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

Certain limitations of the neurosphere assay (NSA) have resulted in a search for alternative culture techniques for brain tumor-initiating cells (TICs). Recently, reports have described growing glioblastoma (GBM) TICs as a monolayer using laminin. We performed a side-by-side analysis of the NSA and laminin (adherent) culture conditions to compare the growth and expansion of GBM TICs. GBM cells were grown using the NSA and adherent culture conditions. Comparisons were made using growth in culture, apoptosis assays, protein expression, limiting dilution clonal frequency assay, genetic affymetrix analysis, and tumorigenicity in vivo. In vitro expansion curves for the NSA and adherent culture conditions were virtually identical (P=0.24) and the clonogenic frequencies (5.2% for NSA vs. 5.0% for laminin, P=0.9) were similar as well. Likewise, markers of differentiation (glial fibrillary acidic protein and beta tubulin III) and proliferation (Ki67 and MCM2) revealed no statistical difference between the sphere and attachment methods. Several different methods were used to determine the numbers of dead or dying cells (trypan blue, DiIC, caspase-3, and annexin V) with none of the assays noting a meaningful variance between the two methods. In addition, genetic expression analysis with microarrays revealed no significant differences between the two groups. Finally, glioma cells derived from both methods of expansion formed large invasive tumors exhibiting GBM features when implanted in immune-compromised animals. A detailed functional, protein and genetic characterization of human GBM cells cultured in serum-free defined conditions demonstrated no statistically meaningful differences when grown using sphere (NSA) or adherent conditions. Hence, both methods are functionally equivalent and remain suitable options for expanding primary high-grade gliomas in tissue culture.

[1]  A. Boyd,et al.  ELK4 neutralization sensitizes glioblastoma to apoptosis through downregulation of the anti-apoptotic protein Mcl-1. , 2011, Neuro-oncology.

[2]  Kevin Burrage,et al.  Determination of Somatic and Cancer Stem Cell Self-Renewing Symmetric Division Rate Using Sphere Assays , 2011, PloS one.

[3]  P. Pelicci,et al.  Biological and Molecular Heterogeneity of Breast Cancers Correlates with Their Cancer Stem Cell Content , 2010, Cell.

[4]  G. Smyth,et al.  ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. , 2009, Journal of immunological methods.

[5]  G. Mazzini,et al.  Dual excitation multi- fluorescence flow cytometry for detailed analyses of viability and apoptotic cell transition. , 2009, European journal of histochemistry : EJH.

[6]  Mark Bernstein,et al.  Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. , 2009, Cell stem cell.

[7]  R A Knight,et al.  Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes , 2009, Cell Death and Differentiation.

[8]  S. Horvath,et al.  Neurosphere Formation Is an Independent Predictor of Clinical Outcome in Malignant Glioma , 2009, Stem cells.

[9]  J. Fawcett,et al.  An efficient method for derivation and propagation of glioblastoma cell lines that conserves the molecular profile of their original tumours , 2009, Journal of Neuroscience Methods.

[10]  C. ffrench-Constant,et al.  Laminin enhances the growth of human neural stem cells in defined culture media , 2008, BMC Neuroscience.

[11]  G. Parkin,et al.  Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture , 2008, Molecular and Cellular Neuroscience.

[12]  Loic Deleyrolle,et al.  Enumeration of Neural Stem and Progenitor Cells in the Neural Colony‐Forming Cell Assay , 2008, Stem cells.

[13]  S. Leenstra,et al.  The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids , 2008, Oncogene.

[14]  M. Biffoni,et al.  Identification and expansion of the tumorigenic lung cancer stem cell population , 2008, Cell Death and Differentiation.

[15]  Elisa Nemes,et al.  Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry , 2007, Nature Protocols.

[16]  J. Rich,et al.  Cancer stem cells in radiation resistance. , 2007, Cancer research.

[17]  T. Iwama,et al.  Long-term maintenance of brain tumor stem cell properties under at non-adherent and adherent culture conditions. , 2007, Biochemical and biophysical research communications.

[18]  L. Ricci-Vitiani,et al.  Identification and expansion of human colon-cancer-initiating cells , 2007, Nature.

[19]  G. Broggi,et al.  Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells , 2006, Nature.

[20]  Mark W. Dewhirst,et al.  Glioma stem cells promote radioresistance by preferential activation of the DNA damage response , 2006, Nature.

[21]  K. Black,et al.  Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma , 2006, Molecular Cancer.

[22]  A. Quiñones‐Hinojosa,et al.  Neurosphere Assays: Growth Factors and Hormone Differences in Tumor and Nontumor Studies , 2006, Stem cells.

[23]  M. Frotscher,et al.  Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology , 2006, Nature Methods.

[24]  L. Ricci-Vitiani,et al.  Chemotherapy resistance of glioblastoma stem cells , 2006, Cell Death and Differentiation.

