Review Special Issues

Towards an advanced cell-based in vitro glioma model system

  • Received: 09 December 2017 Accepted: 14 March 2018 Published: 19 March 2018
  • The modulation of tumor growth and development in vitro has always been one of the key factors in the research of the malignant transformation, including gliomas, prevalent and most deadly cancers of the brain. Indeed, cellular and molecular biology research employing in vitro model cell-based systems have great potential to advance both the mechanistic understanding and the treatment of human glial tumors, as it facilitates not only the understanding of glioma biology and its regulatory mechanisms Additionally they promise to afford the screening of the putative anti-tumor agents and alternative treatment approaches in a personalized manner, i.e. by virtue of using the patient-derived tumor material for such tests. However, in order to become reliable and representative, glioma model systems need to move towards including most inherent cancer features such as local hypoxia, specific genetic aberrations, native tumor microenvironment, and the three-dimensional extracellular matrix.
    This review starts with a brief introduction on the general epidemiological and molecular characteristics of gliomas followed by an overview of the cell-based in vitro models currently used in glioma research. As a conclusion, we suggest approaches to move to innovative cell-based in vitro glioma models. We consider that main criteria for selecting these approaches should include the adequate resemblance to the key in vivo characteristics, robustness, cost-effectiveness and ease to use, as well as the amenability to high throughput handling to allow the standardized drug screening.

    Citation: Valeriia Mikhailova, Valeriia Gulaia, Vladlena Tiasto, Stanislav Rybtsov, Margarita Yatsunskaya, Alexander Kagansky. Towards an advanced cell-based in vitro glioma model system[J]. AIMS Genetics, 2018, 5(2): 91-112. doi: 10.3934/genet.2018.2.91

    Related Papers:

  • The modulation of tumor growth and development in vitro has always been one of the key factors in the research of the malignant transformation, including gliomas, prevalent and most deadly cancers of the brain. Indeed, cellular and molecular biology research employing in vitro model cell-based systems have great potential to advance both the mechanistic understanding and the treatment of human glial tumors, as it facilitates not only the understanding of glioma biology and its regulatory mechanisms Additionally they promise to afford the screening of the putative anti-tumor agents and alternative treatment approaches in a personalized manner, i.e. by virtue of using the patient-derived tumor material for such tests. However, in order to become reliable and representative, glioma model systems need to move towards including most inherent cancer features such as local hypoxia, specific genetic aberrations, native tumor microenvironment, and the three-dimensional extracellular matrix.
    This review starts with a brief introduction on the general epidemiological and molecular characteristics of gliomas followed by an overview of the cell-based in vitro models currently used in glioma research. As a conclusion, we suggest approaches to move to innovative cell-based in vitro glioma models. We consider that main criteria for selecting these approaches should include the adequate resemblance to the key in vivo characteristics, robustness, cost-effectiveness and ease to use, as well as the amenability to high throughput handling to allow the standardized drug screening.


    加载中
    [1] Lindsey AT, Freddie B, Rebecca LS, et al. (2015) Global cancer statistics, 2012. CA Cancer J Clin 65: 87–108. doi: 10.3322/caac.21262
    [2] Kaprina AD, Starinskiy VV, Petrova GB. (2018) Malignant neoplasms in Russia in 2016, Moscow : P.Herzen Moscow Oncology Research Institute publishing house.
    [3] Ostrom QT, Gittleman H, Xu J, et al. (2017) CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2010–2014. Neuro Onco 18:iv1–iv89.
    [4] Ferlay J, Soerjomataram I, Ervik M, et al. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136: E359–E386. doi: 10.1002/ijc.29210
    [5] Ostrom QT, Gittleman H, Xu J, et al. (2016) CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2009–2013. Neuro Oncol 18: v1–v75. doi: 10.1093/neuonc/now207
    [6] Claes A, Idema AJ, Wesseling P. (2007) Diffuse glioma growth: a guerilla war. Acta Neuropathol 114: 443–458. doi: 10.1007/s00401-007-0293-7
    [7] Louis DN, Ohgaki H, Wiestler OD, et al. (2007) The 2007 WHO Classification of Tumours of the Central Nervous System. Acta Neuropathol 114: 97–109. doi: 10.1007/s00401-007-0243-4
    [8] Ostrom QT, Gittleman H, Fulop J, et al. (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro- Oncology 17: iv1–iv62. doi: 10.1093/neuonc/nov189
    [9] Stupp R, Mason WP, van den Bent MJ, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987–996. doi: 10.1056/NEJMoa043330
    [10] Roy S, Lahiri D, Maji T, et al. (2015) Recurrent Glioblastoma: Where we stand. South Asian J Cancer 4: 163–173. doi: 10.4103/2278-330X.175953
    [11] Suzuki H, Aoki K, Chiba K, et al. (2015) Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet. 47: 458–468. doi: 10.1038/ng.3273
    [12] Schomas DA, Laack NN, Rao RD, et al. (2009) Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro-Oncology 11: 437–445. doi: 10.1215/15228517-2008-102
    [13] Darlix A, Zouaoui S, Virion JM, et al. (2014) Significant heterogeneity in the geographical distribution of diffuse grade II/III gliomas in France. J Neuro-Oncology 120: 547–555. doi: 10.1007/s11060-014-1585-0
    [14] Tseng MY, Tseng JH, Merchant E. (2006) Comparison of effects of socioeconomic and geographic variations on survival for adults and children with glioma. J Neurosurg 105: 297–305.
