Measles virus causes immunogenic cell death in human melanoma

Gene Therapy

Volumn 20, Issue 1, 2013, Pages 7-15

  Donnelly, O G ^a,b,c   Errington Mais, F ^a   Steele, L ^a   Hadac, E ^b   Jennings, V ^a   Scott, K ^a   Peach, H ^c   Phillips, R M ^d   Bond, J ^a   Pandha, H ^e   Harrington, K ^f   Vile, R ^a,b   Russell, S ^b   Selby, P ^a   Melcher, A A ^a,c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b MAYO CLINIC   (United States)

^c LEEDS TEACHING HOSPITALS NHS TRUST   (United Kingdom)

^d UNIVERSITY OF BRADFORD   (United Kingdom)

^e UNIVERSITY OF SURREY   (United Kingdom)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

HMGB1; immunotherapy; interferon; measles; melanoma; oncolytic

Indexed keywords

ALPHA INTERFERON; ANTINEOPLASTIC AGENT; BETA INTERFERON; GREEN FLUORESCENT PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; INTERFERON; INTERFERON LAMBDA 3; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; INNATE IMMUNITY; MEASLES VIRUS; MELANOMA; NONHUMAN; PRIORITY JOURNAL; VIRAL GENE THERAPY;

CELL DEATH; CELL LINE, TUMOR; HMGB1 PROTEIN; HUMANS; INTERFERON TYPE I; MEASLES VIRUS; MELANOMA; ONCOLYTIC VIRUSES; UP-REGULATION;

MEASLES VIRUS;

EID: 84871985834     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.205     Document Type: Article

References (66)

