Neurosphere and adherent culture conditions are equivalent for malignant glioma stem cell lines

Anatomy and Cell Biology

Volumn 48, Issue 1, 2015, Pages 25-35

  Rahman, Maryam ^a   Reyner, Karina ^a   Deleyrolle, Loic ^a   Millette, Sebastien ^a   Azari, Hassan ^a,b   Day, Bryan W ^c   Stringer, Brett W ^c   Boyd, Andrew W ^c   Johns, Terrance G ^d   Blot, Vincent ^e   Duggal, Rohit ^f   Reynolds, Brent A ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e PFIZER INC   (United States)

^f GENELUX CORPORATION   (United States)

Author keywords

Adherent culture; Neoplastic stem cells; Neurosphere

Indexed keywords

EID: 84952309549     PISSN: 20933665     EISSN: 20933673     Source Type: Journal    
DOI: 10.5115/acb.2015.48.1.25     Document Type: Article

References (60)

1. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255:1707-10.
2. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron. 1994;13:1071-82.
3. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci. 1996;16:7599-609.
4. Hamilton A. The division of the differentiated cells in the central nervous system of the white rat. J Comp Neurol. 1901;11:297-320.
5. Kershman J. The medulloblast and the medulloblastoma: a study of human embryos. Arch Neurol Psychiatr. 1938;40:937-67.
6. Bryans WA. Mitotic activity in the brain of the adult rat. Anat Rec. 1959;133:65-73.
7. Altman J, Das GD. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol. 1966;126:337-89.
8. Dacey ML, Wallace RB. Postnatal neurogenesis in the feline cerebellum: a structural-functional investigation. Acta Neurobiol Exp (Wars). 1974;34:253-63.
9. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science. 1977;197: 1092-4.
10. Messier B, Leblond CP, Smart I Presence of DNA synthesis and mitosis in the brain of young adult mice. Exp Cell Res. 1958; 14:224-6.
11. Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science. 1984;225:1046-8.
12. Goldman SA, Nottebohm F. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci U S A. 1983;80:2390-4.
13. 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;64:7011-21.
14. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004;432:396-401.
15. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 2005;65:9328-37.
16. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111-5.
17. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504-14.
18. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-7.
19. Huntly BJ, Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer. 2005;5:311-21.
20. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer. 2006;6:425-36.
21. Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA. Human cortical glial tumors contain neural stemlike cells expressing astroglial and neuronal markers in vitro. Glia. 2002;39:193-206.
22. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-60.
23. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.
24. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G, Pilozzi E, Larocca LM, Peschle C, De Maria R. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 2006;13:1238-41.
25. Rich JN. Cancer stem cells in radiation resistance. Cancer Res. 2007;67:8980-4.
26. Chaichana K, Zamora-Berridi G, Camara-Quintana J, Quiñones-Hinojosa A. Neurosphere assays: growth factors and hormone differences in tumor and nontumor studies. Stem Cells. 2006;24:2851-7.
27. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. 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.
28. De Witt Hamer PC, Van Tilborg AA, Eijk PP, Sminia P, Troost D, Van Noorden CJ, Ylstra B, Leenstra S. The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene. 2008;27:2091-6.
29. Arsenijevic Y, Weiss S, Schneider B, Aebischer P. Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci. 2001;21:7194-202.
30. Caldwell MA, He X, Wilkie N, Pollack S, Marshall G, Wafford KA, Svendsen CN. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat Biotechnol. 2001;19:475-9.
31. Reynolds BA, Rietze RL. Neural stem cells and neurospheres: reevaluating the relationship. Nat Methods. 2005;2:333-6.
32. Singec I, Knoth R, Meyer RP, Maciaczyk J, Volk B, Nikkhah G, Frotscher M, Snyder EY. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods. 2006;3:801-6.
33. Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells. 2008; 26:988-96.
34. Hall PE, Lathia JD, Caldwell MA, Ffrench-Constant C. Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci. 2008;9:71.
35. Pollard SM, Conti L, Sun Y, Goffredo D, Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex. 2006;16 Suppl 1:i112-20.
36. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005;3:e283.