    [15] Frosina G. (2011) Frontiers in targeting glioma stem cells. Eur J Cancer 47: 496–507. doi: 10.1016/j.ejca.2010.11.017
    [16] Gasch С, Ffrench B, O'Leary JJ, et al. Catching moving targets: cancer stem cell hierarchies, therapy-resistance & considerations for clinical intervention. Mol Cancer 16: 1–15.
    [17] Clarke J, Butowski N, Chang S. (2010) Recent advances in therapy for glioblastoma. Arch Neurol 67: 279–283.
    [18] Lenting K, Verhaak R, Ter Laan M, et al. (2017) Glioma: experimental models and reality. Acta Neuropathol 133: 263–282. doi: 10.1007/s00401-017-1671-4
    [19] Meric-Bernstam F, Mills GB. (2012) Overcoming implementation challenges of personalized cancer therapy. Nat Rev Clin Oncol 9: 542–548. doi: 10.1038/nrclinonc.2012.127
    [20] Fialkow PJ. (1979) Clonal origin of human tumors. Annu Rev Med 30: 135–143. doi: 10.1146/annurev.me.30.020179.001031
    [21] Rabkin CS, Janz S, Lash A, et al. (1997) Monoclonal origin of multicentric Kaposi's sarcoma lesions. N Engl J Med 336: 988–993. doi: 10.1056/NEJM199704033361403
    [22] Yachida S, Jones S, Bozic I, et al. (2010) Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467: 1114–1117. doi: 10.1038/nature09515
    [23] Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U.S.A 100: 3983–3988. doi: 10.1073/pnas.0530291100
    [24] Wicha MS, Liu S, Dontu G. (2006) Cancer stem cells: an old idea--a paradigm shift. Cancer Res 66: 1883–1890. doi: 10.1158/0008-5472.CAN-05-3153
    [25] Chen W, Dong J, Haiech J, et al. (2016) Cancer Stem Cell Quiescence and Plasticity as Major Challenges in Cancer Therapy. Stem Cells Int 2016:1740936.
    [26] Valent P, Bonnet D, De Maria R, et al. (2012) Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer. 12: 767–775. doi: 10.1038/nrc3368
    [27] Chen J, Li Y, Yu TS, et al. (2012) A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488: 522–526. doi: 10.1038/nature11287
    [28] Liebelt BD, Shingu T, Zhou X, et al.(2016) Glioma Stem Cells: Signaling, Microenvironment, and Therapy. Stem Cells Int 2016: 7849890.
    [29] Fidoamore A, Cristiano L, Antonosante A, et al. (2016) Glioblastoma Stem Cells Microenvironment: The Paracrine Roles of the Niche in Drug and Radioresistance. Stem Cells Int 2016: 6809105.
    [30] Michor F, Polyak K. (2010) The origins and implications of intratumor heterogeneity. Cancer Prev Res (Phila) 3: 1361–1364. doi: 10.1158/1940-6207.CAPR-10-0234
    [31] Gerdes MJ, Sood A, Sevinsky C, et al. (2014) Emerging understanding of multiscale tumor heterogeneity. Front Oncol 4: 366.