1. Grote D, Russell SJ, Cornu TI, Cattaneo R, Vile R, Poland GA et al. Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice. Blood 2001; 97: 3746-3754
2. Peng KW, Ahmann GJ, Pham L, Greipp PR, Cattaneo R, Russell SJ et al. Systemic therapy of myeloma xenografts by an attenuated measles virus. Blood 2001; 98: 2002-2007
3. Peng K-W, TenEyck CJ, Galanis E, Kalli KR, Hartmann LC, Russell SJ et al. Intraperitoneal therapy of ovarian cancer using an engineered measles virus. Cancer Res 2002; 62: 4656-4662
4. Phuong LK, Allen C, Peng KW, Giannini C, Greiner S, TenEyck CJ et al. Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiforme. Cancer Res 2003; 63: 2462-2469 (Pubitemid 36605184)
5. Peng K-W, Frenzke M, Myers R, Soeffker D, Harvey M, Greiner S et al. Biodistribution of oncolytic measles virus after intraperitoneal administration into Ifnar-CD46Ge transgenic mice. Hum Gene Ther 2003; 14: 1565-1577 (Pubitemid 37361100)
6. Dingli D, Dingli D, Peng KW, Harvey ME, Greipp PR, O'Connor MK et al. Imageguided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood 2004; 103: 1641-1646 (Pubitemid 38268954)
7. Langfield KK, Wegman TR, Walker HJ, Griesmann GE, Sauer JA, Stephan SA et al. 77. Production and purification of measles virus for oncolytic virotherapy clinical trials. Mol Ther 2004; 9: S31
8. Kunzi V, Oberholzer PA, Heinzerling L, Dummer R, Naim HY. Recombinant measles virus induces cytolysis of cutaneous T-cell lymphoma in vitro and in vivo. J Invest Dermatol 2006; 126: 2525-2532 (Pubitemid 44596153)
9. Hasegawa K, Pham L, O'Connor MK, Federspiel MJ, Russell SJ, Peng KW et al. Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter. Clin Cancer Res 2006; 12: 1868-1875
10. Blechacz B, Splinter PL, Greiner S, Myers R, Peng KW, Federspiel MJ et al. Engineered measles virus as a novel oncolytic viral therapy system for hepatocellular carcinoma. Hepatology 2006; 44: 1465-1477 (Pubitemid 44953652)
11. Zimmermann M, Armeanu S, Smirnow I, Kupka S, Wagner S, Wehrmann M et al. Human precision-cut liver tumor slices as a tumor patient-individual predictive test system for oncolytic measles vaccine viruses. Int J Oncol 2009; 34: 1247-1256
12. Penheiter AR, Wegman TR, Classic KL, Dingli D, Bender CE, Russell SJ et al. Sodium iodide symporter (NIS)-mediated radiovirotherapy for pancreatic cancer. Am J Roentgenol 2010; 195: 341-349
13. Heinzerling L, Künzi V, Oberholzer PA, Kündig T, Naim H, Dummer R et al. Oncolytic measles virus in cutaneous T-cell lymphomas mounts antitumor immune responses in vivo and targets interferon-resistant tumor cells. Blood 2005; 106: 2287-2294 (Pubitemid 41510798)
14. Msaouel P, Dispenzieri A, Galanis E. Clinical testing of engineered oncolytic measles virus strains in the treatment of cancer: an overview. Curr Opin Mol Ther 2009; 11: 43-53
15. Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S et al. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma. Ann Surg Oncol 2010; 17: 718-730
16. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G et al. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol 2009; 27: 5763-5771
17. O'Day S, Hodi FS, McDermott DF, Weber RW, Sosman JA, Haanen JB et al. A phase III, randomized, double-blind, multicenter study comparing monotherapy with ipilimumab or gp100 peptide vaccine and the combination in patients with previously treated, unresectable stage III or IV melanoma. J Clin Oncol 2010; 28: 4
18. Gauvrit A, Brandler S, Sapede-Peroz C, Boisgerault N, Tangy F, Gregoire M et al. Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response. Cancer Res 2008; 68: 4882-4892
19. Kemper C, Atkinson JP. Measles virus and CD46. Curr Top Microbiol Immunol 2009; 329: 31-57
20. Anderson BD, Nakamura T, Russell SJ, Peng K-WHighCD46. Receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res 2004; 64: 4919-4926 (Pubitemid 38924538)
21. Donnelly OG, Errington-Mais F, Prestwich R, Harrington K, Pandha H, Vile R et al. Recent clinical experience with oncolytic viruses. Curr Pharm Biotechnol 2011, e-pub ahead of print 8 July 2011. Available from: http://www. ncbi. nlm. nih. gov/pubmed/21740364. ISN 1873-4316
22. Galanis E, Hartmann LC, Cliby WA, Long HJ, Peethambaram PP, Barrette BA et al. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res 2010; 70: 875-882
23. Prestwich RJ, Errington F, Diaz RM, Pandha HS, Harrington KJ, Melcher AA et al. The case of oncolytic viruses versus the immune system: waiting on the judgment of Solomon. Hum Gene Ther 2009; 20: 1119-1132
24. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Melcher A et al. VSV oncolytic virotherapy in the B16 model depends upon intact MyD88 signaling. Mol Ther 2011; 19: 150-158
25. Prestwich RJ, Ilett EJ, Errington F, Diaz RM, Steele LP, Kottke T et al. Immunemediated antitumor activity of reovirus is required for therapy and is independent of direct viral oncolysis and replication. Clin Cancer Res 2009; 15: 4374-4381
26. Errington F, Steele L, Prestwich R, Harrington KJ, Pandha HS, Vidal L et al. Reovirus activates human dendritic cells to promote innate antitumor immunity. J Immunol 2008; 180: 6018-6026
27. Prestwich RJ, Errington F, Ilett EJ, Morgan RS, Scott KJ, Kottke T et al. Tumor Infection by oncolytic reovirus primes adaptive antitumor immunity. Clin Cancer Res 2008; 14: 7358-7366
28. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 1938; 27: 493
29. Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Meth 2007; 4: 359-365 (Pubitemid 46766981)
30. Evans CJ, Phillips RM, Jones PF, Loadman PM, Sleeman BD, Twelves CJ et al. A mathematical model of doxorubicin penetration through multicellular layers. J Theor Biol 2009; 257: 598-608
31. Errington F, White CL, Twigger KR, Rose A, Scott K, Steele L et al. Inflammatory tumour cell killing by oncolytic reovirus for the treatment of melanoma. Gene Therapy 2008; 15: 1257-1270
32. Kubo H, Ashida A, Matsumoto K, Kageshita T, Yamamoto A, Saida T et al. Interferon-â therapy for malignant melanoma: the dose is crucial for inhibition of proliferation and induction of apoptosis of melanoma cells. Arch Dermatol Res 2008; 300: 297-301
