Heterogeneous reovirus susceptibility in human glioblastoma stem-like cell cultures

Cancer Gene Therapy

Volumn 20, Issue 9, 2013, Pages 507-513

  Van Den Hengel, S K ^a,b   Balvers, R K ^b   Dautzenberg, I J C ^a   Van Den Wollenberg, D J M ^a   Kloezeman, J J ^b   Lamfers, M L ^b   Sillivis Smit, P A E ^b   Hoeben, R C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

glioblastoma stem like cells; glioma; oncolytic virus; reovirus; virotherapy

Indexed keywords

JUNCTIONAL ADHESION MOLECULE A;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CANCER STEM CELL; CELL POPULATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOLYSIS; FEMALE; FLOW CYTOMETRY; GLIOBLASTOMA; GLIOBLASTOMA STEM LIKE CELL; HUMAN; HUMAN CELL; MALE; MAMMALIAN ORTHOREOVIRUS; MONOLAYER CULTURE; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REOVIRUS INFECTION; WILD TYPE;

MAMMALIAN ORTHOREOVIRUS 3; ORTHOREOVIRUS;

ADULT; AGED; BRAIN NEOPLASMS; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CYTOPATHOGENIC EFFECT, VIRAL; FEMALE; GLIOBLASTOMA; HUMANS; MALE; MIDDLE AGED; NEOPLASTIC STEM CELLS; ONCOLYTIC VIRUSES; RECEPTORS, CELL SURFACE; REOVIRIDAE; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED; VIRAL TROPISM;

EID: 84884595007     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2013.47     Document Type: Article

References (38)