    [32] Lathia JD, Mack SC, Mulkearns-Hubert EE. (2015) Cancer stem cells in glioblastoma. Genes Dev 29: 1203–1217. doi: 10.1101/gad.261982.115
    [33] Anido J, Saez-Borderıas A, Gonzalez-Junca A, et al. (2010) TGF-β receptor inhibitors target theCD44high/Id1 high glioma-initiating cell population in human glioblastoma. Cancer Cell 18: 655–668. doi: 10.1016/j.ccr.2010.10.023
    [34] Lathia JD, Gallagher J, Heddleston JM, et al. (2010) Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 6: 421–432. doi: 10.1016/j.stem.2010.02.018
    [35] Thon N, Damianoff K, Hegermann J, et al. (2010) Presence of pluripotent CD133+ cells correlates with malignancy of gliomas. Mol Cell Neurosci 43: 51–59. doi: 10.1016/j.mcn.2008.07.022
    [36] Bexell D, Gunnarsson S, Siesjo P, et al. (2009) CD133+ and nestin+ tumor-initiating cells dominate in N29 andN32 experimental gliomas. Int J Cancer 125: 15–22. doi: 10.1002/ijc.24306
    [37] Mathieu J, Zhang Z, Zhou W, et al. (2011) HIF induces human embryonic stem cell markers in cancer cells. Cancer Res 71: 4640–4652. doi: 10.1158/0008-5472.CAN-10-3320
    [38] Ikushima H, Todo T, Ino Y, et al. (2011) Glioma-initiating cells retain their tumorigenicity through integration of the Sox axis and Oct4 protein. J Biol Chem 286: 41434–41441. doi: 10.1074/jbc.M111.300863
    [39] Hagerstrand D, He X, Bradic Lindh M, et al. (2011) Identification of a SOX2-dependent subset of tumor- and sphere-forming glioblastoma cells with a distinct tyrosine kinase inhibitor sensitivity profile. Neuro-Oncology 13: 1178–1191. doi: 10.1093/neuonc/nor113
    [40] Ahlenius H, Kokaia Z. (2010) Isolation and generation of neurosphere cultures from embryonic and adult mouse brain. Methods Mol Biol 633: 241–252. doi: 10.1007/978-1-59745-019-5_18
    [41] Galli R. (2013) The neurosphere assay applied to neural stem cells and cancer stem cells. Methods Mol Biol. 986: 267–277. doi: 10.1007/978-1-62703-311-4_17
    [42] Rahman M, Reyner K, Deleyrolle L, et al. (2015) Neurosphere and adherent culture conditions are equivalent for malignant glioma stem cell lines. Anatomy Cell Biol 48: 25–35. doi: 10.5115/acb.2015.48.1.25
    [43] Pastrana E, Silva-Vargas V, Doetsch F. (2011) Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8: 486–498. doi: 10.1016/j.stem.2011.04.007
    [44] Patel AP, Tirosh I, Trombetta JJ, et al. (2014) Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344: 1396–1401. doi: 10.1126/science.1254257
    [45] Venteicher AS, Tirosh I, Hebert C, et al. (2017) Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq. Science 355: 1391–1403.
    [46] Barker N, Bartfeld S, Clevers H. (2010) Tissue-resident adult stem cell populations of rapidly self-renewing organs. Cell Stem Cell 7: 656–670. doi: 10.1016/j.stem.2010.11.016
    [47] Bao S, Wu Q, McLendon RE, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756–760. doi: 10.1038/nature05236
    [48] Perazzoli G, Prados J, Ortiz R, et al. (2015) Temozolomide Resistance in Glioblastoma Cell Lines: Implication of MGMT, MMR, P-Glycoprotein and CD133 Expression. PLoS One. 10: e0140131. doi: 10.1371/journal.pone.0140131
    [49] Paik JH, Ding Z, Narurkar R, et al. (2009) FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5: 540–553. doi: 10.1016/j.stem.2009.09.013
    [50] Martynoga B, Mateo JL, Zhou B, et al. (2013) Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 27: 1769–1786. doi: 10.1101/gad.216804.113
    [51] Louis DN, Perry A, Reifenberger G, et al. (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131: 803–820. doi: 10.1007/s00401-016-1545-1
    [52] Brat DJ, Verhaak RG, Aldape KD, et al. (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372: 2481–2498. doi: 10.1056/NEJMoa1402121
    [53] Chi AS, Batchelor TT, Yang D, et al. (2013) BRAF V600E mutation identifies a subset of low-grade diffusely infiltrating gliomas in adults. J Clin Oncol 31: e233–236. doi: 10.1200/JCO.2012.46.0220
    [54] Suzuki Y, Takahashi-Fujigasaki J, Akasaki Y, et al. (2016) BRAF V600E-mutated diffuse glioma in an adult patient: a case report and review. Brain Tumor Pathol 33: 40–49. doi: 10.1007/s10014-015-0234-4
    [55] Leeper HE, Caron AA, Decker PA, et al. (2015) IDH mutation, 1p19q codeletion and ATRX loss in WHO grade II gliomas. Oncotarget 6: 30295–30305.
