Radiotherapy combined with the immunocytokine L19-IL2 provides long-lasting antitumor effects

Clinical Cancer Research

Volumn 21, Issue 5, 2015, Pages 1151-1160

  Zegers, Catharina M L ^a   Rekers, Nicolle H ^a   Quaden, Dana H F ^a   Lieuwes, Natasja G ^a   Yaromina, Ala ^a   Germeraad, Wilfred T V ^a   Wieten, Lotte ^a   Biessen, Erik A L ^b   Boon, Louis ^c   Neri, Dario ^d   Troost, Esther G C ^a   Dubois, Ludwig J ^a   Lambin, Philippe ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c BIOCEROS   (Netherlands)

^d ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DARLEUKIN; ANTINEOPLASTIC AGENT; FIBRONECTIN; HYBRID PROTEIN; L19-IL2 IMMUNOCYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER RADIOTHERAPY; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELL POPULATION; COLON CARCINOMA; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; FLOW CYTOMETRY; IMMUNOGENICITY; IMMUNOLOGY; IN VIVO STUDY; LEWIS CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TARGETING; TUMOR GROWTH; ANIMAL; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; HUMAN; LYMPHOCYTE DEPLETION; METABOLISM; MORTALITY; MULTIMODALITY CANCER THERAPY; NEOPLASMS; PATHOLOGY; RADIATION DOSE; RADIATION RESPONSE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; FIBRONECTINS; HUMANS; LYMPHOCYTE DEPLETION; MICE; NEOPLASMS; RADIOTHERAPY DOSAGE; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928804945     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2676     Document Type: Article

References (50)

1. Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer 2012;12:860-75.
2. Kaur P, Asea A. Radiation-induced effects and theimmune system in cancer. Front Oncol 2012;2:191.
3. Demaria S, Bhardwaj N, McBride WH, Formenti SC. Combining radiotherapy and immunotherapy: a revived partnership. Int J Radiat Oncol Biol Phys 2005;63:655-66.
4. McBride WH, Chiang CS, Olson JL, Wang CC, Hong JH, Pajonk F, et al. A sense of danger from radiation. Radiat Res 2004;162:1-19.
5. Demaria S, Formenti SC. Role of T lymphocytes in tumor response to radiotherapy. Front Oncol 2012;2:95.
6. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009;9:353-63.
7. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 2004;58: 862-70.
8. Wersall PJ, Blomgren H, Pisa P, Lax I, Kalkner KM, Svedman C. Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma. Acta Oncol 2006;45:493-7.
9. Okuma K, Yamashita H, Niibe Y,Hayakawa K,Nakagawa K. Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: a case report. J Med Case Rep 2011;5:111.
10. Cotter SE, Dunn GP, Collins KM, Sahni D, Zukotynski KA, Hansen JL, et al. Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: potential role of induced antitumor immunity. Arch Dermatol 2011;147:870-2.
11. Kachikwu EL, Iwamoto KS, Liao YP, DeMarco JJ, Agazaryan N, Economou JS, et al. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys 2011;81:1128-35.
12. Postow MA, Harding J, Wolchok JD. Targeting immune checkpoints: releasing the restraints on anti-tumor immunity for patients with melanoma. Cancer J 2012;18:153-9.
13. Stamell EF, Wolchok JD, Gnjatic S, Lee NY, Brownell I. The abscopal effect associated with a systemic anti-melanoma immune response. Int J Radiat Oncol Biol Phys 2013;85:293-5.
14. Topham NJ, Hewitt EW. Natural killer cell cytotoxicity: how do they pull the trigger? Immunology 2009;128:7-15.
15. Janeway CA, Travers P, Walport M, Shlomchik MJ. Immunobiology: The Immune System in Health and Disease. 5th edition ed: Garland Science, New York, NY; 2001.
16. Carnemolla B, Borsi L, Balza E, Castellani P, Meazza R, Berndt A, et al. Enhancement of the antitumor properties of interleukin-2 by its targeted delivery to the tumor blood vessel extracellular matrix. Blood 2002;99: 1659-65.
17. Wang KS, Ritz J, Frank DA. IL-2 induces STAT4 activation in primary NK cells and NK cell lines, but not in T cells. J Immunol 1999;162: 299-304.
18. Krause M, Schmitz M, Noessner E, Skrablin PS, Wehner R, Rieber EP, et al. Adoptive transfer of cytotoxic T-cells for treatment of residual disease after irradiation. Int J Radiat Biol 2007;83:827-36.
19. Payne R, Glenn L, HoenH, Richards B, Smith JW II, Lufkin R, et al. Durable responses and reversible toxicity of high-dose interleukin-2 treatment of melanoma and renal cancer in a Community Hospital Biotherapy Program. J Immunother Cancer 2014;2:13.
20. Alwan LM, Grossmann K, Sageser D, Van Atta J, Agarwal N, Gilreath JA. Comparison of acute toxicity and mortality after two different dosing regimens of high-dose interleukin-2 for patients with metastatic melanoma. Target Oncol 2014;9:63-71.
21. Den Otter W, Jacobs JJ, Battermann JJ, Hordijk GJ, Krastev Z, Moiseeva EV, et al. Local therapy of cancer with free IL-2. Cancer Immunol Immunother 2008;57:931-50.
22. Jacobs JJ, Sparendam D, Den Otter W. Local interleukin 2 therapy is most effective against cancer when injected intratumourally. Cancer Immunol Immunother 2005;54:647-54.
23. Yasuda K, Nirei T, Tsuno NH, Nagawa H, Kitayama J. Intratumoral injection of interleukin-2 augments the local and abscopal effects of radiotherapy in murine rectal cancer. Cancer Sci 2011;102:1257-63.
24. Kontermann RE. Antibody-cytokine fusion proteins. Arch Biochem Biophys 2012;526:194-205.
25. Kaczmarek J, Castellani P, Nicolo G, Spina B, Allemanni G, Zardi L. Distribution of oncofetal fibronectin isoforms in normal, hyperplastic and neoplastic human breast tissues. Int J Cancer 1994;59: 11-6.
26. D'Ovidio MC, Mastracchio A, Marzullo A, Ciabatta M, Pini B, Uccini S, et al. Intratumoral microvessel density and expression of ED-A/ED-B sequences of fibronectin in breast carcinoma. Eur J Cancer 1998;34:1081-5.
27. Pujuguet P, Hammann A, Moutet M, Samuel JL, Martin F, Martin M. Expression of fibronectin ED-A+ and ED-B+ isoforms by human and experimental colorectal cancer. Contribution of cancer cells and tumorassociated myofibroblasts. Am J Pathol 1996;148:579-92.
28. Santimaria M, Moscatelli G, Viale GL, Giovannoni L, Neri G, Viti F, et al. Immunoscintigraphic detection of the ED-B domain of fibronectin, a marker of angiogenesis, in patients with cancer. Clin Cancer Res 2003;9:571-9.
29. El-Emir E, Dearling JL, Huhalov A, Robson MP, Boxer G, Neri D, et al. Characterisation and radioimmunotherapy of L19-SIP, an anti-angiogenic antibody against the extra domain B of fibronectin, in colorectal tumour models. Br J Cancer 2007;96:1862-70.
30. Galler K, Junker K, Franz M, Hentschel J, Richter P, Gajda M, et al. Differential vascular expression and regulation of oncofetal tenascin-C and fibronectin variants in renal cell carcinoma (RCC): implications for an individualized angiogenesis-related targeted drug delivery. HistochemCell Biol 2012;137:195-204.
31. Rossin R, Berndorff D, Friebe M, Dinkelborg LM, Welch MJ. Small-animal PET of tumor angiogenesis using a (76)Br-labeled human recombinant antibody fragment to the ED-B domain of fibronectin. J Nucl Med 2007;48:1172-9.
32. Tijink BM, Perk LR, Budde M, Stigter-van Walsum M, Visser GW, Kloet RW, et al. (124)I-L19-SIP for immuno-PET imaging of tumour vasculature and guidance of (131)I-L19-SIP radioimmunotherapy. Eur J Nucl Med Mol Imaging 2009;36:1235-44.
33. Balza E, Carnemolla B, Mortara L, Castellani P, Soncini D, Accolla RS, et al. Therapy-induced antitumor vaccination in neuroblastomas by the combined targeting of IL-2 and TNFalpha. Int J Cancer 2010;127:101-10.
34. Johannsen M, Spitaleri G, Curigliano G, Roigas J, Weikert S, Kempkensteffen C, et al. The tumour-targeting human L19-IL2 immunocytokine: preclinical safety studies, phase I clinical trial in patients with solid tumours and expansion into patients with advanced renal cell carcinoma. Eur J Cancer 2010;46:2926-35.
35. Eigentler TK, Weide B, de Braud F, Spitaleri G, Romanini A, Pflugfelder A, et al.A dose-escalation and signal-generating study of theimmunocytokine L19-IL2 in combination with dacarbazine for the therapy of patients with metastatic melanoma. Clin Cancer Res 2011;17:7732-42.
36. Hervieu A, Mignot G, Ghiringhelli F. Dacarbazine mediate antimelanoma effects via NK cells. Oncoimmunology 2013;2:e23714.
37. Pfaffen S, Frey K, Stutz I, Roesli C, Neri D. Tumour-targeting properties of antibodies specific to MMP-1A, MMP-2 and MMP-3. Eur J Nucl Med Mol Imaging 2010;37:1559-65.
38. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. Computer control of microscopes using microManager. Curr Protoc Mol Biol 2010;Chapter 14:Unit14 20.
39. Kamrava M, Bernstein MB, Camphausen K, Hodge JW. Combining radiation, immunotherapy, and antiangiogenesis agents in themanagement of cancer: the Three Musketeers or just another quixotic combination? Mol Biosyst 2009;5:1262-70.
40. Schliemann C, Palumbo A, Zuberbuhler K, Villa A, Kaspar M, Trachsel E, et al. Complete eradication of human B-cell lymphoma xenografts using rituximab in combination with the immunocytokine L19-IL2. Blood 2009;113:2275-83.
41. Menrad A, Menssen HD. ED-B fibronectin as a target for antibody-based cancer treatments. Expert Opin Ther Targets 2005;9:491-500.
42. Wagner K, Schulz P, Scholz A, Wiedenmann B, Menrad A. The targeted immunocytokine L19-IL2 efficiently inhibits the growth of orthotopic pancreatic cancer. Clin Cancer Res 2008;14:4951-60.
43. Becker JC, Pancook JD,Gillies SD, Furukawa K, Reisfeld RA. T cell-mediated eradication of murine metastatic melanoma induced by targeted interleukin 2 therapy. J Exp Med 1996;183:2361-6.
44. Xiang R, Lode HN, Dolman CS, Dreier T, Varki NM, Qian X, et al. Elimination of established murine colon carcinoma metastases by antibody-interleukin 2 fusion protein therapy. Cancer Res 1997;57:4948-55.
45. Johnson EE, Yamane BH, Buhtoiarov IN, Lum HD, Rakhmilevich AL, Mahvi DM, et al. Radiofrequency ablation combined with KS-IL2 immunocytokine (EMD 273066) results in an enhanced antitumor effect against murine colon adenocarcinoma. Clin Cancer Res 2009;15:4875-84.
46. Gutbrodt KL, Schliemann C, Giovannoni L, Frey K, Pabst T, Klapper W, et al. Antibody-based delivery of interleukin-2 to neovasculature has potent activity against acute myeloid leukemia. Sci Transl Med 2013; 5:201ra118.
47. Hemmerle T, Neri D. The antibody-based targeted delivery of interleukin-4 and 12 to the tumor neovasculature eradicates tumors in three mouse models of cancer. Int J Cancer 2014;134:467-77.
48. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Tolllike receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9.
49. Schaue D, Ratikan JA, Iwamoto KS, McBride WH. Maximizing tumor immunity with fractionated radiation. Int J Radiat Oncol Biol Phys 2012;83:1306-10.
50. Seung SK, Curti BD, Crittenden M, Walker E, Coffey T, Siebert JC, et al. Phase 1 study of stereotactic body radiotherapy and interleukin-2-tumor and immunological responses. Sci Transl Med 2012;4:137ra74.