In vitro co-culture model of medulloblastoma and human neural stem cells for drug delivery assessment

Journal of Biotechnology

Volumn 205, Issue , 2015, Pages 3-13

  Ivanov, Delyan P ^a   Parker, Terry L ^a   Walker, David A ^a   Alexander, Cameron ^a   Ashford, Marianne B ^b   Gellert, Paul R ^b   Garnett, Martin C ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Cancer drug screening in 3D; Co culture spheroid; Human stem cell neurosphere; Medulloblastoma; Three dimensional tumor model

Indexed keywords

BRAIN; CELL CULTURE; CELLS; CYTOLOGY; DIAGNOSIS; DRUG DELIVERY; PHYSIOLOGICAL MODELS; TISSUE; TUMORS;

CANCER DRUG; CO-CULTURES; HUMAN STEM CELL NEUROSPHERE; MEDULLOBLASTOMA; TUMOR MODELS;

STEM CELLS;

ANTINEOPLASTIC AGENT; ETOPOSIDE;

BIOLOGICAL MODEL; BRAIN TUMOR; CELL CULTURE; CELL SURVIVAL; COCULTURE; CYTOLOGY; DRUG EFFECTS; DRUG SCREENING; HUMAN; MEDULLOBLASTOMA; MULTICELLULAR SPHEROID; NEURAL STEM CELL; PATHOLOGY; PROCEDURES;

ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG SCREENING ASSAYS, ANTITUMOR; ETOPOSIDE; HUMANS; MEDULLOBLASTOMA; MODELS, BIOLOGICAL; NEURAL STEM CELLS; SPHEROIDS, CELLULAR;

EID: 84939938946     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2015.01.002     Document Type: Article

References (79)

