How stemlike are sphere cultures from long-term cancer cell lines? Lessons from mouse glioma models

Journal of Neuropathology and Experimental Neurology

Volumn 73, Issue 11, 2014, Pages 1062-1077

  Ahmad, Mushfika ^a,b,c   Frei, Karl ^b,c   Willscher, Edith ^d   Stefanski, Anja ^e   Kaulich, Kerstin ^f   Roth, Patrick ^a,c   Stühler, Kai ^e   Reifenberger, Guido ^f   Binder, Hans ^d   Weller, Michael ^a,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d Molecular Proteomics Laboratory Center for Biological and Medical Research   (United States)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Expression profiling; Glioma stem cells; Murine glioma; Radiosensitivity; Stemness; Temozolomide

Indexed keywords

CELL MARKER; HERMES ANTIGEN; KI 67 ANTIGEN; TEMOZOLOMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER INCIDENCE; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL GROWTH; CELL LINEAGE; CELL RENEWAL; CLONOGENESIS; CONTROLLED STUDY; DRUG EXPOSURE; FLOW CYTOMETRY; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA CELL; GLIOMA CELL LINE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; IRRADIATION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; NONSPHERE CULTURE; PROTEOMICS; RADIOSENSITIVITY; SPHERE CULTURE; T LYMPHOCYTE; TUMOR RECURRENCE; TUMOR RESISTANCE; ANIMAL; C57BL MOUSE; GLIOMA; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; GLIOMA; MICE; MICE, INBRED C57BL; NEOPLASTIC STEM CELLS;

EID: 84916212569     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000130     Document Type: Article

References (41)

1. Ronning PA, Helseth E, Meling TR, et al. A population-based study on the effect of temozolomide in the treatment of glioblastoma multiforme. Neuro Oncol 2012;14:1178-94
2. Ignatova TN, Kukekov VG, Laywell ED, et al. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002;39:193-206
3. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401
4. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64:7011-21
5. Eramo A, Ricci-Vitiani L, Zeuner A, et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006;13:1238-41
6. Liu GT, Yuan XP, Zeng ZH, et al. Analysis of gene expression and chemoresistance of CDI33(+) cancer stem cells in glioblastoma. Mol Cancer 2006;5:67
7. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756-60
8. Qiang L, Yang Y, Ma YJ, et al. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett 2009;279: 13-21
9. Shen G, Shen F, Shi ZJ, et al. Identification of cancer stem-like cells in the C6 glioma cell line and the limitation of current identification methods. In Vitro Cell Dev-An 2008;44:280-99
10. Zhou XD, Wang XY, Qu FJ, et al. Detection of cancer stem cells from the C6 glioma cell line. J Int Med Res 2009;37:503-10
11. Muto J, Imai T, Ogawa D, et al. RNA-binding protein Musashi1 modulates glioma cell growth through the post-transcriptional regulation of Notch and PI3 kinase/Akt signaling pathways. PLoS One 2012;7:10
12. Pellegatta S, Poliani PL, Corno D, et al. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cellYmediated immune response against malignant gliomas. Cancer Res 2006;66: 10247-52
13. Wu A, Oh S, Wiesner SM, et al. Persistence of CD133+ cells in human and mouse glioma cell lines: Detailed characterization of GL261 glioma cells with cancer stem cell-like properties. Stem cells and development 2008;17:173-94
14. Huszthy PC, Daphu I, Niclou SP, et al. In vivo models of primary brain tumors: Pitfalls and perspectives. Neuro Oncol 2012;14:979-93
15. Serano RD, Pegram CN, Bigner DD. Tumorigenic cell culture lines from a spontaneous VM/Dk murine astrocytoma (SMA). Acta Neuropathol 1980;51:53-64
16. Ausman JI, Shapiro WR, Rall DP. Studies on the chemotherapy of experimental brain tumors: Development of an experimental model. Cancer Res 1970;30:2394-400
17. Fraser H. Astrocytomas in an inbred mouse strain. J Pathol 1971;103: 266-70
18. Binder H, Krohn K, Preibisch S. "Hook"-calibration of GeneChipmicroarrays: Chip characteristics and expression measures. Algorithms Mol Biol 2008;3:11
19. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4:249-64
20. Wirth H, Loffler M, von Bergen M, et al. Expression cartography of human tissues using self organizing maps. BMC Bioinformatics 2011;12:306
21. Hopp L, Wirth H, Fasold M, et al. Portraying the expression landscapes of cancer subtypes: A glioblastoma multiforme and prostate cancer case study. Systems Biomed 2013;1:99-121
22. Wirth H, von Bergen M, Binder H. Mining SOM expression portraits: Feature selection and integrating concepts of molecular function. BioData Mining 2012;5:18
23. Wirth H, von Bergen M, Murugaiyan J, et al. MALDI-typing of infectious algae of the genus Prototheca using SOM portraits. J Microbiol Methods 2012;88:83-97
24. Wang X. Computational analysis of expression of human embryonic stem cell-associated signatures in tumors. BMC Res Notes 2011;4:471
25. Li A, Walling J, Kotliarov Y, et al. Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol Cancer Res 2008;6:21-30
26. Ernst A, Hofmann S, Ahmadi R, et al. Genomic and expression profiling of glioblastoma stem cell-like spheroid cultures identifies novel tumor-relevant genes associated with survival. Clin Cancer Res 2009;15: 6541-50
27. Schulte A, Gunther HS, Phillips HS, et al. A distinct subset of glioma cell lines with stem cell-like properties reflects the transcriptional phenotype of glioblastomas and overexpresses CXCR4 as therapeutic target. Glia 2011;59:590-602
28. Zimmerman HM, Arnold H. Experimental brain tumors: II. Tumors produced with benzpyrene. Am J Pathol 1943;19:939-55
29. Yoshida T, Matsuda Y, Naito Z, et al. CD44 in human glioma correlates with histopathological grade and cell migration. Pathol Int 2012;62: 463-70
30. Wei KC, Huang CY, Chen PY, et al. Evaluation of the prognostic value of CD44 in glioblastoma multiforme. Anticancer Res 2010;30:253-59
31. Anido J, Saez-Borderias A, Gonzalez-Junca A, et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 2010;18:655-68
32. Sun Y, Kong W, Falk A, et al. CD133 (Prominin) negative human neural stem cells are clonogenic and tripotent. PLoS One 2009;4:e5498
33. Joo KM, Kim SY, Jin X, et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest 2008;88:808-15
34. Beier D, Rohrl S, Pillai DR, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 2008;68:5706-15
35. Doetsch F, Caille I, Lim DA, et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-16
36. Pollard SM, Yoshikawa K, Clarke ID, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009;4:568-90
37. Gravel M, Gao E, Hervouet-Zeiber C, et al. Transcriptional regulation of 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene expression by cyclic AMP in C6 cells. J Neurochem 2000;75:1940-50
38. Scherer SS, Braun PE, Grinspan J, et al. Differential regulation of the 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene during oligodendrocyte development. Neuron 1994;12:1363-75
39. Weller M, van den Bent M, Hopkins K, et al. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 2014;15:e395-403
40. Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: A critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 2011;8: 486-98
41. Barrett LE, Granot Z, Coker C, et al. Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 2012;21:11-24