Glioblastoma cell lines derived under serum-free conditions can be used as an in vitro model system to evaluate therapeutic response

Cancer Letters

Volumn 305, Issue 1, 2011, Pages 50-57

  Kenney Herbert, Emma M ^a   Ball, Siolian L R ^a   Al Mayhani, Talal M Fael ^a   Watts, Colin ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Drug development; Glioblastoma; Glioblastoma cell line; Model system; PDGF; VEGF

Indexed keywords

PLATELET DERIVED GROWTH FACTOR; PROTEIN ANTIBODY; THROMBOCYTE GROWTH FACTOR ANTIBODY; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR 2;

ADULT; AGED; ANTIBODY RESPONSE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; DRUG RESPONSE; DRUG SCREENING; FEMALE; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION;

AGED; ANTIBODIES; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; PLATELET-DERIVED GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79953219031     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.02.025     Document Type: Article

References (44)

1. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J., Janzer R.C., Ludwin S.K., Allgeier A., Fisher B., Belanger K., Hau P., Brandes A.A., Gijtenbeek J., Marosi C., Vecht C.J., Mokhtari K., Wesseling P., Villa S., Eisenhauer E., Gorlia T., Weller M., Lacombe D., Cairncross J.G., Mirimanoff R.O. 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, 10:459-466.
2. Wick W., Weller M., van den Bent M., Stupp R. Bevacizumab and recurrent malignant gliomas: a European perspective. J. Clin. Oncol. 2010, 28:e188-e189. Author reply e190-e192.
3. Vredenburgh J.J., Desjardins A., Herndon J.E., Marcello J., Reardon D.A., Quinn J.A., Rich J.N., Sathornsumetee S., Gururangan S., Sampson J., Wagner M., Bailey L., Bigner D.D., Friedman A.H., Friedman H.S. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J. Clin. Oncol. 2007, 25:4722-4729.
4. Ali S.A., McHayleh W.M., Ahmad A., Sehgal R., Braffet M., Rahman M., Bejjani G., Friedland D.M. Bevacizumab and irinotecan therapy in glioblastoma multiforme: a series of 13 cases. J. Neurosurg. 2008, 109:268-272.
5. Wen P.Y., Yung W.K., Lamborn K.R., Dahia P.L., Wang Y., Peng B., Abrey L.E., Raizer J., Cloughesy T.F., Fink K., Gilbert M., Chang S., Junck L., Schiff D., Lieberman F., Fine H.A., Mehta M., Robins H.I., DeAngelis L.M., Groves M.D., Puduvalli V.K., Levin V., Conrad C., Maher E.A., Aldape K., Hayes M., Letvak L., Egorin M.J., Capdeville R., Kaplan R., Murgo A.J., Stiles C., Prados M.D. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clin. Cancer Res. 2006, 12:4899-4907.
6. Reardon D.A., Egorin M.J., Quinn J.A., Rich J.N., Gururangan S., Vredenburgh J.J., Desjardins A., Sathornsumetee S., Provenzale J.M., Herndon J.E., Dowell J.M., Badruddoja M.A., McLendon R.E., Lagattuta T.F., Kicielinski K.P., Dresemann G., Sampson J.H., Friedman A.H., Salvado A.J., Friedman H.S. Phase II study of imatinib mesylate plus hydroxyurea in adults with recurrent glioblastoma multiforme. J. Clin. Oncol. 2005, 23:9359-9368.
7. Pietras K., Sjoblom T., Rubin K., Heldin C.H., Ostman A. PDGF receptors as cancer drug targets. Cancer Cell 2003, 3:439-443.
8. Kilic T., Alberta J.A., Zdunek P.R., Acar M., Iannarelli P., O'Reilly T., Buchdunger E., Black P.M., Stiles C.D. Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. Cancer Res. 2000, 60:5143-5150.
9. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., Park J.K., Fine H.A. 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.
10. Fael Al-Mayhani T.M., Ball S.L., Zhao J.W., Fawcett J., Ichimura K., Collins P.V., Watts C. An efficient method for derivation and propagation of glioblastoma cell lines that conserves the molecular profile of their original tumours. J. Neurosci. Methods 2009, 176:192-199.
11. Hicklin D.J., Ellis L.M. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J. Clin. Oncol. 2005, 23:1011-1027.
12. Knizetova P., Ehrmann J., Hlobilkova A., Vancova I., Kalita O., Kolar Z., Bartek J. Autocrine regulation of glioblastoma cell cycle progression, viability and radioresistance through the VEGF-VEGFR2 (KDR) interplay. Cell Cycle 2008, 7:2553-2561.
13. Dresemann G. Imatinib and hydroxyurea in pretreated progressive glioblastoma multiforme: a patient series. Ann. Oncol. 2005, 16:1702-1708.
14. Dresemann G., Weller M., Rosenthal M.A., Wedding U., Wagner W., Engel E., Heinrich B., Mayer-Steinacker R., Karup-Hansen A., Fluge O., Nowak A., Mehdorn M., Schleyer E., Krex D., Olver I.N., Steinbach J.P., Hosius C., Sieder C., Sorenson G., Parker R., Nikolova Z. Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide. J. Neurooncol. 2010, 96:393-402.
15. Bao S., Wu Q., Sathornsumetee S., Hao Y., Li Z., Hjelmeland A.B., Shi Q., McLendon R.E., Bigner D.D., Rich J.N. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006, 66:7843-7848.
16. Plate K.H., Breier G., Weich H.A., Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992, 359:845-848.
17. Katada J., Muramatsu M., Hayashi I., Tsutsumi M., Konishi Y., Majima M. Significance of vascular endothelial cell growth factor up-regulation mediated via a chymase-angiotensin-dependent pathway during angiogenesis in hamster sponge granulomas. J. Pharmacol. Exp. Ther. 2002, 302:949-956.
18. Khasawneh M.K., Bukowski R.M. Pathways of dysregulation in renal cell carcinoma: rational approaches to development of novel treatment. Clin. Genitourin. Cancer 2006, 5(Suppl. 1):S7-S18.
19. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., Oh E.Y., Gaber M.W., Finklestein D., Allen M., Frank A., Bayazitov I.T., Zakharenko S.S., Gajjar A., Davidoff A., Gilbertson R.J. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11:69-82.
20. Reardon D.A., Dresemann G., Taillibert S., Campone M., van den Bent M., Clement P., Blomquist E., Gordower L., Schultz H., Raizer J., Hau P., Easaw J., Gil M., Tonn J., Gijtenbeek A., Schlegel U., Bergstrom P., Green S., Weir A., Nikolova Z. Multicentre phase II studies evaluating imatinib plus hydroxyurea in patients with progressive glioblastoma. Br. J. Cancer 2009, 101:1995-2004.
21. Raymond E., Brandes A.A., Dittrich C., Fumoleau P., Coudert B., Clement P.M., Frenay M., Rampling R., Stupp R., Kros J.M., Heinrich M.C., Gorlia T., Lacombe D., van den Bent M.J. Phase II study of imatinib in patients with recurrent gliomas of various histologies: a European Organisation for Research and Treatment of Cancer Brain Tumor Group Study. J. Clin. Oncol. 2008, 26:4659-4665.
22. Batchelor T.T., Sorensen A.G., di Tomaso E., Zhang W.T., Duda D.G., Cohen K.S., Kozak K.R., Cahill D.P., Chen P.J., Zhu M., Ancukiewicz M., Mrugala M.M., Plotkin S., Drappatz J., Louis D.N., Ivy P., Scadden D.T., Benner T., Loeffler J.S., Wen P.Y., Jain R.K. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11:83-95.
23. Stommel J.M., Kimmelman A.C., Ying H., Nabioullin R., Ponugoti A.H., Wiedemeyer R., Stegh A.H., Bradner J.E., Ligon K.L., Brennan C., Chin L., DePinho R.A. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007, 318:287-290.
24. Shamah S.M., Stiles C.D., Guha A. Dominant-negative mutants of platelet-derived growth factor revert the transformed phenotype of human astrocytoma cells. Mol. Cell Biol. 1993, 13:7203-7212.
