The Human Glioblastoma Cell Culture Resource: Validated Cell Models Representing All Molecular Subtypes

EBioMedicine

Volumn 2, Issue 10, 2015, Pages 1351-1363

  Xie, Yuan ^a   Bergström, Tobias ^a   Jiang, Yiwen ^a   Johansson, Patrik ^a   Marinescu, Voichita Dana ^a   Lindberg, Nanna ^b   Segerman, Anna ^a   Wicher, Grzegorz ^a   Niklasson, Mia ^a   Baskaran, Sathishkumar ^a   Sreedharan, Smitha ^a   Everlien, Isabelle ^a   Kastemar, Marianne ^a   Hermansson, Annika ^a   Elfineh, Lioudmila ^a   Libard, Sylwia ^a   Holland, Eric Charles ^b   Hesselager, Göran ^c   Alafuzoff, Irina ^a   Westermark, Bengt ^a   Nelander, Sven ^a   Forsberg Nilsson, Karin ^a   Uhrbom, Lene ^a   more..

^a UPPSALA UNIVERSITY   (Sweden)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Cell culture; Glioblastoma; Molecular subtype; Stem cell culture condition; Xenograft models

Indexed keywords

NESTIN; TRANSCRIPTION FACTOR SOX2; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL PROLIFERATION; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHORT TANDEM REPEAT; SURVIVAL; ADULT; AGED; ANIMAL; BIOBANK; CANCER GRADING; CANCER STAGING; CELL TRANSFORMATION; CLUSTER ANALYSIS; COPY NUMBER VARIATION; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; GENOMIC INSTABILITY; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; TUMOR CELL CULTURE; TUMOR CELL LINE; VERY ELDERLY; XENOGRAFT; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BIOLOGICAL SPECIMEN BANKS; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; DNA COPY NUMBER VARIATIONS; GENE EXPRESSION PROFILING; GENOMIC INSTABILITY; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; TUMOR CELLS, CULTURED; YOUNG ADULT;

EID: 84949758707     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.08.026     Document Type: Article

References (57)