    [56] Weller M, Weber RG, Willscher E, et al. (2015) Molecular classification of diffuse cerebral WHO grade II/III gliomas using genome- and transcriptome-wide profiling improves stratification of prognostically distinct patient groups. Acta Neuropathol 129: 679–693. doi: 10.1007/s00401-015-1409-0
    [57] Eckel-Passow JE, Lachance DH, Molinaro AM, et al. (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372: 2499–2508. doi: 10.1056/NEJMoa1407279
    [58] Cloughesy TF, Cavenee WK, Mischel PS. (2014) Glioblastoma: from molecular pathology to targeted treatment. Annu Rev Pathol 9: 1–25. doi: 10.1146/annurev-pathol-011110-130324
    [59] Liu XY, Gerges N, Korshunov A, et al. (2012) Frequent ATRX mutations and loss of expression in adult diffuse astrocytic tumors carrying IDH1/IDH2 and TP53 mutations. Acta Neuropathol 124: 615–625. doi: 10.1007/s00401-012-1031-3
    [60] Ohgaki H, Kleihues P. (2013) The definition of primary and secondary glioblastoma. Clin Cancer Res 19: 764–772. doi: 10.1158/1078-0432.CCR-12-3002
    [61] Egan KM, Thompson RC, Nabors L, et al. (2011) Cancer susceptibility variants and the risk of adult glioma in a US case–control study. J Neuro-Oncol 104: 535–542. doi: 10.1007/s11060-010-0506-0
    [62] Jenkins RB, Xiao Y, Sicotte H, et al. (2012) A low-frequency variant at 8q24. 21 is strongly associated with risk of oligodendroglial tumors and astrocytomas with IDH1 or IDH2 mutation. Nat Genet 44: 1122–1125.
    [63] Kinnersley B, Labussiere M, Holroyd A, et al. (2015) Genome-wide association study identifies multiple susceptibility loci for glioma. Nat Commun 6:8559. doi: 10.1038/ncomms9559
    [64] Rice T, Zheng S, Decker PA, et al. (2013) Inherited variant on chromosome 11q23 increases susceptibility to IDH-mutated but not IDH-normal gliomas regardless of grade or histology. Neuro-Oncology 15: 535–541. doi: 10.1093/neuonc/nos324
    [65] Wrensch M, Jenkins RB, Chang JS, et al. (2009) Variants in the CDKN2B and RTEL1 regions are associated with high-grade glioma susceptibility. Nat Genet 41: 905–908. doi: 10.1038/ng.408
    [66] Shete S, Hosking FJ, Robertson LB, et al. (2009) Genome-wide association study identifies five susceptibility loci for glioma. Nat Genet 41: 899–904. doi: 10.1038/ng.407
    [67] Walsh KM, Codd V, Smirnov IV, et al. (2014) Variants near TERT and TERC influencing telomere length are associated with high-grade glioma risk. Nat Genet 46: 731–735. doi: 10.1038/ng.3004
    [68] Lu C, Ward PS, Kapoor GS, et al. (2012) IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483: 474–478. doi: 10.1038/nature10860
    [69] Sundarraj N, Schachner M, Pfeiffer SE. (1975) Biochemically differentiated mouse glial lines carrying a nervous system specific cell surface antigen (NS-1). Proc Natl Acad Sci U.S.A 72: 1927–1931. doi: 10.1073/pnas.72.5.1927
    [70] Dawson G, Sundarraj N, Pfeiffer SE. (1977) Synthesis of myelin glycosphingolipids (galactosylceramide and galactosyl (3-O-sulfate) ceramide (sulfatide) by cloned cell lines derived from mouse neurotumors. J Biol Chem 252: 2777–2779.
    [71] Fields KL, Gosling C, Megson M, et al. (1975) New cell surface antigens in rat defined by tumors of the nervous system. Proc Natl Acad Sci U.S.A 72: 1296–1300. doi: 10.1073/pnas.72.4.1296
    [72] Allen M, Bjerke M, Edlund H, et al. (2016) Origin of the U87MG glioma cell line: Good news and bad news. Sci Transl Med 8: 354–353.