1. Amann A., Zwierzina M., Gamerith G., Bitsche M., Huber J.M., Vogel G.F., Blumer M., Koeck S., Pechriggl E.J., Kelm J.M., Hilbe W., Zwierzina H. Development of an innovative 3D cell culture system to study tumour--stroma interactions in non-small cell lung cancer cells. PLoS One 2014, 9:e92511. 10.1371/journal.pone.0092511.
2. Astashkina A., Mann B., Grainger D.W. A critical evaluation of in vitro cell culture models for high-throughput drug screening and toxicity. Pharmacol. Ther. 2012, 134:82-106. 10.1016/j.pharmthera.2012.01.001.
3. Attenello F., Mukherjee D., Datoo G., McGirt M., Bohan E., Weingart J., Olivi A., Quinones-Hinojosa A., Brem H. Use of gliadel (BCNU) wafer in the surgical treatment of malignant glioma: A 10-Year institutional experience. Ann. Surg. Oncol. 2008, 15:2887-2893.
4. Barbaro N.M., Gupta N., Kunwar S. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration 2004, 427:740-744. 10.1038/nature02298.1.
5. Barua N.U., Lowis S.P., Woolley M., O'Sullivan S., Harrison R., Gill S.S. Robot-guided convection-enhanced delivery of carboplatin for advanced brainstem glioma. Acta Neurochir. (Wien). 2013, 155:1459-1465. 10.1007/s00701-013-1700-6.
6. Begum J., Day W., Henderson C., Purewal S., Cerveira J., Summers H., Rees P., Davies D., Filby A. A method for evaluating the use of fluorescent dyes to track proliferation in cell lines by dye dilution. Cytometry. A 2013, 83:1085-1095. 10.1002/cyto.a.22403.
7. Bhojwani D., Sabin N.D., Pei D., Yang J.J., Khan R.B., Panetta J.C., Krull K.R., Inaba H., Rubnitz J.E., Metzger M.L., Howard S.C., Ribeiro R.C., Cheng C., Reddick W.E., Jeha S., Sandlund J.T., Evans W.E., Pui C.-H., Relling M.V. Methotrexate-induced neurotoxicity and leukoencephalopathy in childhood acute lymphoblastic leukemia. J. Clin. Oncol. 2014, 32:949-959. 10.1200/JCO.;1; 2013.53.0808.
8. Carpenter M.K., Cui X., Hu Z., Jackson J., Sherman S., Wahlberg L.U. In vitro expansion of a multipotent population of human neural progenitor cells 1999, 278:265-278.
9. Carrera S., de Verdier P.J., Khan Z., Zhao B., Mahale A., Bowman K.J., Zainol M., Jones G.D.D., Lee S.W., Aaronson S.A., Macip S. Protection of cells in physiological oxygen tensions against DNA damage-induced apoptosis. J. Biol. Chem. 2010, 285:13658-13665. 10.1074/jbc.M109.062562.
10. Chambers K.F., Pearson J.F., Aziz N., O'Toole P., Garrod D., Lang S.H. Stroma regulates increased epithelial lateral cell adhesion in 3D culture: a role for actin/cadherin dynamics. PLoS One 2011, 6:e18796. 10.1371/journal.pone.0018796.
11. Chintala S.K., Fueyo J., Gomez-Manzano C., Venkaiah B., Bjerkvig R., Yung W.K., Sawaya R., Kyritsis a.P., Rao J.S. Adenovirus-mediated p16/CDKN2 gene transfer suppresses glioma invasion in vitro. Oncogene 1997, 15:2049-2057. 10.1038/sj.onc.1201382.
12. Conroy S., Garnett M., Vloeberghs M., Grundy R., Craven I., Walker D. Medulloblastoma in childhood: revisiting intrathecal therapy in infants and children. Cancer Chemother. Pharmacol. 2010, 65:1173-1189.
13. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712. 10.1126/science.1064829.
14. Deeken J.F., Löscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin. Cancer Res. 2007, 13:1663-1674. 10.1158/1078-0432.CCR-06-2854.
15. Dietrich J., Han R., Yang Y., Mayer-Pröschel M., Noble M. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J. Biol. 2006, 5:22. 10.1186/jbiol50.