1. Babateen O., Jin Z., Bhandage A., Korol S.V., Westermark B., Forsberg Nilsson K., Uhrbom L., Smits A., Birnir B. Etomidate, propofol and diazepam potentiate GABA-evoked GABAA currents in a cell line derived from human glioblastoma. Eur. J. Pharmacol. 2015, 748:101-107.
2. Balvers R.K., Kleijn A., Kloezeman J.J., French P.J., Kremer A., Van Den Bent M.J., Dirven C.M., Leenstra S., Lamfers M.L. Serum-free culture success of glial tumors is related to specific molecular profiles and expression of extracellular matrix-associated gene modules. Neuro Oncol. 2013, 15:1684-1695.
3. 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.
4. Barretina J., Caponigro G., Stransky N., Venkatesan K., Margolin A.A., Kim S., Wilson C.J., Lehar J., Kryukov G.V., Sonkin D., Reddy A., Liu M., Murray L., Berger M.F., Monahan J.E., Morais P., Meltzer J., Korejwa A., Jane-Valbuena J., Mapa F.A., Thibault J., Bric-Furlong E., Raman P., Shipway A., Engels I.H., Cheng J., Yu G.K., Yu J., Aspesi P., Jr., De Silva M., Jagtap K., Jones M.D., Wang L., Hatton C., Palescandolo E., Gupta S., Mahan S., Sougnez C., Onofrio R.C., Liefeld T., Macconaill L., Winckler W., Reich M., Li N., Mesirov J.P., Gabriel S.B., Getz G., Ardlie K., Chan V., Myer V.E., Weber B.L., Porter J., Warmuth M., Finan P., Harris J.L., Meyerson M., Golub T.R., Morrissey M.P., Sellers W.R., Schlegel R., Garraway L.A. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012, 483:603-607.
5. Beier D., Hau P., Proescholdt M., Lohmeier A., Wischhusen J., Oefner P.J., Aigner L., Brawanski A., Bogdahn U., Beier C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007, 67:4010-4015.
6. Bhang H.E.C., Ruddy D.A., Radhakrishna V.K., Caushi J.X., Zhao R., Hims M.M., Singh A.P., Kao I., Rakiec D., Shaw P., Balak M., Raza A., Ackley E., Keen N., Schlabach M.R., Palmer M., Leary R.J., Chiang D.Y., Sellers W.R., Michor F., Cooke V.G., Korn J.M., Stegmeier F. Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nat. Med. 2015, 21:440-448.
7. Bhat K.P., Balasubramaniyan V., Vaillant B., Ezhilarasan R., Hummelink K., Hollingsworth F., Wani K., Heathcock L., James J.D., Goodman L.D., Conroy S., Long L., Lelic N., Wang S., Gumin J., Raj D., Kodama Y., Raghunathan A., Olar A., Joshi K., Pelloski C.E., Heimberger A., Kim S.H., Cahill D.P., Rao G., Den Dunnen W.F., Boddeke H.W., Phillips H.S., Nakano I., Lang F.F., Colman H., Sulman E.P., Aldape K. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell 2013, 24:331-346.
8. Bleau A.M., Hambardzumyan D., Ozawa T., Fomchenko E.I., Huse J.T., Brennan C.W., Holland E.C. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009, 4:226-235.
9. Brennan C.W., Verhaak R.G.W., McKenna A., Campos B., Noushmehr H., Salama S.R., Zheng S.Y., Chakravarty D., Sanborn J.Z., Berman S.H., Beroukhim R., Bernard B., WU C.J., Genovese G., Shmulevich I., Barnholtz-Sloan J., Zou L.H., Vegesna R., Shukla S.A., Ciriello G., Yung W.K., Zhang W., Sougnez C., Mikkelsen T., Aldape K., Bigner D.D., Van Meir E.G., Prados M., Sloan A., Black K.L., Eschbacher J., Finocchiaro G., Friedman W., Andrews D.W., Guha A., Iacocca M., O'neill B.P., Foltz G., Myers J., Weisenberger D.J., Penny R., Kucherlapati R., Perou C.M., Hayes D.N., Gibbs R., Marra M., Mills G.B., Lander E., Spellman P., Wilson R., Sander C., Weinstein J., Meyerson M., Gabriel S., Laird P.W., Haussler D., Getz G., Chin L., Network T.R. The somatic genomic landscape of glioblastoma. Cell 2013, 155:462-477.
10. Capes-Davis A., Theodosopoulos G., Atkin I., Drexler H.G., Kohara A., Macleod R.A., Masters J.R., Nakamura Y., Reid Y.A., Reddel R.R., Freshney R.I. Check your cultures! A list of cross-contaminated or misidentified cell lines. Int. J. Cancer 2010, 127:1-8.
11. Charles N.A., Holland E.C., Gilbertson R., Glass R., Kettenmann H. The brain tumor microenvironment. Glia 2011, 59:1169-1180.
12. Chen J., Li Y., Yu T.S., Mckay R.M., Burns D.K., Kernie S.G., Parada L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488:522-526.
13. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.-L., Cattaneo E., Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3:e283.
14. Dahlstrand J., Collins V.P., Lendahl U. Expression of the class VI intermediate filament nestin in human central nervous system tumors. Cancer Res. 1992, 52:5334-5341.
15. Dolecek T.A., Propp J.M., Stroup N.E., Kruchko C. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro-Oncology 2012, 14(Suppl. 5):v1-v49.
16. Fael Al-mayhani T.M., Ball S.L.R., 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.
17. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
