Cellular factors promoting resistance to effective treatment of glioma with oncolytic myxoma virus

Cancer Research

Volumn 74, Issue 24, 2014, Pages 7260-7273

  Zemp, Franz J ^a   McKenzie, Brienne A ^a   Lun, Xueqing ^a   Reilly, Karlyne M ^b   McFadden, Grant ^c   Yong, V Wee ^d   Forsyth, Peter A ^a,e  

^a UNIVERSITY OF CALGARY   (Canada)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; ONCOLYTIC MYXOMA VIRUS; ONCOLYTIC VIRUS; UNCLASSIFIED DRUG; RAPAMYCIN;

ABLATION THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL INFILTRATION; CELL POPULATION; CONTROLLED STUDY; DRUG CLEARANCE; DRUG EFFICACY; FEMALE; FLOW CYTOMETRY; GLIOMA; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; MONOTHERAPY; MOUSE; MYXOMA VIRUS; NATURAL KILLER CELL; NONHUMAN; T LYMPHOCYTE; VIROTHERAPY; VIRUS INFECTION; ANIMAL; BRAIN NEOPLASMS; CELLULAR IMMUNITY; DRUG SCREENING; HUMAN; IMMUNOLOGY; ONCOLYTIC VIROTHERAPY; TUMOR CELL LINE; VIROLOGY;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; FLOW CYTOMETRY; GLIOMA; HUMANS; IMMUNITY, CELLULAR; KILLER CELLS, NATURAL; MICE; MYXOMA VIRUS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; SIROLIMUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84917709275     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0876     Document Type: Article

References (49)