[25]  Austin G Smith,et al.  Adherent neural stem (NS) cells from fetal and adult forebrain. , 2006, Cerebral cortex.

[26]  Angelo L. Vescovi,et al.  Brain tumour stem cells , 2006, Nature Reviews Cancer.

[27]  Yuri Kotliarov,et al.  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. , 2006, Cancer cell.

[28]  P. Black,et al.  Glioma-produced extracellular matrix influences brain tumor tropism of human neural stem cells , 2006, Journal of Neuro-Oncology.

[29]  D. Elder,et al.  A tumorigenic subpopulation with stem cell properties in melanomas. , 2005, Cancer research.

[30]  Austin G Smith,et al.  Niche-Independent Symmetrical Self-Renewal of a Mammalian Tissue Stem Cell , 2005, PLoS biology.

[31]  Brent A Reynolds,et al.  Neural stem cells and neurospheres—re-evaluating the relationship , 2005, Nature Methods.

[32]  Gordon K. Smyth,et al.  Use of within-array replicate spots for assessing differential expression in microarray experiments , 2005, Bioinform..

[33]  D. Gilliland,et al.  Leukaemia stem cells and the evolution of cancer-stem-cell research , 2005, Nature Reviews Cancer.

[34]  R. Henkelman,et al.  Identification of human brain tumour initiating cells , 2004, Nature.

[35]  Ugo Orfanelli,et al.  Isolation and Characterization of Tumorigenic, Stem-like Neural Precursors from Human Glioblastoma , 2004, Cancer Research.

[36]  G. Barnett,et al.  Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells , 2002, Oncogene.

[37]  D. Steindler,et al.  Human cortical glial tumors contain neural stem‐like cells expressing astroglial and neuronal markers in vitro , 2002, Glia.

[38]  S. Weiss,et al.  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 , 2001, Journal of Neuroscience.

[39]  Scott Pollack,et al.  Growth factors regulate the survival and fate of cells derived from human neurospheres , 2001, Nature Biotechnology.

[40]  R. Bjerkvig,et al.  Extracellular matrix-induced cell migration from glioblastoma biopsy specimens in vitro , 1999, Acta Neuropathologica.

[41]  A. Porter,et al.  Emerging roles of caspase-3 in apoptosis , 1999, Cell Death and Differentiation.

[42]  Patrick Ng,et al.  Caspase-3 Is Required for α-Fodrin Cleavage but Dispensable for Cleavage of Other Death Substrates in Apoptosis* , 1998, The Journal of Biological Chemistry.

[43]  Alan G. Porter,et al.  Caspase-3 Is Required for DNA Fragmentation and Morphological Changes Associated with Apoptosis* , 1998, The Journal of Biological Chemistry.

[44]  J. Dick,et al.  Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell , 1997, Nature Medicine.

[45]  Brent A. Reynolds,et al.  Multipotent CNS Stem Cells Are Present in the Adult Mammalian Spinal Cord and Ventricular Neuroaxis , 1996, The Journal of Neuroscience.

[46]  G. Pilkington,et al.  Nonexpression of CD15 by neoplastic glia: a barrier to metastasis? , 1995, Anticancer research.

[47]  Brent A. Reynolds,et al.  Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells , 1994, Neuron.

[48]  S. Weiss,et al.  Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. , 1992, Science.

[49]  M. Loeffler,et al.  Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. , 1990, Development.

[50]  F. Nottebohm,et al.  Neurons generated in the adult brain are recruited into functional circuits. , 1984, Science.

[51]  F. Nottebohm,et al.  Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. Hinds,et al.  Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. , 1977, Science.

[53]  J. Altman,et al.  Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incoorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions , 1966, The Journal of comparative neurology.

[54]  W. A. Bryans Mitotic activity in the brain of the adult rat , 1959 .

[55]  C. P. Leblond,et al.  Presence of DNA synthesis and mitosis in the brain of young adult mice. , 1958, Experimental cell research.

[56]  J. Kershman THE MEDULLOBLAST AND THE MEDULLOBLASTOMA: A STUDY OF HUMAN EMBRYOS , 1938 .

[57]  A. Hamilton The division of differentiated cells in the central nervous system of the white rat , 1901 .

[58]  C. Tseng,et al.  Evaluation of the prognostic value of CD44 in glioblastoma multiforme. , 2010, Anticancer research.

[59]  R. Galli,et al.  Cultures of Stem Cells of the Central Nervous System , 2001 .

[60]  S. Fedoroff,et al.  Protocols for Neural Cell Culture , 1997, Humana Press.

[61]  R. Wallace,et al.  Postnatal neurogenesis in the feline cerebellum: a structural-functional investigation. , 1974, Acta neurobiologiae experimentalis.

[62]  Wallace Rb,et al.  Postnatal neurogenesis in the feline cerebellum: a structural-functional investigation. , 1974 .