16. Duggan, R., 2012. Ryan Duggan's three step approach to gating Annexin V data appropriately [WWW Document]. URL . http://ucflow.blogspot.co.uk/2012/07/my-3-step-approach-to-gating-annexin-v.html.
17. Fang C., Avis I., Salomon D., Cuttitta F. Novel phenotypic fluorescent three-dimensional platforms for high-throughput drug screening and personalized chemotherapy. J. Cancer 2013, 4:402-415. 10.7150/jca.6780.
18. Fleischhack G., Reif S., Hasan C., Jaehde U., Hettmer S., Bode U. Feasibility of intraventricular administration of etoposide in patients with metastatic brain tumours. Br. J. Cancer 2001, 84:1453-1459.
19. Foty R.A., Steinberg M.S. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 2005, 278:255-263. 10.1016/j.ydbio.2004.11.012.
20. Gállego Pérez-Larraya J., Palma J.A., Carmona-Iragui M., Fernández-Torrón R., Irimia P., Rodríguez-Otero P., Panizo C., Martínez-Vila E. Neurologic complications of intrathecal liposomal cytarabine administered prophylactically to patients with non-Hodgkin lymphoma. J. Neurooncol. 2011, 103:603-609. 10.1007/s11060-010-0428-x.
21. Go Y., Chintala S.K., Mohanam S., Gokaslan Z., Venkaiah B., Bjerkvig R., Oka K., Nicolson G.L., Sawaya R., Rao J.S. Inhibition of in vivo tumorigenicity and invasiveness of a human glioblastoma cell line transfected with antisense uPAR vectors. Clin. Exp. Metastasis 1997, 15:440-446.
22. Gregg R.W., Molepo J.M., Monpetit V.J., Mikael N.Z., Redmond D., Gadia M., Stewart D.J. Cisplatin neurotoxicity: the relationship between dosage, time, and platinum concentration in neurologic tissues, and morphologic evidence of toxicity. J. Clin. Oncol. 1992, 10:795-803.
23. Hay M., Thomas D.W., Craighead J.L., Economides C., Rosenthal J. Clinical development success rates for investigational drugs. Nat. Biotechnol. 2014, 32:40-51. 10.1038/nbt.2786.
24. Hickman J.a., Graeser R., de Hoogt R., Vidic S., Brito C., Gutekunst M., van der Kuip H. Three-dimensional models of cancer for pharmacology and cancer cell biology: capturing tumor complexity in vitro/ex vivo. Biotechnol. J. 2014, 9:1115-1128. 10.1002/biot.201300492.
25. Honig M.G., Hume R.I. Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J. Cell Biol. 1986, 103:171-187.
26. Hsiao A.Y., Torisawa Y., Tung Y.-C., Sud S., Taichman R.S., Pienta K.J., Takayama S. Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials 2009, 30:3020-3027. 10.1016/j.biomaterials.2009.02.047.
27. Indovina P., Collini M., Chirico G., Santini M.T. Three-dimensional cell organization leads to almost immediate HRE activity as demonstrated by molecular imaging of MG-63 spheroids using two-photon excitation microscopy. FEBS Lett. 2007, 581:719-726. 10.1016/j.febslet.2007.01.040.
28. Ivanov D.P., Parker T.L., Walker D.A., Alexander C., Ashford M.B., Gellert P.R., Garnett M.C. Multiplexing spheroid volume, resazurin and acid phosphatase viability assays for high-throughput screening of tumour spheroids and stem cell neurospheres. PLoS One 2014, 9:e103817. 10.1371/journal.pone.0103817.
29. Keles G.E., Berger M.S., Srinivasan J., Kolstoe D.D., Bobola M.S., Silber J.R. Establishment and characterization of four human medulloblastoma-derived cell lines. Oncol. Res. 1995, 7:493-503.
30. Khoshyomn S., Penar P.L., McBride W.J., Taatjes D.J. Four-dimensional analysis of human brain tumor spheroid invasion into fetal rat brain aggregates using confocal scanning laser microscopy. J. Neurooncol. 1998, 38:1-10.
31. Kilani R.T., Tamimi Y., Hanel E.G., Wong K.K., Karmali S., Lee P.W.K., Moore R.B. Selective reovirus killing of bladder cancer in a co-culture spheroid model. Virus Res. 2003, 93:1-12. 10.1016/S0168-1702(03)00045-5.