37. Sun Y, Pollard S, Conti L, Toselli M, Biella G, Parkin G, Willatt L, Falk A, Cattaneo E, Smith A. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci. 2008;38:245-58.
38. Fael Al-Mayhani TM, Ball SL, Zhao JW, Fawcett J, Ichimura K, Collins PV, 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;176:192-9.
39. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, Squire JA, 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;4:568-80.
40. Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347:70-8.
41. Smyth GK, Michaud J, Scott HS. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics. 2005;21:2067-75.
42. Deleyrolle LP, Ericksson G, Morrison BJ, Lopez JA, Burrage K, Burrage P, Vescovi A, Rietze RL, Reynolds BA. Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS One. 2011;6:e15844.
43. Laks DR, Masterman-Smith M, Visnyei K, Angenieux B, Orozco NM, Foran I, Yong WH, Vinters HV, Liau LM, Lazareff JA, Mischel PS, Cloughesy TF, Horvath S, Kornblum HI. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells. 2009;27:980-7.
44. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi AL. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444:761-5.
45. Inagaki A, Soeda A, Oka N, Kitajima H, Nakagawa J, Motohashi T, Kunisada T, Iwama T. Long-term maintenance of brain tumor stem cell properties under at non-adherent and adherent culture conditions. Biochem Biophys Res Commun. 2007;361:586-92.
46. Wei KC, Huang CY, Chen PY, Feng LY, Wu TW, Chen SM, Tsai HC, Lu YJ, Tsang NM, Tseng CK, Pai PC, Shin JW. Evaluation of the prognostic value of CD44 in glioblastoma multiforme. Anticancer Res. 2010;30:253-9.
47. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010;140:62-73.
48. Day BW, Stringer BW, Spanevello MD, Charmsaz S, Jamieson PR, Ensbey KS, Carter JC, Cox JM, Ellis VJ, Brown CL, Walker DG, Inglis PL, Allan S, Reynolds BA, Lickliter JD, Boyd AW. ELK4 neutralization sensitizes glioblastoma to apoptosis through downregulation of the anti-apoptotic protein Mcl-1. Neuro Oncol. 2011;13:1202-12.
49. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ. Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene. 2002;21:8404-13.
50. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, Bredesen DE, Brenner C, Castedo M, Cidlowski JA, Ciechanover A, Cohen GM, De Laurenzi V, De Maria R, Deshmukh M, Dynlacht BD, El-Deiry WS, Flavell RA, Fulda S, Garrido C, Golstein P, Gougeon ML, Green DR, Gronemeyer H, Hajnoczky G, Hardwick JM, Hengartner MO, Ichijo H, Jaattela M, Kepp O, Kimchi A, Klionsky DJ, Knight RA, Kornbluth S, Kumar S, Levine B, Lipton SA, Lugli E, Madeo F, Malomi W, Marine JC, Martin SJ, Medema JP, Mehlen P, Melino G, Moll UM, Morselli E, Nagata S, Nicholson DW, Nicotera P, Nunez G, Oren M, Penninger J, Pervaiz S, Peter ME, Piacentini M, Prehn JH, Puthalakath H, Rabinovich GA, Rizzuto R, Rodrigues CM, Rubinsztein DC, Rudel T, Scorrano L, Simon HU, Steller H, Tschopp J, Tsujimoto Y, Vandenabeele P, Vitale I, Vousden KH, Youle RJ, Yuan J, Zhivotovsky B, Kroemer G. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ. 2009;16:1093-107.
51. Troiano L, Ferraresi R, Lugli E, Nemes E, Roat E, Nasi M, Pinti M, Cossarizza A. Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry. Nat Protoc. 2007;2:2719-27.
52. Mazzini G, Ferrari C, Erba E. Dual excitation multi- fluorescence flow cytometry for detailed analyses of viability and apoptotic cell transition. Eur J Histochem. 2003;47:289-98.
53. Martin K, Akinwunmi J, Rooprai HK, Kennedy AJ, Linke A, Ognjenovic N, Pilkington GJ. Nonexpression of CD15 by neoplastic glia: a barrier to metastasis. Anticancer Res. 1995;15: 1159-66.
54. Porter AG, Jänicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999;6:99-104.
55. Jänicke RU, Ng P, Sprengart ML, Porter AG. Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem. 1998;273:15540-5.
56. Jänicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem. 1998;273:9357-60.
57. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development. 1990;110:1001-20.
58. Gritti A, Galli R, Vescovi AL. Cultures of stem cells of the central nervous system. In: Fedoroff S, Richardson A, editors. Protocols for Neural Cell Culture. 3rd ed. Totowa: Humana Press; 2001. p.173-98.
59. Mahesparan R, Tysnes BB, Read TA, Enger PO, Bjerkvig R, Lund-Johansen M. Extracellular matrix-induced cell migration from glioblastoma biopsy specimens in vitro. Acta Neuropathol. 1999; 97:231-9.
60. Ziu M, Schmidt NO, Cargioli TG, Aboody KS, Black PM, Carroll RS. Glioma-produced extracellular matrix influences brain tumor tropism of human neural stem cells. J Neurooncol. 2006; 79:125-33.