09-3167
32. S.Pesonen, I.Diaconu, V.Cerullo, S.Escutenaire, M.Raki, L.Kangasniemi, P.Nokisalmi, G.Dotti, K.Guse, L.Laasonen et al. Integrin targeted oncolytic adenoviruses Ad5-D24-RGD and Ad5-RGD-D24-GMCSF for treatment of patients with advanced chemotherapy refractory solid tumors. Int J Cancer 2012; 130:1937-47; PMID:21630267; http://dx.doi.org/10.1002/ijc.26216
33. A.Koski, M.Raki, P.Nokisalmi, I.Liikanen, L.Kangasniemi, T.Joensuu, A.Kanerva, S.Pesonen, R.Alemany, A.Hemminki. Verapamil results in increased blood levels of oncolytic adenovirus in treatment of patients with advanced cancer. Mol Ther 2012; 20:221-9; PMID:22044933; http://dx.doi.org/10.1038/mt.2011.230
34. M.Raki, A.Kanerva, A.Ristimaki, R.A.Desmond, D.T.Chen, T.Ranki, M.Sarkioja, L.Kangasniemi, A.Hemminki. 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; PMID:15800658; http://dx.doi.org/10.1038/sj.gt.3302517
35. K.Ottolino-Perry, J.S.Diallo, B.D.Lichty, J.C.Bell, J.A.McCart. Intelligent design: combination therapy with oncolytic viruses. Mol Ther 2010; 18:251-63; PMID:20029399; http://dx.doi.org/10.1038/mt.2009.283
36. F.R.Khuri, J.Nemunaitis, I.Ganly, J.Arseneau, I.F.Tannock, L.Romel, M.Gore, J.Ironside, R.H.MacDougall, C.Heise 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; 6:879-85; PMID:10932224; http://dx.doi.org/10.1038/78638
37. N.E.Sladek. Therapeutic efficacy of cyclophosphamide as a function of inhibition of its metabolism. Cancer Res 1972; 32:1848-54; PMID:4641276
38. A.H.Ginsberg, W.T.Monte, K.P.Johnson. Effect of cyclophosphamide in vitro and on vaccinia virus replication in tissue culture. J Virol 1977; 21:277-83; PMID:833925
39. T.Ranki, M.Sarkioja, T.Hakkarainen, K.von Smitten, A.Kanerva, A.Hemminki. Systemic efficacy of oncolytic adenoviruses in imagable orthotopic models of hormone refractory metastatic breast cancer. Int J Cancer 2007; 121:165-74; PMID:17315187; http://dx.doi.org/10.1002/ijc.22627
40. K.Guse, T.Ranki, M.Ala-Opas, P.Bono, M.Sarkioja, M.Rajecki, A.Kanerva, T.Hakkarainen, A.Hemminki. Treatment of metastatic renal cancer with capsid-modified oncolytic adenoviruses. Mol Cancer Ther 2007; 6:2728-36; PMID:17938266; http://dx.doi.org/10.1158/1535-7163.MCT-07-0176
41. A.Kanerva, M.Raki, T.Ranki, M.Sarkioja, J.Koponen, R.A.Desmond, A.Helin, U.H.Stenman, H.Isoniemi, K.Hockerstedt et al. Chlorpromazine and apigenin reduce adenovirus replication and decrease replication associated toxicity. J Gene Med 2007; 9:3-9; PMID:17149790; http://dx.doi.org/10.1002/jgm.984
42. A.M.Cohen, D.K.Hines, E.S.Korach, B.J.Ratzkin. In vivo activation of neutrophil function in hamsters by recombinant human granulocyte colony-stimulating factor. Infect Immun 1988; 56:2861-5; PMID:2459064
43. M.A.Thomas, J.F.Spencer, M.C.La Regina, D.Dhar, A.E.Tollefson, K.Toth, W.S.Wold. Syrian hamster as a permissive immunocompetent animal model for the study of oncolytic adenovirus vectors. Cancer Res 2006; 66:1270-6; PMID:16452178; http://dx.doi.org/10.1158/0008-5472.CAN-05-3497
44. J.D.Wolchok, A.Hoos, S.O'Day, J.S.Weber, O.Hamid, C.Lebbe, M.Maio, M.Binder, O.Bohnsack, G.Nichol et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15:7412-20; PMID:19934295; http://dx.doi.org/10.1158/1078-0432.CCR-09-1624
45. R.C.Bast, Jr., T.L.Klug, E.St John, E.Jenison, J.M.Niloff, H.Lazarus, R.S.Berkowitz, T.Leavitt, C.T.Griffiths, L.Parker et al. A radioimmunoassay using a monoclonal antibody to monitor the course of epithelial ovarian cancer. New Engl J Med 1983; 309:883-7; PMID:6310399; http://dx.doi.org/10.1056/NEJM198310133091503
46. T.J.Wallace, T.Torre, M.Grob, J.Yu, I.Avital, B.Brucher, A.Stojadinovic, Y.G.Man. Current approaches, challenges and future directions for monitoring treatment response in prostate cancer. J Cancer 2014; 5:3-24; PMID:24396494; http://dx.doi.org/10.7150/jca.7709
47. A.Hemminki. Treatment of chemotherapy-refractory cancer in the advanced therapy access program. Mol Ther 2012; 20:1654-5; PMID:22945227; http://dx.doi.org/10.1038/mt.2012.170
48. A.Hemminki, M.Oksanen, M.Merisalo-Soikkeli. Oncolytic virotherapy trials–letter. Clin Cancer Res 2013; 19:4541-2; PMID:23946419; http://dx.doi.org/10.1158/1078-0432.CCR-13-1471
49. www.oncos.com.
50. A.Kanerva, K.R.Zinn, T.R.Chaudhuri, J.T.Lam, K.Suzuki, T.G.Uil, T.Hakkarainen, G.J.Bauerschmitz, M.Wang, B.Liu et al. Enhanced therapeutic efficacy for ovarian cancer with a serotype 3 receptor-targeted oncolytic adenovirus. Mol Ther 2003; 8:449-58; PMID:12946318; http://dx.doi.org/10.1016/S1525-0016(03)00200-4
51. A.Kanerva, G.V.Mikheeva, V.Krasnykh, C.J.Coolidge, J.T.Lam, P.J.Mahasreshti, S.D.Barker, M.Straughn, M.N.Barnes, R.D.Alvarez et al. Targeting adenovirus to the serotype 3 receptor increases gene transfer efficiency to ovarian cancer cells. Clin Cancer Res 2002; 8:275-80; PMID:11801569
52. A.Hemminki. Oncolytic immunotherapy: where are we clinically? Scientifica 2014; 2014:862925; PMID:24551478; http://dx.doi.org/10.1155/2014/862925