32. Kilani R.T., Tamimi Y., Karmali S., Mackey J., Hanel E.G., Wong K.K., Moore R.B. Selective cytotoxicity of gemcitabine in bladder cancer cell lines. Anticancer. Drugs 2002, 13:557-566.
33. König K., Uchugonova A., Gorjup E. Multiphoton fluorescence lifetime imaging of 3D-stem cell spheroids during differentiation. Microsc. Res. Tech. 2011, 74:9-17. 10.1002/jemt.20866.
34. Kool M., Jones D.T.W., Jäger N., Northcott P., a, Pugh T.J., Hovestadt V., Piro R.M., Esparza L.A., Markant S.L., Remke M., Milde T., Bourdeaut F., Ryzhova M., Sturm D., Pfaff E., Stark S., Hutter S., Seker-Cin H., Johann P., Bender S., Schmidt C., Rausch T., Shih D., Reimand J., Sieber L., Wittmann A., Linke L., Witt H., Weber U.D., Zapatka M., König R., Beroukhim R., Bergthold G., van Sluis P., Volckmann R., Koster J., Versteeg R., Schmidt S., Wolf S., Lawerenz C., Bartholomae C.C., von Kalle C., Unterberg A., Herold-Mende C., Hofer S., Kulozik A.E., von Deimling A., Scheurlen W., Felsberg J., Reifenberger G., Hasselblatt M., Crawford J.R., Grant G.a., Jabado N., Perry A., Cowdrey C., Croul S., Zadeh G., Korbel J.O., Doz F., Delattre O., Bader G.D., McCabe M.G., Collins V.P., Kieran M.W., Cho Y.-J., Pomeroy S.L., Witt O., Brors B., Taylor M.D., Schüller U., Korshunov A., Eils R., Wechsler-Reya R.J., Lichter P., Pfister S.M. Genome sequencing of SHH medulloblastoma predicts genotype-related response to smoothened inhibition. Cancer Cell 2014, 25:393-405. 10.1016/j.ccr.2014.02.004.
35. Koopman G., Reutelingsperger C.P., Kuijten G.a., Keehnen R.M., Pals S.T., van Oers M.H. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994, 84:1415-1420.
36. L Berg E., Hsu Y.-C., Lee J.A. Consideration of the cellular microenvironment: physiologically relevant co-culture systems in drug discovery. Adv. Drug Deliv. Rev. 2014, 69-70:190-204. 10.1016/j.addr.2014.01.013.
37. Langley R.R., Fidler I.J. The seed and soil hypothesis revisited--the role of tumor-stroma interactions in metastasis to different organs. Int. J. Cancer 2011, 128:2527-2535. 10.1002/ijc.26031.
38. Lassailly F., Griessinger E., Bonnet D. Microenvironmental contaminations induced by fluorescent lipophilic dyes used for noninvasive in vitro and in vivo cell tracking. Blood 2010, 115:5347-5354. 10.1182/blood-2009-05-224030.
39. Luo C., Johnston P.J., MacPhail S.H., Banáth J.P., Oloumi A., Olive P.L. Cell fusion studies to examine the mechanism for etoposide resistance in Chinese hamster V79 spheroids. Exp. Cell Res. 1998, 243:282-289. 10.1006/excr.1998.4170.
40. Meng W. Evaluation of a nanoparticle drug delivery vehicle in medulloblastoma and organotypic brain cell cultures 2006, University of Nottingham.
41. Meng W., Kallinteri P., Walker D.A., Parker T.L., Garnett M.C. Evaluation of poly (glycerol-adipate) nanoparticle uptake in an in vitro 3-D brain tumor co-culture model. Exp. Biol. Med. (Maywood). 2007, 232:1100-1108. 10.3181/0612-RM-301.
42. Muldoon L.L., Soussain C., Jahnke K., Johanson C., Siegal T., Smith Q.R., Hall W.a., Hynynen K., Senter P.D., Peereboom D.M., Neuwelt E.a. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J. Clin. Oncol. 2007, 25:2295-2305. 10.1200/JCO.2006.09.9861.
43. Nagato M., Heike T., Kato T., Yamanaka Y., Yoshimoto M., Shimazaki T., Okano H., Nakahata T. Prospective characterization of neural stem cells by flow cytometry analysis using a combination of surface markers. J. Neurosci. Res. 2005, 80:456-466. 10.1002/jnr.20442.