33. Kawai T, Akira S. Innate immune recognition of viral infection. Nat Immunol 2006; 7: 131-137 (Pubitemid 43135878)
34. Pichlmair A, Sousa CRE. Innate Recognition of Viruses. Immunity 2007; 27: 370-383 (Pubitemid 47418682)
35. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13: 1050-1059 (Pubitemid 47517504)
36. Huang B, Sikorski R, Kirn DH, Thorne SH. Synergistic anti-tumor effects between oncolytic vaccinia virus and paclitaxel are mediated by the IFN response and HMGB1. Gene Therapy 2011; 18: 164-172
37. Prestwich RJ, Errington F, Steele LP, Ilett EJ, Morgan RS, Harrington KJ et al. Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J Immunol 2009; 183: 4312-4321
38. White CL, Twigger KR, Vidal L, De Bono JS, Coffey M, Heinemann L et al. Characterization of the adaptive and innate immune response to intravenous oncolytic reovirus (Dearing type 3) during a phase I clinical trial. Gene Therapy 2008; 15: 911-920 (Pubitemid 351791478)
39. Ohgimoto K, Ohgimoto S, Ihara T, Mizuta H, Ishido S, Ayata M et al. Difference in production of infectious wild-type measles and vaccine viruses in monocytederived dendritic cells. Virus Res 2007; 123: 1-8 (Pubitemid 44762250)
40. Schneider-Schaulies S, Schneider-Schaulies J. Measles virus-induced immunosuppression. Curr Top Microbiol Immunol 2009; 330: 243-269
41. Yang L, Carbone DP. Tumor-host immune interactions and dendritic cell dysfunction. Adv Cancer Res 2004; 92: 13-27 (Pubitemid 39458111)
42. Steele L, Errington F, Prestwich R, Ilett E, Harrington K, Pandha H et al. Pro-inflammatory cytokine/chemokine production by reovirus treated melanoma cells is PKR/NFkB mediated and supports innate and adaptive anti-tumour immune priming. Mol Cancer 2011; 10: 20
43. Galivo F, Diaz RM, Wongthida P, Thompson J, Kottke T, Barber G et al. Single-cycle viral gene expression, rather than progressive replication and oncolysis, is required for VSV therapy of B16 melanoma. Gene Therapy 2009; 17: 158-170
44. Liu C, Hasegawa K, Russell SJ, Sadelain M, Peng K-W. Prostate-specific membrane antigen retargeted measles virotherapy for the treatment of prostate cancer. Prostate 2009; 69: 1128-1141
45. Msaouel P, Iankov ID, Allen C, Aderca I, Federspiel MJ, Tindall DJ et al. Noninvasive imaging and radiovirotherapy of prostate cancer using an oncolytic measles virus expressing the sodium iodide symporter. Mol Ther 2009; 17: 2041-2048
46. Iankov ID, Msaouel P, Allen C, Federspiel MJ, Bulur PA, Dietz AB et al. Demonstration of anti-tumor activity of oncolytic measles virus strains in a malignant pleural effusion breast cancer model. Breast Cancer Res Treat 2010; 122: 745-754
47. Myers R, Harvey M, Kaufmann TJ, Greiner SM, Krempski JW, Raffel C et al. Toxicology study of repeat intracerebral administration of a measles virus derivative producing carcinoembryonic antigen in rhesus macaques in support of a phase I/II clinical trial for patients with recurrent gliomas. Hum Gene Ther 2008; 19: 690-698 (Pubitemid 352009918)
48. Dingli D, Offord C, Myers R, Peng KW, Carr TW, Josic K et al. Dynamics of multiple myeloma tumor therapy with a recombinant measles virus. Cancer Gene Ther 2009; 16: 873-882
49. Haralambieva I, Iankov I, Hasegawa K, Harvey M, Russell SJ, Peng KW et al. Engineering oncolytic measles virus to circumvent the intracellular innate immune response. Mol Ther 2007; 15: 588-597
50. Li H, Peng K-W, Dingli D, Kratzke RA, Russell SJ. Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy. Cancer Gene Ther 2010; 17: 550-558
51. Critchley-Thorne RJ, Simons DL, Yan N, Miyahira AK, Dirbas FM, Johnson DL et al. Impaired interferon signaling is a common immune defect in human cancer. Pro Nat Acad Sci 2009; 106: 9010-9015
52. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N et al. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 2000; 6: 821-825 (Pubitemid 30469434)
53. Willmon CL, Saloura V, Fridlender ZG, Wongthida P, Diaz RM, Thompson J et al. Expression of IFN-\{beta\} enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma. Cancer Res 2009; 69: 7713-7720
54. Mocellin S, Pasquali S, Rossi CR, Nitti D. Interferon alpha adjuvant therapy in patients with high-risk melanoma: a systematic review and meta-analysis. J Natl Cancer Inst 2010; 102: 493-501
55. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nature immunol 2004; 5: 987-995 (Pubitemid 41057715)
56. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418: 191-195 (Pubitemid 34773774)
57. Bianchi ME, Manfredi AA. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 2007; 220: 35-46 (Pubitemid 350045574)
58. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5: 331-342 (Pubitemid 40516158)
59. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: endogenous danger signaling. Mol Med 2008; 14: 476-484
60. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Pulido J et al. Type III IFN Interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immunecompetent mouse models of cancer. Cancer Res 2010; 70: 4539-4549
61. Banaszynski LA, Sellmyer MA, Contag CH, Wandless TJ, Thorne SH. Chemical control of protein stability and function in living mice. Nat Med 2008; 14: 1123-1127
62. Ungerechts G, Springfeld C, Frenzke ME, Lampe J, Parker WB, Sorscher EJ et al. An immunocompetent murine model for oncolysis with an armed and targeted measles virus. Mol Ther 2007; 15: 1991-1997 (Pubitemid 350011739)
63. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009; 21: 233-240
64. Duprex WP, McQuaid S, Hangartner L, Billeter MA, Rima BK. Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J Virol 1999; 73: 9568-9575 (Pubitemid 29487112)
65. Radecke F, Spielhofer P, Schneider H, Kaelin K, Huber M, Dö tsch C et al. Rescue of measles viruses from cloned DNA. EMBO J 1995; 14: 5773-5784
66. Errington F, Jones J, Merrick A, Bateman A, Harrington K, Gough M et al. Fusogenic membrane glycoprotein-mediated tumour cell fusion activates human dendritic cells for enhanced IL-12 production and T-cell priming. Gene Therapy 2006; 13: 138-149 (Pubitemid 43039906)