18. Garnett M.J., Edelman E.J., Heidorn S.J., Greenman C.D., Dastur A., Lau K.W., Greninger P., Thompson I.R., Luo X., Soares J., Liu Q., Iorio F., Surdez D., Chen L., Milano R.J., Bignell G.R., Tam A.T., Davies H., Stevenson J.A., Barthorpe S., Lutz S.R., Kogera F., Lawrence K., McLaren-Douglas A., Mitropoulos X., Mironenko T., Thi H., Richardson L., Zhou W., Jewitt F., Zhang T., O'Brien P., Boisvert J.L., Price S., Hur W., Yang W., Deng X., Butler A., Choi H.G., Chang J.W., Baselga J., Stamenkovic I., Engelman J.A., Sharma S.V., Delattre O., Saez-Rodriguez J., Gray N.S., Settleman J., Futreal P.A., Haber D.A., Stratton M.R., Ramaswamy S., McDermott U., Benes C.H. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012, 483:570-575.
19. Graham V., Khudyakov J., Ellis P., Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39:749-765.
20. Hemmati H.D., Nakano I., Lazareff J.A., Masterman-Smith M., Geschwind D.H., Bronner-Fraser M., Kornblum H.I. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15178-15183.
21. Ignatova T.N., Kukekov V.G., Laywell E.D., Suslov O.N., Vrionis F.D., Steindler D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002, 39:193-206.
22. James G., Witten D., Hastie T., Tibshirani R. An Introduction to Statistical Learning: With Applications in R 2013, Springer, New York.
23. Joo K.M., Kim J., Jin J., Kim M., Seol H.J., Muradov J., Yang H., Choi Y.L., Park W.Y., Kong D.S., Lee J.I., Ko Y.H., Woo H.G., Lee J., Kim S., Nam D.H. Patient-specific orthotopic glioblastoma xenograft models recapitulate the histopathology and biology of human glioblastomas in situ. Cell Rep. 2013, 3:260-273.
24. Kastenhuber E.R., Huse J.T., Berman S.H., Pedraza A., Zhang J., Suehara Y., Viale A., Cavatore M., Heguy A., Szerlip N., Ladanyi M., Brennan C.W. Quantitative assessment of intragenic receptor tyrosine kinase deletions in primary glioblastomas: their prevalence and molecular correlates. Acta Neuropathol. 2014, 127:747-759.
25. Kitambi S.S., Toledo E.M., Usoskin D., Wee S., Harisankar A., Svensson R., Sigmundsson K., Kalderen C., Niklasson M., Kundu S., Aranda S., Westermark B., Uhrbom L., Andang M., Damberg P., Nelander S., Arenas E., Artursson P., Walfridsson J., Forsberg Nilsson K., Hammarstrom L.G., Ernfors P. Vulnerability of glioblastoma cells to catastrophic vacuolization and death induced by a small molecule. Cell 2014, 157:313-328.
26. Laks D.R., Masterman-Smith M., Visnyei K., Angenieux B., Orozco N.M., Foran I., Yong W.H., Vinters H.V., Liau L.M., Lazareff J.A., Mischel P.S., Cloughesy T.F., Horvath S., Kornblum H.I. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 2009, 27:980-987.
27. Lathia J.D., Gallagher J., Heddleston J.M., Wang J., Eyler C.E., Macswords J., Wu Q., Vasanji A., Mclendon R.E., Hjelmeland A.B., Rich J.N. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010, 6:421-432.
28. 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.
29. Lendahl U., Zimmerman L.B., McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 1990, 60:585-595.
30. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
31. Mahesparan R., Read T.-A., Lund-Johansen M., Skaftnesmo K., Bjerkvig R., Engebraaten O. Expression of extracellular matrix components in a highly infiltrative in vivo glioma model. Acta Neuropathol. 2003, 105:49-57.
32. Mayrhofer M., Dilorenzo S., Isaksson A. Patchwork: allele-specific copy number analysis of whole-genome sequenced tumor tissue. Genome Biol. 2013, 14:R24.
33. Meyer M., Reimand J., Lan X., Head R., Zhu X., Kushida M., Bayani J., Pressey J.C., Lionel A.C., Clarke I.D., Cusimano M., Squire J.A., Scherer S.W., Bernstein M., Woodin M.A., Bader G.D., Dirks P.B. Single cell-derived clonal analysis of human glioblastoma links functional and genomic heterogeneity. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:851-856.
34. Nilsson J., Fioretos T., Hoglund M., Fontes M. Approximate geodesic distances reveal biologically relevant structures in microarray data. Bioinformatics 2004, 20:874-880.
35. Noushmehr H., Weisenberger D.J., Diefes K., Phillips H.S., Pujara K., Berman B.P., Pan F., Pelloski C.E., Sulman E.P., Bhat K.P., Verhaak R.G.W., Hoadley K.A., Hayes D.N., Perou C.M., Schmidt H.K., Ding L., Wilson R.K., Van Den Berg D., Shen H., Bengtsson H., Neuvial P., Cope L.M., Buckley J., Herman J.G., Baylin S.B., Laird P.W., Aldape K., Network C.G.A.R. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
36. Ogden A.T., Waziri A.E., Lochhead R.A., Fusco D., Lopez K., Ellis J.A., Kang J., Assanah M., Mckhann G.M., Sisti M.B., McCormick P.C., Canoll P., Bruce J.N. Identification of AB25+CD133-tumor-initiating cells in adult human gliomas. Neurosurgery 2008, 62:505-515.