44. Nam C., Doi K., Nakayama H. Etoposide induces G2/M arrest and apoptosis in neural progenitor cells via DNA damage and an ATM/p53-related pathway. Histol. Histopathol. 2010, 25:485-493.
45. Nör C., Sassi F.A., de Farias C.B., Schwartsmann G., Abujamra A.L., Lenz G., Brunetto A.L., Roesler R. The histone deacetylase inhibitor sodium butyrate promotes cell death and differentiation and reduces neurosphere formation in human medulloblastoma cells. Mol. Neurobiol. 2013, 48:533-543. 10.1007/s12035-013-8441-7.
46. Nygaard S.J., Haugland H.K., Laerum O.D., Lund-Johansen M., Bjerkvig R., Tysnes O.B. Dynamic determination of human glioma invasion in vitro. J. Neurosurg. 1998, 89:441-447. 10.3171/jns.1998.89.3.0441.
47. Nygaard S.J., Pedersen P.H., Mikkelsen T., Terzis A.J., Tysnes O.B., Bjerkvig R. Glioma cell invasion visualized by scanning confocal laser microscopy in an in vitro co-culture system. Invasion Metastasis 1995, 15:179-188.
48. Othman R.T., Kimishi I., Bradshaw T.D., Storer L.C.D., Korshunov A., Pfister S.M., Grundy R.G., Kerr I.D., Coyle B. Overcoming multiple drug resistance mechanisms in medulloblastoma. Acta Neuropathol. Commun. 2014, 2:57. 10.1186/2051-5960-2-57.
49. Pambid M.R., Berns R., Adomat H.H., Hu K., Triscott J., Maurer N., Zisman N., Ramaswamy V., Hawkins C.E., Taylor M.D., Dunham C., Guns E., Dunn S.E. Overcoming resistance to Sonic Hedgehog inhibition by targeting p90 ribosomal S6 kinase in pediatric medulloblastoma. Pediatr. Blood Cancer 2014, 61:107-115. 10.1002/pbc.24675.
50. Parish C.R. Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol. Cell Biol. 1999, 77:499-508. 10.1046/j.1440-1711.1999.00877.x.
51. Phan-Lai V., Florczyk S.J., Kievit F.M., Wang K., Gad E., Disis M.L., Zhang M. Three-dimensional scaffolds to evaluate tumor associated fibroblast-mediated suppression of breast tumor specific T cells. Biomacromolecules 2013, 14:1330-1337. 10.1021/bm301928u.
52. Quah B.J.C., Parish C.R. New and improved methods for measuring lymphocyte proliferation in vitro and in vivo using CFSE-like fluorescent dyes. J. Immunol. Methods 2012, 379:1-14. 10.1016/j.jim.2012.02.012.
53. Quiñones-Hinojosa A., Chaichana K. The human subventricular zone: a source of new cells and a potential source of brain tumors. Exp. Neurol. 2007, 205:313-324. 10.1016/j.expneurol.2007.03.016.
54. Rahman C.V., Smith S.J., Morgan P.S., Langmack K.A., Clarke P.A., Ritchie A.A., Macarthur D.C., Rose F.R., Shakesheff K.M., Grundy R.G., Ruman Rahman Adjuvant chemotherapy for brain tumors delivered via a novel intra-cavity moldable polymer matrix. PLoS One 2013, 8:e77435. 10.1371/journal.pone.0077435.
55. Ramaswamy V., Remke M., Bouffet E., Faria C.C., Perreault S., Cho Y.-J., Shih D.J., Luu B., Dubuc A.M., Northcott P.a., Schüller U., Gururangan S., McLendon R., Bigner D., Fouladi M., Ligon K.L., Pomeroy S.L., Dunn S., Triscott J., Jabado N., Fontebasso A., Jones D.T.W., Kool M., Karajannis M.a., Gardner S.L., Zagzag D., Nunes S., Pimentel J., Mora J., Lipp E., Walter A.W., Ryzhova M., Zheludkova O., Kumirova E., Alshami J., Croul S.E., Rutka J.T., Hawkins C., Tabori U., Codispoti K.-E.T., Packer R.J., Pfister S.M., Korshunov A., Taylor M.D. Recurrence patterns across medulloblastoma subgroups: an integrated clinical and molecular analysis. Lancet Oncol. 2013, 14:1200-1207. 10.1016/S1470-2045(13)70449-2.