    [73] Torsvik A, Stieber D, Enger PO, et al. (2014) U-251 revisited: genetic drift and phenotypic consequences of long-term cultures of glioblastoma cells. Cancer Med 3: 812–824. doi: 10.1002/cam4.219
    [74] De Vries GH, Boullerne AI. (2010) Glial cell lines: an overview. Neurochem Res 35: 1978–2000. doi: 10.1007/s11064-010-0318-9
    [75] Louis JC, Magal E, Muir D, et al. (1992) CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J Neurosci Res 31: 193–204. doi: 10.1002/jnr.490310125
    [76] Richter-Landsberg C, Heinrich M. (1996) OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J Neurosci Res 45: 161–173. doi: 10.1002/(SICI)1097-4547(19960715)45:2<161::AID-JNR8>3.0.CO;2-8
    [77] Jung M, Kramer E, Grzenkowski M, et al. (1995) Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur J Neurosci 7: 1245–1265. doi: 10.1111/j.1460-9568.1995.tb01115.x
    [78] Foster LM, Phan T, Verity AN, et al. (1992) Generation and analysis of normal and shiverer temperature-sensitive immortalized cell lines exhibiting phenotypic characteristics of oligodendrocytes at several stages of differentiation. J Neurosci Res 31: 193–204. doi: 10.1002/jnr.490310125
    [79] Post GR, Dawson G. (1992) Characterization of a cell line derived from a human oligodendroglioma. Mol Chem Neuropathol 16: 303–317. doi: 10.1007/BF03159976
    [80] McLaurin J, Trudel GC, Shaw IT, et al. (1995) A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J Neurobiol 26: 283–293. doi: 10.1002/neu.480260212
    [81] Benda P, Lightbody J, Sato G, et al. (1968) Differentiated rat glial cell strain in tissue culture. Science 161: 370–371. doi: 10.1126/science.161.3839.370
    [82] Radany EH, Brenner M, Besnard F, et al. (1992) Directed establishment of rat brain cell lines with the phenotypic characteristics of type 1 astrocytes. Proc Natl Acad Sci U.S.A. 89: 6467–6471. doi: 10.1073/pnas.89.14.6467
    [83] Loo DT, Fuquay JI, Rawson CL, et al. (1987) Extended culture of mouse embryo cells without senescence: inhibition by serum. Science 236: 200–202. doi: 10.1126/science.3494308
    [84] Giard DJ, Aaronson SA, Todaro GJ, et al. (1973) In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 51: 1417–1423. doi: 10.1093/jnci/51.5.1417
    [85] Pontén J, Macintyre EH. (1968) Long term culture of normal and neoplastic human glia. Acta Pathol Microbiol Scand 74: 465–486.
    [86] Westermark B, Ponten J, Hugosson R. (1973) Determinants for the establishment of permanent tissue culture lines from human gliomas. Acta Pathol Microbiol Scand A 81: 791–805.
    [87] Lee J, Kotliarova S, Kotliarov Y, et al. (2006) 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 9: 391–403. doi: 10.1016/j.ccr.2006.03.030
    [88] Luca AC, Mersch S, Deenen R, et al. (2013) Impact of the 3D Microenvironment on Phenotype, Gene Expression, and EGFR Inhibition of Colorectal Cancer Cell Lines. PloS One 8: e59689. doi: 10.1371/journal.pone.0059689
    [89] Storch K, Eke I, Borgmann K, et al. (2010) Three-dimensional cell growth confers radioresistance by chromatin density modification. Cancer Res 70: 3925–3934. doi: 10.1158/0008-5472.CAN-09-3848
    [90] Hehlgans S, Lange I, Eke I, et al. (2009) 3D cell cultures of human head and neck squamous cell carcinoma cells are radiosensitized by the focal adhesion kinase inhibitor TAE226. Radiotherapy oncology: j Eu Soc Therapeutic Radiology Oncology 92:371–378. doi: 10.1016/j.radonc.2009.08.001
    [91] Bristow RG, Hill RP. (2008) Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev. Cancer 8: 180–192.
    [92] Gomez-Roman N, Stevenson K, Gilmour L, et al. (2017) A novel 3D human glioblastoma cell culture system for modeling drug and radiation responses. Neuro Oncol 19:229–241.