37. Ostrom Q.T., Gittleman H., Liao P., Rouse C., Chen Y., Dowling J., Wolinsky Y., Kruchko C., Barnholtz-Sloan J. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neuro Oncol. 2014, Suppl. 4:iv1-iv63.
38. Patel A.P., Tirosh I., Trombetta J.J., Shalek A.K., Gillespie S.M., Wakimoto H., Cahill D.P., Nahed B.V., Curry W.T., Martuza R.L., Louis D.N., Rozenblatt-Rosen O., Suva M.L., Regev A., Bernstein B.E. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014, 344:1396-1401.
39. Phillips H.S., Kharbanda S., Chen R., Forrest W.F., Soriano R.H., Wu T.D., Misra A., Nigro J.M., Colman H., Soroceanu L., Williams P.M., Modrusan Z., Feuerstein B.G., Aldape K. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006, 9:157-173.
40. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., Squire J.A., Smith A., Dirks P. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
41. Pontén J., Macintyre E.H. Long term culture of normal and neoplastic human glia. Acta Pathol. Microbiol. Scand. 1968, 74:465-486.
42. Savary K., Caglayan D., Caja L., Tzavlaki K., Bin Nayeem S., Bergstrom T., Jiang Y., Uhrbom L., Forsberg-Nilsson K., Westermark B., Heldin C.H., Ferletta M., Moustakas A. Snail depletes the tumorigenic potential of glioblastoma. Oncogene 2013, 32:5409-5420.
43. Scherf U., Ross D.T., Waltham M., Smith L.H., Lee J.K., Tanabe L., Kohn K.W., Reinhold W.C., Myers T.G., Andrews D.T., Scudiero D.A., Eisen M.B., Sausville E.A., Pommier Y., Botstein D., Brown P.O., Weinstein J.N. A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 2000, 24:236-244.
44. Schmidt L., Kling T., Monsefi N., Olsson M., Hansson C., Baskaran S., Lundgren B., Martens U., Haggblad M., Westermark B., Forsberg Nilsson K., Uhrbom L., Karlsson-Lindahl L., Gerlee P., Nelander S. Comparative drug pair screening across multiple glioblastoma cell lines reveals novel drug-drug interactions. Neuro Oncol. 2013, 15:1469-1478.
45. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., Frotscher M., Snyder E.Y. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Methods 2006, 3:801-806.
46. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63:5821-5828.
47. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
48. Son M.J., Woolard K., Nam D.-H., Lee J., Fine H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4:440-452.
49. Sottoriva A., Spiteri I., Piccirillo S.G., Touloumis A., Collins V.P., Marioni J.C., Curtis C., Watts C., Tavare S. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4009-4014.
50. Stupp R., Mason W.P., Van Den Bent M.J., Weller M., Fisher B., Taphoorn M.J.B., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O., European Organisation For Research And Treatment Of Cancer Brain Tumor And Radiotherapy Groups & National Cancer Institute Of Canada Clinical Trials Group Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
51. Suslov O.N. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc. Natl. Acad. Sci. 2002, 99:14506-14511.
52. Tenenbaum J.B., De Silva V., Langford J.C. A global geometric framework for nonlinear dimensionality reduction. Science 2000, 290:2319-2323.
53. Verhaak R.G.W., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., Alexe G., Lawrence M., O'kelly M., Tamayo P., Weir B.A., Gabriel S., Winckler W., Gupta S., Jakkula L., Feiler H.S., Hodgson J.G., James C.D., Sarkaria J.N., Brennan C., Kahn A., Spellman P.T., Wilson R.K., Speed T.P., Gray J.W., Meyerson M., Getz G., Perou C.M., Hayes D.N. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
54. Wee S., Niklasson M., Marinescu V.D., Segerman A., Schmidt L., Hermansson A., Dirks P., Forsberg-Nilsson K., Westermark B., Uhrbom L., Linnarsson S., Nelander S., Andang M. Selective calcium sensitivity in immature glioma cancer stem cells. PLoS One 2014, 9:e115698.
55. Weller M., Wick W., Von Deimling A. Isocitrate dehydrogenase mutations: a challenge to traditional views on the genesis and malignant progression of gliomas. Glia 2011, 59:1200-1204.
56. Westermark B., Ponten J., Hugosson R. Determinants for the establishment of permanent tissue culture lines from human gliomas. Acta Pathol. Microbiol. Scand. A 1973, 81:791-805.
57. Yu D., Jin C., Ramachandran M., Xu J., Nilsson B., Korsgren O., Le Blanc K., Uhrbom L., Forsberg-Nilsson K., Westermark B., Adamson R., Maitland N., Fan X.L., Essand M. Adenovirus serotype 5 vectors with Tat-PTD modified hexon and serotype 35 fiber show greatly enhanced transduction capacity of primary cell cultures. PLoS One 2013, 8.