56. Rangarajan A., Hong S.J., Gifford A., Weinberg R.A. Species- and cell type-specific requirements for cellular transformation. Cancer Cell 2004, 6:171-183. 10.1016/j.ccr.2004.07.009.
57. Samlowski W.E., Robertson B.A., Draper B.K., Prystas E., McGregor J.R. Effects of supravital fluorochromes used to analyze the in vivo homing of murine lymphocytes on cellular function. J. Immunol. Methods 1991, 144:101-115. 10.1016/0022-1759(91)90236-9.
58. Shen D.D., Artru A.a., Adkison K.K. Principles and applicability of CSF sampling for the assessment of CNS drug delivery and pharmacodynamics. Adv. Drug Deliv. Rev. 2004, 56:1825-1857. 10.1016/j.addr.2004.07.011.
59. Shih D.J.H., Northcott P.a., Remke M., Korshunov A., Ramaswamy V., Kool M., Luu B., Yao Y., Wang X., Dubuc A.M., Garzia L., Peacock J., Mack S.C., Wu X., Rolider A., Morrissy a.S., Cavalli F.M.G., Jones D.T.W., Zitterbart K., Faria C.C., Schüller U., Kren L., Kumabe T., Tominaga T., Shin Ra Y., Garami M., Hauser P., Chan J.a., Robinson S., Bognár L., Klekner A., Saad A.G., Liau L.M., Albrecht S., Fontebasso A., Cinalli G., De Antonellis P., Zollo M., Cooper M.K., Thompson R.C., Bailey S., Lindsey J.C., Di Rocco C., Massimi L., Michiels E.M.C., Scherer S.W., Phillips J.J., Gupta N., Fan X., Muraszko K.M., Vibhakar R., Eberhart C.G., Fouladi M., Lach B., Jung S., Wechsler-Reya R.J., Fèvre-Montange M., Jouvet A., Jabado N., Pollack I.F., Weiss W.a., Lee J.-Y., Cho B.-K., Kim S.-K., Wang K.-C., Leonard J.R., Rubin J.B., de Torres C., Lavarino C., Mora J., Cho Y.-J., Tabori U., Olson J.M., Gajjar A., Packer R.J., Rutkowski S., Pomeroy S.L., French P.J., Kloosterhof N.K., Kros J.M., Van Meir E.G., Clifford S.C., Bourdeaut F., Delattre O., Doz F.F., Hawkins C.E., Malkin D., Grajkowska W.a., Perek-Polnik M., Bouffet E., Rutka J.T., Pfister S.M., Taylor M.D. Cytogenetic prognostication within medulloblastoma subgroups. J. Clin. Oncol. 2014, 32:886-896. 10.1200/JCO.2013.50.9539.
60. Shuper a., Stark B., Kornreich L., Cohen I.J., Aviner S., Steinmetz a., Stein J., Goshen Y., Yaniv I. Methotrexate treatment protocols and the central nervous system: significant cure with significant neurotoxicity. J. Child Neurol. 2000, 15:573-580. 10.1177/088307380001500902.
61. Slavc I., Schuller E., Falger J., Günes M., Pillwein K., Czech T., Dietrich W., Rössler K., Dieckmann K., Prayer D., Hainfellner J. Feasibility of long-term intraventricular therapy with mafosfamide (n = 26) and etoposide (n = 11): experience in 26 children with disseminated malignant brain tumors. J. Neurooncol. 2003, 64:239-247.
62. Spink B.C., Cole R.W., Katz B.H., Gierthy J.F., Bradley L.M., Spink D.C. Inhibition of MCF-7 breast cancer cell proliferation by MCF-10A breast epithelial cells in coculture. Cell Biol. Int. 2006, 30:227-238. 10.1016/j.cellbi.2005.11.006.
63. Srivastava V.K., Nalbantoglu J. Flow cytometric characterization of the DAOY medulloblastoma cell line for the cancer stem-like phenotype. Cytometry. A 2008, 73:940-948. 10.1002/cyto.a.20633.
64. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z.R., Du J., Davis A., Mongare M.M., Gould J., Frederick D.T., Cooper Z.A., Chapman P.B., Solit D.B., Ribas A., Lo R.S., Flaherty K.T., Ogino S., Wargo J.A., Golub T.R. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487:500-504. 10.1038/nature11183.
65. Taylor M.D., Northcott P.a., Korshunov A., Remke M., Cho Y.-J., Clifford S.C., Eberhart C.G., Parsons D.W., Rutkowski S., Gajjar A., Ellison D.W., Lichter P., Gilbertson R.J., Pomeroy S.L., Kool M., Pfister S.M. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 2012, 123:465-472. 10.1007/s00401-011-0922-z.