    [93] Mullins CS, Schneider B, Stockhammer F, et al. (2013) Establishment and characterization of primary glioblastoma cell lines from fresh and frozen material: a detailed comparison. PLoS One 8: e71070. doi: 10.1371/journal.pone.0071070
    [94] Cheng L, Huang Z, Zhou W, et al. (2013) Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153: 139–152. doi: 10.1016/j.cell.2013.02.021
    [95] Soda Y, Marumoto T, Friedmann-Morvinski D, et al. (2011) Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U.S.A 108: 4274–4280. doi: 10.1073/pnas.1016030108
    [96] Wang R, Chadalavada K, Wilshire J, et al. (2010) Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468: 829–833. doi: 10.1038/nature09624
    [97] Singec I, Knoth R, Meyer RP, et al. (2006) Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods 3: 801–806. doi: 10.1038/nmeth926
    [98] Gritti A, Galli R, Vescovi AL. (2008) Clonal analyses and cryopreservation of neural stem cell cultures. Methods Mol Biol 438: 173–184. doi: 10.1007/978-1-59745-133-8_14
    [99] Brewer GJ, Torricelli JR, Evege EK, et al. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567–576. doi: 10.1002/jnr.490350513
    [100] Luchman HA, Stechishin OD, Dang NH, et al. (2012) An in vivo patient-derived model of endogenous IDH1-mutant glioma. Neuro Oncol 14: 184–191. doi: 10.1093/neuonc/nor207
    [101] Rohle D, Popovici-Muller J, Palaskas N, et al. (2013) An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 340: 626–630. doi: 10.1126/science.1236062
    [102] Alcantara LSR, Wang Z, Sun D, et al. (2015) Adult Lineage-Restricted CNS Progenitors Specify Distinct Glioblastoma Subtypes. Cancer Cell 28: 429–440. doi: 10.1016/j.ccell.2015.09.007
    [103] Lindberg N, Jiang Y, Xie Y, et al. (2014) Oncogenic signaling is dominant to cell of origin and dictates astrocytic or oligodendroglial tumor development from oligodendrocyte precursor cells. J Neuro Sci 34: 14644–14651.
    [104] Wang J, Wakeman TP, Lathia JD, et al. (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28: 17–28.
    [105] Adorno-Cruz V, Kibria G, Liu X, et al. (2015) Cancer stem cells: targeting the roots of cancer, seeds of metastasis, and sources of therapy resistance. Cancer Res 75: 924–929. doi: 10.1158/0008-5472.CAN-14-3225
    [106] Shlush LI, Mitchell A, Heisler L, et al. (2017) Tracing the origins of relapse in acute myeloid leukaemia to stem cells. Nature 547: 104–108. doi: 10.1038/nature22993
    [107] Stopschinski BE, Beier CP, Beier D. (2013) Glioblastoma cancer stem cells--from concept to clinical application. Cancer Lett 338: 32–40. doi: 10.1016/j.canlet.2012.05.033
    [108] Holmberg Olausson K, Maire CL, Haidar S, et al. (2014) Prominin-1 (CD133) defines both stem and non-stem cell populations in CNS development and gliomas. PLoS One 9: e106694. doi: 10.1371/journal.pone.0106694
    [109] Wee B, Charles N, Holland EC. (2011) Animal models to study cancer-initiating cells from glioblastoma. Front Bio Sci (Landmark Ed) 16: 2243–2258. doi: 10.2741/3851
    [110] Mack SC, Hubert CG, Miller TE, et al. (2016) An epigenetic gateway to brain tumor cell identity. Nat Neuro Sci 19: 10–19. doi: 10.1038/nn.4190
    [111] Irvin DM, McNeill RS, Bash RE, et al. (2017) Intrinsic Astrocyte Heterogeneity Influences Tumor Growth in Glioma Mouse Models. Brain Pathol 27: 36–50. doi: 10.1111/bpa.12348
    [112] Chen W, Wang D, Du X, et al. (2015) Glioma cells escaped from cytotoxicity of temozolomide and vincristine by communicating with human astrocytes. Med Oncol 32:43 . doi: 10.1007/s12032-015-0487-0
    [113] Chen W, Xia T, Wang D, et al. (2016) Human astrocytes secrete IL-6 to promote glioma migration and invasion through upregulation of cytomembrane MMP14. Oncotarget 7: 62425–62438.
    [114] Graeber MB, Scheithauer BW, Kreutzberg GW. (2002) Microglia in brain tumors. Glia 40: 252–259. doi: 10.1002/glia.10147
    [115] Watters JJ, Schartner JM, Badie B. (2005) Microglia function in brain tumors. J Neurosci Res 81: 447–455. doi: 10.1002/jnr.20485
    [116] Hambardzumyan D, Gutmann DH, Kettenmann H. (2016) The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci 19: 20–27. doi: 10.1038/nn.4185
    [117] Brooks WH, Markesbery WR, Gupta GD, et al. (1978) Relationship of lymphocyte invasion and survival of brain tumor patients. Ann Neurol 4: 219–24. doi: 10.1002/ana.410040305
    [118] Hao C, Parney IF, Roa WH, et al. (2002) Cytokine and cytokine receptor mRNA expression in human glioblastomas: evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol 103: 171–178.. doi: 10.1007/s004010100448
    [119] Rodrigues JC, Gonzalez GC, Zhang L, et al. (2010) Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neuro Oncol 12: 351–365. doi: 10.1093/neuonc/nop023
    [120] Jackson C, Ruzevick J, Phallen J, et al. (2011) Challenges in immunotherapy presented by the glioblastoma multiforme microenvironment. Clin Dev Immunol 2011: 732413 .