1. Ricard D, Idbaih A, Ducray F, Lahutte M, Hoang-Xuan K, Delattre JY. Primary brain tumours in adults. Lancet 2012; 379: 1984-1996.
2. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-7021. (Pubitemid 39331011)
3. Vescovi A L, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006; 6: 425-436.
4. Bao S, Wu Q, McLendon R E, Hao Y, Shi Q, Hjelmeland A. B et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760. (Pubitemid 44949604)
5. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006; 13: 1238-1241. (Pubitemid 43905604)
6. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR et al. Analysis of gene expression and chemoresistance of CD133\+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
7. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006; 9: 391-403. (Pubitemid 43668737)
8. Vik-Mo EO, Sandberg C, Olstorn H, Varghese M, Brandal P, Ramm-Pettersen J et al. Brain tumor stem cells maintain overall phenotype and tumorigenicity after in vitro culturing in serum-free conditions. Neuro Oncol 2010; 12: 1220-1230.
9. Wollmann G, Ozduman K, van den Pol AN. Oncolytic virus therapy for glioblastoma multiforme: concepts and candidates. Cancer J 2012; 18: 69-81.
10. 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: 103-117.
11. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, Schnell FJ et al. Junction adhesion molecule is a receptor for reovirus. Cell 2001; 104: 441-451. (Pubitemid 32206464)
12. Campbell JA, Schelling P, Wetzel JD, Johnson EM, Forrest JC, Wilson GA et al. Junctional adhesion molecule a serves as a receptor for prototype and fieldisolate strains of mammalian reovirus. J Virol 2005; 79: 7967-7978. (Pubitemid 40853501)
13. van Houdt WJ, Smakman N, Van Den Wollenberg DJ, Emmink BL, Veenendaal LM, van Diest PJ et al. Transient infection of freshly isolated human colorectal tumor cells by reovirus T3D intermediate subviral particles. Cancer Gene Ther 2008; 15: 284-292. (Pubitemid 351508137)
14. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW. Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc Natl Acad Sci USA 2004; 101: 11099-11104. (Pubitemid 38989590)
15. Smakman N, Van Den Wollenberg DJ, Elias SG, Sasazuki T, Shirasawa S, Hoeben RC et al. KRAS(D13) Promotes apoptosis of human colorectal tumor cells by ReovirusT3D and oxaliplatin but not by tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res 2006; 66: 5403-5408. (Pubitemid 43844967)
16. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 1998; 17: 3351-3362. (Pubitemid 28279509)
17. Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol 2012; 30: 658-670.
18. Forsyth P, Roldan G, George D, Wallace C, Palmer CA, Morris D et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008; 16: 627-632. (Pubitemid 351315004)
19. Van Den Wollenberg DJ, Dautzenberg IJ, van den Hengel SK, Cramer SJ, de Groot RJ, Hoeben RC. Isolation of reovirus T3D mutants capable of infecting human tumor cells independent of junction adhesion molecule-A. PLoS One 2012; 7: e48064.
20. Elliott N.T, Yuan F. A review of three-dimensional in vitro tissue models for drug discovery and transport studies. J Pharm Sci. 2011; 100: 59-74.
21. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 2010; 148: 3-15.
22. Grill J, Lamfers ML, van Beusechem VW, Dirven CM, Pherai DS, Kater M et al. The organotypic multicellular spheroid is a relevant three-dimensional model to study adenovirus replication and penetration in human tumors in vitro. Mol Ther 2002; 6: 609-614. (Pubitemid 35363693)
23. Balvers RK, Kleijn A, Kloezeman JJ, French PJ, Kremer A, van den Bent MJ et al. Serum-free culture success of glial tumors is related to specific molecular profiles and expression of extracellular matrix-associated gene modules. Neuro-Oncology 2013 (in press).
24. Fallaux FJ, Kranenburg O, Cramer SJ, Houweling A, Van Ormondt H, Hoeben RC et al. Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther 1996; 7: 215-222. (Pubitemid 26044840)
25. Herrmann R, Fayad W, Schwarz S, Berndtsson M, Linder S. Screening for compounds that induce apoptosis of cancer cells grown as multicellular spheroids. J Biomol Screen 2008; 13: 1-8.
26. Nduom E K, Hadjipanayis CG, Van Meir EG. Glioblastoma cancer stem-like cells: implications for pathogenesis and treatment. Cancer J 2012; 18: 100-106.
27. Alloussi SH, Alkassar M, Urbschat S, Graf N, Gartner B. All reovirus subtypes show oncolytic potential in primary cells of human high-grade glioma. Oncol Rep. 2011; 26: 645-649.
28. 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: 903-912. (Pubitemid 32624647)
29. Coombs KM. Reovirus structure and morphogenesis. Curr Top Microbiol Immunol 2006; 309: 117-167. (Pubitemid 47400276)
30. Schiff LA. Reovirus capsid proteins sigma 3 and mu 1: interactions that influence viral entry, assembly, and translational control. Curr Top Microbiol Immunol 1998; 233: 167-183. (Pubitemid 28194921)
31. Kuriyama N, Kuriyama H, Julin C M, Lamborn K, Israel MA. Pretreatment with protease is a useful experimental strategy for enhancing adenovirus-mediated cancer gene therapy. Hum Gene Ther 2000; 11: 2219-2230.
32. Kuppen PJ, van der Eb MM, Jonges LE, Hagenaars M, Hokland ME, Nannmark U et al. Tumor structure and extracellular matrix as a possible barrier for therapeutic approaches using immune cells or adenoviruses in colorectal cancer. Histochem Cell Biol 2001; 115: 67-72. (Pubitemid 32202055)
33. Lamfers M, Idema S, van Milligen F, Schouten T, van der Valk P, Vandertop P et al. Homing properties of adipose-derived stem cells to intracerebral glioma and the effects of adenovirus infection. Cancer Lett 2009; 274: 78-87.
34. Power AT, Bell JC. Taming the Trojan horse: optimizing dynamic carrier cell/oncolytic virus systems for cancer biotherapy. Gene Ther 2008; 15: 772-779. (Pubitemid 351627361)
35. Willmon C, Harrington K, Kottke T, Prestwich R, Melcher A, Vile R. Cell carriers for oncolytic viruses: Fed Ex for cancer therapy. Mol Ther 2009; 17: 1667-1676.
36. Ilett EJ, Barcena M, Errington-Mais F, Griffin S, Harrington KJ, Pandha HS et al. Internalization of oncolytic reovirus by human dendritic cell carriers protects the virus from neutralization. Clin Cancer Res 2011; 17: 2767-2776.
37. Ilett EJ, Prestwich RJ, Kottke T, Errington F, Thompson JM, Harrington KJ et al. Dendritic cells and T cells deliver oncolytic reovirus for tumour killing despite preexisting anti-viral immunity. Gene Ther 2009; 16: 689-699.
38. Sottoriva A, Spiteri I, Piccirillo S G, Touloumis A, Collins VP, Marioni JC et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 2013; 110: 4009-4014.