66. Terzis A.J., Dietze A., Vig R.B., Old H.A.R.N. Effects of photodynam ic therapy on gliom a spheroids 1997, 11:196-205.
67. Terzis A.J., Thorsen F., Heese O., Visted T., Bjerkvig R., Dahl O., Arnold H., Gundersen G. Proliferation, migration and invasion of human glioma cells exposed to paclitaxel (Taxol) in vitro. Br. J. Cancer 1997, 75:1744-1752.
68. Thorsen F., Visted T., Lehtolainen P., Ylä-Herttuala S., Bjerkvig R. Release of replication-deficient retroviruses from a packaging cell line: interaction with glioma tumor spheroids in vitro. Int. J. Cancer 1997, 71:874-880.
69. Tomlinson F.H., Lihou M.G., Smith P.J. Comparison of in vitro activity of epipodophyllotoxins with other chemotherapeutic agents in human medulloblastomas. Br. J. Cancer 1991, 64:1051-1059.
70. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., Weissman I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. 2000, 97:14720-14725. 10.1073/pnas.97.26.14720.
71. Upreti M., Jamshidi-Parsian A., Koonce N.A., Webber J.S., Sharma S.K., Asea A.A., Mader M.J., Griffin R.J. Tumor-endothelial cell three-dimensional spheroids: new aspects to enhance radiation and drug therapeutics. Transl. Oncol. 2011, 4:365-376.
72. Urich E., Patsch C., Aigner S., Graf M., Iacone R., Freskgård P.-O. Multicellular self-assembled spheroidal model of the blood brain barrier. Sci. Rep. 2013, 3:1500. 10.1038/srep01500.
73. Van der Gaast A., Sonneveld P., Mans D.R., Splinter T.A. Intrathecal administration of etoposide in the treatment of malignant meningitis: feasibility and pharmacokinetic data. Cancer Chemother. Pharmacol. 1992, 29:335-337.
74. Vanner R.J., Remke M., Gallo M., Selvadurai H.J., Coutinho F., Lee L., Kushida M., Head R., Morrissy S., Zhu X., Aviv T., Voisin V., Clarke I.D., Li Y., Mungall A.J., Moore R.a., Ma Y., Jones S.J.M., Marra M.a., Malkin D., Northcott P.a., Kool M., Pfister S.M., Bader G., Hochedlinger K., Korshunov A., Taylor M.D., Dirks P.B. Quiescent Sox2(+) cells drive hierarchical growth and relapse in sonic hedgehog subgroup medulloblastoma. Cancer Cell 2014, 1-15. 10.1016/j.ccr.2014.05.005.
75. Von Bueren A.O., Oehler C., Shalaby T., von Hoff K., Pruschy M., Seifert B., Gerber N.U., Warmuth-Metz M., Stearns D., Eberhart C.G., Kortmann R.D., Rutkowski S., Grotzer M.a. c-MYC expression sensitizes medulloblastoma cells to radio- and chemotherapy and has no impact on response in medulloblastoma patients. BMC Cancer 2011, 11:74. 10.1186/1471-2407-11-74.
76. Wartenberg M. Tumor-induced angiogenesis studied in confrontation cultures of multicellular tumor spheroids and embryoid bodies grown from pluripotent embryonic stem cells. FASEB J. 2001, 15:995-1005. 10.1096/fj.00-0350com.
77. Weston S.A., Parish C.R. New fluorescent dyes for lymphocyte migration studies, analysis by flow cytometry and fluorescence microscopy. J. Immunol. Methods 1990, 133:87-97.
78. Zanini C., Ercole E., Mandili G., Salaroli R., Poli A., Renna C., Papa V., Cenacchi G., Forni M. Medullospheres from DAOY, UW228 and ONS-76 cells: increased stem cell population and proteomic modifications. PLoS One 2013, 8:e63748. 10.1371/journal.pone.0063748.
79. Zembruski N.C.L., Stache V., Haefeli W.E., Weiss J. 7-Aminoactinomycin D for apoptosis staining in flow cytometry. Anal. Biochem. 2012, 429:79-81. 10.1016/j.ab.2012.07.005.