25. Friedman H.S., Prados M.D., Wen P.Y., Mikkelsen T., Schiff D., Abrey L.E., Yung W.K., Paleologos N., Nicholas M.K., Jensen R., Vredenburgh J., Huang J., Zheng M., Cloughesy T. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 2009, 27:4733-4740.
26. Kamoun W.S., Ley C.D., Farrar C.T., Duyverman A.M., Lahdenranta J., Lacorre D.A., Batchelor T.T., di Tomaso E., Duda D.G., Munn L.L., Fukumura D., Sorensen A.G., Jain R.K. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J. Clin. Oncol. 2009, 27:2542-2552.
27. Jain R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307:58-62.
28. de Groot J.F., Fuller G., Kumar A.J., Piao Y., Eterovic K., Ji Y., Conrad C.A. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro. Oncol. 2010, 12:233-242.
29. Fleming T.P., Saxena A., Clark W.C., Robertson J.T., Oldfield E.H., Aaronson S.A., Ali I.U. Amplification and/or overexpression of platelet-derived growth factor receptors and epidermal growth factor receptor in human glial tumors. Cancer Res. 1992, 52:4550-4553.
30. Lokker N.A., Sullivan C.M., Hollenbach S.J., Israel M.A., Giese N.A. Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res. 2002, 62:3729-3735.
31. Kesari S., Stiles C.D. The bad seed: PDGF receptors link adult neural progenitors to glioma stem cells. Neuron 2006, 51:151-153.
32. Clarke I.D., Dirks P.B. A human brain tumor-derived PDGFR-alpha deletion mutant is transforming. Oncogene 2003, 22:722-733.
33. Nishikawa R., Ji X.D., Harmon R.C., Lazar C.S., Gill G.N., Cavenee W.K., Huang H.J. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc. Natl. Acad. Sci. USA 1994, 91:7727-7731.
34. Huang H.S., Nagane M., Klingbeil C.K., Lin H., Nishikawa R., Ji X.D., Huang C.M., Gill G.N., Wiley H.S., Cavenee W.K. The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J. Biol. Chem. 1997, 272:2927-2935.
35. Sugawa N., Ekstrand A.J., James C.D., Collins V.P. Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas. Proc. Natl. Acad. Sci. USA 1990, 87:8602-8606.
36. Nieder C., Adam M., Molls M., Grosu A.L. Therapeutic options for recurrent high-grade glioma in adult patients: recent advances. Crit. Rev. Oncol. Hematol. 2006, 60:181-193.
37. Ballman K.V., Buckner J.C., Brown P.D., Giannini C., Flynn P.J., LaPlant B.R., Jaeckle K.A. The relationship between six-month progression-free survival and 12-month overall survival end points for phase II trials in patients with glioblastoma multiforme. Neuro. Oncol. 2007, 9:29-38.
38. Buckner J.C. Factors influencing survival in high-grade gliomas. Semin. Oncol. 2003, 30:10-14.
39. De Witt Hamer P.C., Van Tilborg A.A., Eijk P.P., Sminia P., Troost D., Van Noorden C.J., Ylstra B., Leenstra S. The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 2008, 27:2091-2096.
40. Mao X.G., Zhang X., Xue X.Y., Guo G., Wang P., Zhang W., Fei Z., Zhen H.N., You S.W., Yang H. Brain tumor stem-like cells identified by neural stem cell marker CD15. Transl. Oncol. 2009, 2:247-257.
41. Blough M.D., Westgate M.R., Beauchamp D., Kelly J.J., Stechishin O., Ramirez A.L., Weiss S., Cairncross J.G. Sensitivity to temozolomide in brain tumor initiating cells. Neuro. Oncol. 2010.
42. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
43. Yilmaz O.H., Valdez R., Theisen B.K., Guo W., Ferguson D.O., Wu H., Morrison S.J. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006, 441:475-482.
44. Kreisl T.N., Kim L., Moore K., Duic P., Royce C., Stroud I., Garren N., Mackey M., Butman J.A., Camphausen K., Park J., Albert P.S., Fine H.A. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J. Clin. Oncol. 2009, 27:740-745.