    [121] Wischhusen J, Jung G, Radovanovic I, et al. (2002) Identification of CD70-mediated apoptosis of immune effector cells as a novel immune escape pathway of human glioblastoma. Cancer Res 62: 2592–2599.
    [122] Chahlavi A, Rayman P, Richmond AL, et al. (2005) Glioblastomas induce T-lymphocyte death by two distinct pathways involving gangliosides and CD70. Cancer Res 65: 5428–5438. doi: 10.1158/0008-5472.CAN-04-4395
    [123] Charles NA, Holland EC, Gilbertson R, et al. (2012) The brain tumor microenvironment. Glia 60: 502–514. doi: 10.1002/glia.21264
    [124] Wen PY, Kesari S. (2008) Malignant gliomas in adults. N Engl J Med 359: 492–507. doi: 10.1056/NEJMra0708126
    [125] Calabrese C, Poppleton H, Kocak M, et al. (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69–82. doi: 10.1016/j.ccr.2006.11.020
    [126] Charles N, Ozawa T, Squatrito M, et al. (2010) Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 6: 141–152. doi: 10.1016/j.stem.2010.01.001
    [127] Hambardzumyan D, Becher OJ, Rosenblum MK, et al. (2008) PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 22: 436–448. doi: 10.1101/gad.1627008
    [128] Shaw KM, Wrobel C, Brugge J. (2004) Use of Three-Dimensional Basement Membrane Cultures to Model Oncogene-Induced Changes in Mammary Epithelial Morphogenesis. J. Mammary Gland Biol 9: 297–310. doi: 10.1007/s10911-004-1402-z
    [129] Trédan O, Galmarini CM, Patel K, et al. (2007) Drug Resistance and the Solid Tumor Microenvironment. J Natl. Cancer Inst 99: 1441–1454. doi: 10.1093/jnci/djm135
    [130] Caliari SR, Burdick JA. (2016) A practical guide to hydrogels for cell culture. Nat Methods 13: 405–414. doi: 10.1038/nmeth.3839
    [131] Ahmed EM. (2015) Hydrogel: Preparation, characterization, and applications: A review. J Adv Res 6: 105–121. doi: 10.1016/j.jare.2013.07.006
    [132] Dawson E, Mapili G, Erickson K, et al. (2008) Biomaterials for stem cell differentiation. Adv Drug Deliv Rev 60: 215–228. doi: 10.1016/j.addr.2007.08.037
    [133] Kiefer JA, Farach-Carson MC. (2001) Type I collagen-mediated proliferation of PC3 prostate carcinoma cell line: Implications for enhanced growth in the bone microenvironment. Matrix Bio 20: 429–437. doi: 10.1016/S0945-053X(01)00159-7
    [134] Menke A, Philippi C, Vogelmann R, et al. (2001) Down-Regulation of E-Cadherin Gene Expression by Collagen Type I and Type III in Pancreatic Cancer Cell Lines. Cancer Res 61: 3508–3517.
    [135] Kim YJ, Bae HI, Kwon OK, et al. (2009) Three-dimensional gastric cancer cell culture using nanofiber scaffold for chemosensitivity test. Int J Biol Macromol 45: 65–71. doi: 10.1016/j.ijbiomac.2009.04.003
    [136] Sun W, Incitti T, Migliaresi C, et al. (2017) Viability and neuronal differentiation of neural stem cells encapsulated in silk fibroin hydrogel functionalized with an IKVAV peptide. J Tissue Eng Regen Med 11: 1532–1541. doi: 10.1002/term.2053
    [137] Musah S, Morin SA, Wrighton PJ, et al. (2012) Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS Nano 6: 10168–10177. doi: 10.1021/nn3039148
    [138] Souza GR, Molina JR, Raphael RM, et al. (2010) Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol 5: 291–296. doi: 10.1038/nnano.2010.23
    [139] Carpenter PM, Dao AV, Arain ZS, et al. (2009) Motility induction in breast carcinoma by mammary epithelial laminin 332 (laminin 5). Mol. Cancer Res 7: 462–475. doi: 10.1158/1541-7786.MCR-08-0148
    [140] Zhou Z, Wang J, Cao R, et al. (2004) Impaired Angiogenesis, Delayed Wound Healing and Retarded Tumor Growth in Perlecan Heparan Sulfate-Deficient Mice. Cancer Res 64: 4699–4702. doi: 10.1158/0008-5472.CAN-04-0810
    [141] Miyamoto H, Murakami T, Tsuchida K, et al. (2004) Tumor‐stroma interaction of human pancreatic cancer: acquired resistance to anticancer drugs and proliferation regulation is dependent on extracellular matrix proteins. Pancreas 28: 38–44. doi: 10.1097/00006676-200401000-00006
