Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death

International Journal of Cancer

Volumn 136, Issue 5, 2015, Pages E313-E325

  Koks, Carolien A ^a   Garg, Abhishek D ^a   Ehrhardt, Michael ^b   Riva, Matteo ^a   Vandenberk, Lien ^a   Boon, Louis ^c   De Vleeschouwer, Steven ^d,e   Agostinis, Patrizia ^a   Graf, Norbert ^b   Gool, Stefaan W ^a,e  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b SAARLAND UNIVERSITY   (Germany)

^c BIOCEROS   (Netherlands)

^d KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Antitumor immunity; Glioma; Immunogenic cell death; Necroptosis; Newcastle disease virus

Indexed keywords

CALRETICULIN; GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; ONCOLYTIC VIRUS; TUMOR ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; AUTOPHAGY; CANCER SURVIVAL; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; GLIOMA; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; IN VITRO STUDY; IN VIVO STUDY; LONG TERM SURVIVAL; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NECROPTOSIS; NEWCASTLE DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; T CELL DEPLETION; T LYMPHOCYTE; VIROTHERAPY; ANIMAL; APOPTOSIS; C57BL MOUSE; ENZYME IMMUNOASSAY; HUMAN; IMMUNOLOGY; NECROSIS; NEWCASTLE DISEASE VIRUS; ONCOLYTIC VIROTHERAPY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; AUTOPHAGY; FEMALE; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOLOGIC MEMORY; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; NECROSIS; NEWCASTLE DISEASE VIRUS; ONCOLYTIC VIROTHERAPY; T-LYMPHOCYTES; TUMOR CELLS, CULTURED; VIRUS REPLICATION;

EID: 84918574716     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29202     Document Type: Article

References (45)

1. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109.
2. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10:459-66.
3. Stummer W, Pichlmeier U, Meinel T, et al. Fluorescenceguided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006;7:392-401.
4. Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol 2012;30:658-70.
5. Lam HY, Yeap SK, Rasoli M, et al. Safety and clinical usage of newcastle disease virus in cancer therapy. J Biomed Biotechnol 2011;2011:718710.
6. Freeman AI, Zakay-Rones Z, Gomori JM, et al. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol Ther 2006;13:221-8.
7. Alkassar M, Gartner B, Roemer K, et al. The combined effects of oncolytic reovirus plus Newcastle disease virus and reovirus plus parvovirus on U87 and U373 cells in vitro and in vivo. J Neurooncol 2011;104:715-27.
8. Friedman A, Tian JP, Fulci G, et al. Glioma virotherapy: effects of innate immune suppression and increased viral replication capacity. Cancer Res 2006;66:2314-9.
9. Lun X, Alain T, Zemp FJ, et al. Myxoma virus virotherapy for glioma in immunocompetent animal models: optimizing administration routes and synergy with rapamycin. Cancer Res 2010;70:598-608.
10. Geletneky K, Kiprianova I, Ayache A, et al. Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro Oncol 2010;12:804-14.
11. Lun X, Chan J, Zhou H, et al. Efficacy and safety/toxicity study of recombinant vaccinia virus JX-594 in two immunocompetent animal models of glioma. Mol Ther 2010;18:1927-36.
12. Krysko DV, Garg AD, Kaczmarek A, et al. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer 2012;12:860-75.
13. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013;31:51-72.
14. Miyamoto S, Inoue H, Nakamura T, et al. Coxsackievirus B3 is an oncolytic virus with immunostimulatory properties that is active against lung adenocarcinoma. Cancer Res 2012;72:2609-21.
15. Donnelly OG, Errington-Mais F, Steele L, et al. Measles virus causes immunogenic cell death in human melanoma. Gene Ther 2013;20:7-15.
16. Chucholowius HW, Rott R. A new method for purification of myxoviruses by zonal centrifugation with two different sucrose density gradients. Proc Soc Exp Biol Med 1972;140:245-7.
17. Maes W, Rosas GG, Verbinnen B, et al. DC vaccination with anti-CD25 treatment leads to longterm immunity against experimental glioma. Neuro Oncol 2009;11:529-42.
18. Garg AD, Krysko DV, Verfaillie T, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J 2012;31:1062-79.
19. Maes H, Van ES, Krysko DV, et al. BNIP3 supports melanoma cell migration and vasculogenic mimicry by orchestrating the actin cytoskeleton. Cell Death Dis 2014;5:e1127.
20. Hathcock KS. T cell enrichment by nonadherence to nylon. Curr Protoc Immunol 2001; Chapter 3: Unit.
21. Verschuere T, Toelen J, Maes W, et al. Gliomaderived galectin-1 regulates innate and adaptive antitumor immunity. Int J Cancer 2013;134:873-84.
22. Vandenabeele P, Grootjans S, Callewaert N, et al. Necrostatin-1 blocks both RIPK1 and IDO: consequences for the study of cell death in experimental disease models. Cell Death Differ 2013;20:185-7.
23. Whalen MJ, Carlos TM, Dixon CE, et al. Reduced brain edema after traumatic brain injury in mice deficient in P-selectin and intercellular adhesion molecule-1. J Leukoc Biol 2000;67:160-8.
24. Garg AD, Dudek AM, Ferreira GB, et al. ROSinduced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death. Autophagy 2013;9:1292-307.
25. Apetoh L, Ghiringhelli F, Tesniere A, et al. Tolllike receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9.
26. Prins RM, Odesa SK, Liau LM. Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Res 2003;63:8487-91.
27. Russell RC, Yuan HX, Guan KL. Autophagy regulation by nutrient signaling. Cell Res 2014;24:42-57.
28. Martins I, Wang Y, Michaud M, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 2014;21:79-91.
29. Roach PJ. AMPK -> ULK1 -> autophagy. Mol Cell Biol 2011;31:3082-4.
30. Laurie SA, Bell JC, Atkins HL, et al. A phase 1 clinical study of intravenous administration of PV701, an oncolytic virus, using two-step desensitization. Clin Cancer Res 2006;12:2555-62.
31. Chiocca EA, Abbed KM, Tatter S, et al. A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther 2004;10:958-66.
32. Forsyth P, Roldan G, George D, et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008;16:627-32.
33. Markert JM, Liechty PG, Wang W, et al. Phase Ib trial of mutant herpes simplex virus G207 inoculated pre- and post-tumor resection for recurrent GBM. Mol Ther 2009;17:199-207.
34. Ulasov IV, Rivera AA, Nettelbeck DM, et al. An oncolytic adenoviral vector carrying the tyrosinase promoter for glioma gene therapy. Int J Oncol 2007;31:1177-85.
35. Garg AD, Nowis D, Golab J, et al. Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta 2010;1805:53-71.
36. Ravindra PV, Tiwari AK, Sharma B, et al. Newcastle disease virus as an oncolytic agent. Indian J Med Res 2009;130:507-13.
37. Fournier P, Arnold A, Wilden H, et al. Newcastle disease virus induces pro-inflammatory conditions and type I interferon for counter-acting Treg activity. Int J Oncol 2012;40:840-50.
38. Elankumaran S, Rockemann D, Samal SK. Newcastle disease virus exerts oncolysis by both intrinsic and extrinsic caspase-dependent pathways of cell death. J Virol 2006;80:7522-34.
39. Bardeletti G. Respiration and ATP level in BHK21/13S cells during the earlist stages of rubella virus replication. Intervirology 1977;8:100-9.
40. Ando T, Imamura H, Suzuki R, et al. Visualization and measurement of ATP levels in living cells replicating hepatitis C virus genome RNA. PLoS Pathog 2012;8:e1002561.
41. Desbiez C, David C, Mettouchi A, et al. Rep protein of tomato yellow leaf curl geminivirus has an ATPase activity required for viral DNA replication. Proc Natl Acad Sci USA 1995;92:5640-4.
42. Dignam SS, Correia JJ, Nada SE, et al. Activation of the ATPase activity of adeno-associated virus Rep68 and Rep78. Biochemistry 2007;46:6364-74.
43. Alvarez-Breckenridge CA, Yu J, Price R, et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med 2012;18:1827-34.
44. Ogbomo H, Zemp FJ, Lun X, et al. Myxoma virus infection promotes NK lysis of malignant gliomas in vitro and in vivo. PLoS One 2013;8:e66825.
45. Song DZ, Liang Y, Xiao Q, et al. TRAIL is involved in the tumoricidal activity of mouse natural killer cells stimulated by Newcastle disease virus in vitro. Anat Rec (Hoboken) 2013;296:1552-60.