1. Canadian Cancer Society. Available from: http://www.cancer.ca/en
2. Cancer Facts and Figures 2014. American Cancer Society. Available from: http://www.cancer.org/
3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
4. Zemp FJ, Corredor JC, Lun X, Muruve DA, Forsyth PA. Oncolytic viruses as experimental treatments for malignant gliomas: using a scourge to treat a devil. Cytokine Growth Factor Rev 2010;21:103-17.
5. Kaufmann JK, Chiocca EA. Glioma virus therapies between bench and bedside. Neuro Oncol 2014;16:334-51.
6. Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol 2012;30:658-70.
7. Conrad C, Miller CR, Ji Y, Gomez-Manzano C, Bharara S, McMurray JS, et al. Delta24-hyCD adenovirus suppresses glioma growth in vivo by combining oncolysis and chemosensitization. Cancer Gene Ther 2005;12:284-94.
8. Mineta T, Rabkin SD, Yazaki T, Hunter WD, Martuza RL. Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat Med 1995;1:938-43.
9. Gromeier M, Lachmann S, Rosenfeld MR, Gutin PH, Wimmer E. Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci U S A 2000;97:6803-08.
10. Wilcox ME, Yang W, Senger D, Rewcastle NB, Morris DG, Brasher PM, et al. Reovirus as an oncolytic agent against experimental human malignant gliomas. J Natl Cancer Inst 2001;93:903-12.
11. Zemp FJ, McKenzie BA, Lun X, Maxwell L, Reilly KM, McFadden G, et al. Resistance to oncolytic myxoma virus therapy in nf1(-/-)/trp53(-/-) syngeneic mouse glioma models is independent of anti-viral type-I interferon. PLoS ONE 2013;8:e65801.
12. Hellums EK, Markert JM, Parker JN, He B, Perbal B, Roizman B, et al. Increased efficacy of an interleukin-12-secreting herpes simplex virus in a syngeneic intracranial murine glioma model. Neuro Oncol 2005; 7:213-24.
13. Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr, Zaupa C, Aghi M, et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 2009;69:3472-81.
14. Lun X, Chan J, Zhou H, Sun B, Kelly JJ, Stechishin OO, et al. Effi cacy and safety/toxicity study of recombinant vaccinia virus JX- 594 in two immunocompetent animal models of glioma. Mol Ther 2010;18:1927-36.
15. Lun X, Alain T, Zemp FJ, Zhou H, Rahman MM, Hamilton MG, et al. Myxoma virus virotherapy for glioma in immunocompetent animal models: optimizing administration routes and synergy with rapamycin. Cancer Res 2010;70:598-608.
16. Zemp FJ, Lun X, McKenzie BA, Zhou H, Maxwell L, Sun B, et al. Treating brain tumor-initiating cells using a combination of myxoma virus and rapamycin. Neuro Oncol 2013;15:904-20.
17. Ogbomo H, Zemp FJ, Lun X, Zhang J, Stack D, Rahman MM, et al. Myxoma virus infection promotes NK lysis of malignant gliomas in vitro and in vivo. PLoS ONE 2013;8:e66825.
18. Lun XQ, Zhou H, Alain T, Sun B, Wang L, Barrett JW, et al. Targeting human medulloblastoma: oncolytic virotherapy with myxoma virus is enhanced by rapamycin. Cancer Res 2007;67:8818-27.
19. Lun X, Yang W, Alain T, Shi ZQ, Muzik H, Barrett JW, et al. Myxoma virus is a novel oncolytic viruswith significant antitumor activity against experimental human gliomas. Cancer Res 2005;65:9982-90.
20. Markert JM, Liechty PG, Wang W, Gaston S, Braz E, Karrasch M, 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.
21. Papanastassiou V, Rampling R, Fraser M, Petty R, Hadley D, Nicoll J, et al. The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther 2002;9:398-406.
22. Fulci G, Breymann L, Gianni D, Kurozomi K, Rhee SS, Yu J, et al. Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses. Proc Natl Acad Sci U S A 2006;103: 12873-78.
23. Fulci G, Dmitrieva N, Gianni D, Fontana EJ, Pan X, Lu Y, et al. Depletion of peripheral macrophages and brain microglia increases brain tumor titers of oncolytic viruses. Cancer Res 2007;67:9398-406.
24. Allen C, Vongpunsawad S, Nakamura T, James CD, Schroeder M, Cattaneo R, et al. Retargeted oncolytic measles strains entering via the EGFRvIII receptor maintain signi ficant antitumor activity against gliomas with increased tumor speci ficity. Cancer Res 2006;66: 11840-50.
25. Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol 2006;8:261-79.
26. Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg 2009;110:572-82.
27. Roggendorf W, Strupp S, Paulus W. Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol 1996;92:288-93.
28. Alvarez-Breckenridge CA, Yu J, Price R, Wei M, Wang Y, Nowicki MO, et al. The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/T-BET signaling and generation of gamma interferon. J Virol 2012;86:4566-77.
29. Alvarez-Breckenridge CA, Yu J, Price R, Wojton J, Pradarelli J, Mao H, et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med 2012;18:1827-34.
30. Reilly KM, Loisel DA, Bronson RT, McLaughlin ME, Jacks T. Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat Genet 2000;26:109-13.
31. Wennier ST, Liu J, Li S, Rahman MM, Mona M, McFadden G. Myxoma virus sensitizes cancer cells to gemcitabine and is an effective oncolytic virotherapeutic in models of disseminated pancreatic cancer. Mol Ther 2012;20:759-68.
32. Smallwood SE, Rahman MM, Smith DW, McFadden G. Myxoma virus: propagation, purification, quantification, and storage. Curr Protoc Microbiol 2010;Chapter 14: Unit 14A 11.
33. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011;91:461-553.
34. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 2001;193:713-26.
35. Schilling M, Strecker JK, Ringelstein EB, Schabitz WR, Kiefer R. The role of CC chemokine receptor 2 on microglia activation and bloodborne cell recruitment after transient focal cerebral ischemia in mice. Brain Res 2009;1289:79-84.
36. Lim JK, Obara CJ, Rivollier A, Pletnev AG, Kelsall BL, Murphy PM. Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J Immunol 2011;186:471-8.
37. Sunderkotter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004;172:4410-7.
38. Huitinga I, van Rooijen N, de Groot CJ, Uitdehaag BM, Dijkstra CD. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med 1990;172:1025-33.
39. Liu WT, Huang CY, Lu IC, Gean PW. Inhibition of glioma growth by minocycline is mediated through endoplasmic reticulum stressinduced apoptosis and autophagic cell death. Neuro Oncol 2013;15:1127-41.
40. Campbell JH, Burdo TH, Autissier P, Bombardier JP, Westmoreland SV, Soulas C, et al. Minocycline inhibition of monocyte activation correlates with neuronal protection in SIV neuroAIDS. PLoS ONE 2011;6:e18688.
41. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 1998;95:15769-74.
42. Cao X, Shores EW, Hu-Li J, Anver MR, Kelsall BL, Russell SM, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995;2:223-38.
43. Lun XQ, Jang JH, Tang N, Deng H, Head R, Bell JC, et al. Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide. Clin Cancer Res 2009;15:2777-88.
44. Vantourout P, Hayday A. Six-of-the-best: unique contributions of gammadelta T cells to immunology. Nat Rev Immunol 2013;13: 88-100.
45. Juno JA, Keynan Y, Fowke KR. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 2012;8:e1002838.
46. Brait VH, Arumugam TV, Drummond GR, Sobey CG. Importance of T lymphocytes in brain injury, immunodeficiency, and recovery after cerebral ischemia. J Cereb Blood Flow Metab 2012;32:598-611.
47. Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 2013;31:413-41.
48. Chiocca EA, Rabkin SD. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol Res 2014;2:295-300.
49. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A 2013;110:4009-14.