    [142] Nguyen TV, Sleiman M, Moriarty T, et al. (2014) Sorafenib resistance and JNK signaling in carcinoma during extracellular matrix stiffening. Biomaterials 35: 5749–5759. doi: 10.1016/j.biomaterials.2014.03.058
    [143] Vinci M, Gowan S, Boxall F, et al. (2012) Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol 10: 29–49. doi: 10.1186/1741-7007-10-29
    [144] Rybtsov S, Batsivari A, Bilotkach K, et al. (2014) Tracing the Origin of the HSC Hierarchy Reveals an SCF-Dependent, IL-3-Independent CD43- Embryonic Precursor. Stem Cell Rep 3: 489–501. doi: 10.1016/j.stemcr.2014.07.009
    [145] Herter S, Morra L, Schlenker R, et al. (2017) A novel three-dimensional heterotypic spheroid model for the assessment of the activity of cancer immunotherapy agents. Cancer Immunol Immunother 66: 129–140. doi: 10.1007/s00262-016-1927-1
    [146] Hirt C, Papadimitropoulos A, Mele V, et al. (2014) "In vitro" 3D models of tumor-immune system interaction. Adv Drug Deliv Rev 79-80:145–54. doi: 10.1016/j.addr.2014.05.003
    [147] Ma FX, Chen F, Chi Y, et al. (2013) Culture of pancreatic progenitor cells in hanging drop and on floating filter. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 35: 270–274.
    [148] Ingthorsson S., Sigurdsson V., Fridriksdottir JR A. (2010) Endothelial cells stimulate growth of normal and cancerous breast epithelial cells in 3D culture. BMC Res 3: 184–195. doi: 10.1186/1756-0500-3-184
    [149] Li L, Lu YJ. (2011) Optimizing a 3D Culture System to Study the Interaction between Epithelial Breast Cancer and Its Surrounding Fibroblasts. Cancer 2: 458–466. doi: 10.7150/jca.2.458
    [150] Touboul C, Raphael L, Farsi H AI, et al. (2013) Mesenchymal stem cells enhance ovarian cancer cell infiltration through IL6 secretion in an amniochorionic membrane based 3D model. J Transl. Med 11: 28–39. doi: 10.1186/1479-5876-11-28
    [151] Li L, Fukunaga-Kalabis M, Herlyn M. (2011) The three-dimensional human skin reconstruct model: a tool to study normal skin and melanoma progression. J Vis Exp 54: e2937.
    [152] Vörsmann H, Groeber F, Walles H, et al. (2013) Development of a human three-dimensional organotypic skin-melanoma spheroid model for in vitro drug testing. Cell Death Dis 4: e719. doi: 10.1038/cddis.2013.249
    [153] Carmeliet P, Jain RK. (2000) Angiogenesis in cancer and other diseases. Nature. 407: 249–257. doi: 10.1038/35025220
    [154] Upreti M, Jamshidi-Parsian A, Koonce NA, et al. (2011) Tumor-Endothelial Cell Three-dimensional Spheroids: New Aspects to Enhance Radiation and Drug Therapeutics. Transl Oncol 4: 365–376. doi: 10.1593/tlo.11187
    [155] Ramgolam K, Lauriol J, Lalou C, et al. (2011) Melanoma spheroids grown under neural crest cell conditions are highly plastic migratory/invasive tumor cells endowed with immunomodulator function. PLoS One 6: e18784. doi: 10.1371/journal.pone.0018784
    [156] Giannattasio A, Weil S, Kloess S, et al. (2015) Cytotoxicity and infiltration of human NK cells in in vivo-like tumor spheroids. BMC Cancer 15: 351–363. doi: 10.1186/s12885-015-1321-y
    [157] Marchwicka A, Cebrat M, Sampath P, et al. (2014) Perspectives of Differentiation Therapies of Acute Myeloid Leukemia: The Search for the Molecular Basis of Patients' Variable Responses to 1,25-Dihydroxyvitamin D and Vitamin D Analogs. Frontiers in Oncology 4:125–136.
    [158] Caren H, Beck S, Pollard SM. (2016) Differentiation therapy for glioblastoma–too many obstacles? Mol Cellr Oncol 3: e1124174. doi: 10.1080/23723556.2015.1124174
  • Reader Comments
  • © 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(5759) PDF downloads(1251) Cited by(13)

Article outline

Figures and Tables

Tables(2)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog