Cancer Treatment Reviews
Volume 35, Issue 8 , Pages 714-723 , December 2009

High-grade glioma mouse models and their applicability for preclinical testing

  • Nienke A. de Vries

      Affiliations

    • Department of Clinical Chemistry, The Netherlands Cancer Institute (Antoni van Leeuwenhoek Hospital), Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
    • Tel.: +31 20 512 1828.
  • ,
  • Jos H. Beijnen

      Affiliations

    • Department of Pharmacy and Pharmacology, The Netherlands Cancer Institute/Slotervaart Hospital), Louwesweg 6, 1066 EC Amsterdam, The Netherlands
    • Division of Drug Toxicology, Faculty of Pharmacy, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands
    • Tel.: +31 20 512 4342.
  • ,
  • Olaf van Tellingen

      Affiliations

    • Department of Clinical Chemistry, The Netherlands Cancer Institute (Antoni van Leeuwenhoek Hospital), Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
    • Corresponding Author InformationCorresponding author. Tel.: +31 20 512 2792; fax: +31 20 512 2799.

Received 9 June 2009 ,Revised 15 August 2009 ,Accepted 24 August 2009.

References 

  1. Mourad PD, Farrell L, Stamps LD, Chicoine MR, Silbergeld DL. Why are systemic glioblastoma metastases rare? Systemic and cerebral growth of mouse glioblastoma. Surg Neurol. 2005;63:511–519
  2. Kleihues P, Louis DN, Scheithauer BW, Rorke LB, Reifenberger G, Burger PC, et al. The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol. 2002;61:215–225
  3. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol. 2005;64:479–489
  4. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 2007;170:445–1453
  5. Rasheed BK, Wiltshire RN, Bigner SH, Bigner DD. Molecular pathogenesis of malignant gliomas. Curr Opin Oncol. 1999;11:162–167
  6. Solomon DA, Kim JS, Jean W, Waldman T. Conspirators in a capital crime: co-deletion of p18INK4c and p16INK4a/p14ARF/p15INK4b in glioblastoma multiforme. Cancer Res. 2008;68:8657–8660
  7. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, et al. Malignant glioma: genetics and biology of a grave matter. Genes Dev. 2001;15:1311–1333
  8. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2006;21:2683–2710
  9. Cully M, You H, Levine AJ, Mak TW. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer. 2006;6:184–192
  10. Wong ML, Kaye AH, Hovens CM. Targeting malignant glioma survival signalling to improve clinical outcomes. J Clin Neurosci. 2007;14:301–308
  11. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer. 2003;3:11–22
  12. Guha A, Feldkamp MM, Lau N, Boss G, Pawson A. Proliferation of human malignant astrocytomas is dependent on Ras activation. Oncogene. 1997;15:2755–2765
  13. Nozaki M, Tada M, Kobayashi H, Zhang CL, Sawamura Y, Abe H, et al. Roles of the functional loss of p53 and other genes in astrocytoma tumorigenesis and progression. Neuro Oncol. 1999;1:124–137
  14. Ivanchuk SM, Mondal S, Dirks PB, Rutka JT. The INK4A/ARF locus: role in cell cycle control and apoptosis and implications for glioma growth. J Neurooncol. 2001;51:219–229
  15. Gil J, Peters G. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol. 2006;7:667–677
  16. Ohgaki H, Dessen P, Jourde B, Horstmann S, Nishikawa T, Di Patre PL, et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 2004;64:6892–6899
  17. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, et al. P53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature. 2008;455:1129–1133
  18. The Cancer Genome Atlas Research Network . Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455:1061–1068
  19. Fukushima T, Favereaux A, Huang H, Shimizu T, Yonekawa Y, Nakazato Y, et al. Genetic alterations in primary glioblastomas in Japan. J Neuropathol Exp Neurol. 2006;65:12–18
  20. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–996
  21. Grossman SA. Arguments against the routine use of currently available adjuvant chemotherapy in high-grade gliomas. Semin Oncol. 2003;30:19–22
  22. de Vries NA, Beijnen JH, Boogerd W, van Tellingen O. Blood–brain barrier and chemotherapeutic treatment of brain tumors. Expert Rev Neurother. 2006;6:1199–1209
  23. Perry J, Chambers A, Spithoff K, Laperriere N. Gliadel wafers in the treatment of malignant glioma: a systematic review. Curr Oncol. 2007;14:189–194
  24. Hart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K. Chemotherapeutic wafers for high grade glioma. Cochrane Database Syst Rev. 2008;CD007294
  25. Bota DA, Desjardins A, Quinn JA, Affronti ML, Friedman HS. Interstitial chemotherapy with biodegradable BCNU (Gliadel) wafers in the treatment of malignant gliomas. Ther Clin Risk Manage. 2007;3:707–715
  26. Norden AD, Drappatz J, Wen PY. Novel anti-angiogenic therapies for malignant gliomas. Lancet Neurol. 2008;7:1152–1160
  27. Miletic H, Niclou SP, Johansson M, Bjerkvig R. Anti-VEGF therapies for malignant glioma: treatment effects and escape mechanisms. Expert Opin Ther Targets. 2009;13:455–468
  28. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220–231
  29. Claes A, Wesseling P, Jeuken J, Maass C, Heerschap A, Leenders WP. Antiangiogenic compounds interfere with chemotherapy of brain tumors due to vessel normalization. Mol Cancer Ther. 2008;7:71–78
  30. Bradley NJ, Bloom HJ, Davies AJ, Swift SM. Growth of human gliomas in immune-deficient mice: a possible model for pre-clinical therapy studies. Brit J Cancer. 1978;38:263–272
  31. Bullard DE, Schold SC, Bigner SH, Bigner DD. Growth and chemotherapeutic response in athymic mice of tumors arising from human glioma-derived cell lines. J Neuropathol Exp Neurol. 1981;40:410–427
  32. Horten BC, Basler GA, Shapiro WR. Xenograft of human malignant glial tumors into brains of nude mice. A histopatholgical study. J Neuropathol Exp Neurol. 1981;40:493–511
  33. Shapiro WR, Basler GA, Chernik NL, Posner JB. Human brain tumor transplantation into nude mice. J Natl Cancer Inst. 1979;62:447–453
  34. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, 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. Cancer Cell. 2006;9:391–403
  35. Antunes L, Angioi-Duprez KS, Bracard SR, Klein-Monhoven NA, Le Faou AE, Duprez AM, et al. Analysis of tissue chimerism in nude mouse brain and abdominal xenograft models of human glioblastoma multiforme: what does it tell us about the models and about glioblastoma biology and therapy?. J Histochem Cytochem. 2000;48:847–858
  36. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011–7021
  37. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene. 2004;23:7267–7273
  38. Aguzzi A, Brandner S, Isenmann S, Steinbach JP, Sure U. Transgenic and gene disruption techniques in the study of neurocarcinogenesis. Glia. 1995;15:348–364
  39. Weissenberger J, Steinbach JP, Malin G, Spada S, Rulicke T, Aguzzi A. Development and malignant progression of astrocytomas in GFAP-v-src transgenic mice. Oncogene. 1997;14:2005–2013
  40. Ding H, Roncari L, Shannon P, Wu X, Lau N, Karaskova J, et al. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res. 2001;61:3826–3836
  41. Xiao A, Wu H, Pandolfi PP, Louis DN, Van Dyke T. Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell. 2002;1:157–168
  42. Reilly KM, Loisel DA, Bronson RT, McLaughlin ME, Jacks T. Nf1; Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat Genet. 2000;26:109–113
  43. Zhu Y, Guignard F, Zhao D, Liu L, Burns DK, Mason RP, et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell. 2005;8:119–130
  44. Wang Y, Yang J, Zheng H, Tomasek GJ, Zhang P, McKeever PE, et al. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell. 2009;15:514–526
  45. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 2000;14:994–1004
  46. Backman SA, Stambolic V, Suzuki A, Haight J, Elia A, Pretorius J, et al. Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet. 2001;29:396–403
  47. Kwon CH, Zhu X, Zhang J, Knoop LL, Tharp R, Smeyne RJ, et al. Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet. 2001;29:404–411
  48. Furth PA, St Onge L, Boger H, Gruss P, Gossen M, Kistner A, et al. Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. Proc Natl Acad Sci USA. 1994;91:9302–9306
  49. Sauer B, Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA. 1988;85:5166–5170
  50. Lakso M, Sauer B, Mosinger B, Lee EJ, Manning RW, Yu SH, et al. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc Natl Acad Sci USA. 1992;89:6232–6236
  51. Alcantara Llaguno S, Chen J, Kwon CH, Jackson EL, Li Y, Burns DK, et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell. 2009;15:45–56
  52. Uhrbom L, Hesselager G, Nister M, Westermark B. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res. 1998;58:5275–5279
  53. Holland EC, Varmus HE. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc Natl Acad Sci USA. 1998;95:1218–1223
  54. Holland EC, Hively WP, Gallo V, Varmus HE. Modeling mutations in the G1 arrest pathway in human gliomas: overexpression of CDK4 but not loss of INK4a-ARF induces hyperploidy in cultured mouse astrocytes. Genes Dev. 1998;12:3644–3649
  55. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet. 2000;25:55–57
  56. Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res. 2002;62:5551–5558
  57. Holmen SL, Williams BO. Essential role for Ras signaling in glioblastoma maintenance. Cancer Res. 2005;65:8250–8255
  58. Wei Q, Clarke L, Scheidenhelm DK, Qian B, Tong A, Sabha N, et al. High-grade glioma formation results from postnatal Pten loss or mutant epidermal growth factor receptor expression in a transgenic mouse glioma model. Cancer Res. 2006;66:7429–7437
  59. Charest A, Wilker EW, McLaughlin ME, Lane K, Gowda R, Coven S, et al. ROS fusion tyrosine kinase activates a SH2 domain-containing phosphatase-2/phosphatidylinositol 3-kinase/mammalian target of rapamycin signaling axis to form glioblastoma in mice. Cancer Res. 2006;66:7473–7481
  60. Marumoto T, Tashiro A, Friedmann-Morvinski D, Scadeng M, Soda Y, Gage FH, et al. Development of a novel mouse glioma model using lentiviral vectors. Nat Med. 2009;15:110–116
  61. Wiesner SM, Decker SA, Larson JD, Ericson K, Forster C, Gallardo JL, et al. De novo induction of genetically engineered brain tumors in mice using plasmid DNA. Cancer Res. 2009;69:431–439
  62. Hambardzumyan D, Amankulor NM, Helmy KY, Becher OJ, Holland EC. Modeling adult gliomas using RCAS/t-va technology. Transl Oncol. 2009;2:89–95
  63. Maira SM, Stauffer F, Brueggen J, Furet P, Schnell C, Fritsch C, et al. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther. 2008;7:1851–1863
  64. Delmas C, End D, Rochaix P, Favre G, Toulas C, Cohen-Jonathan E. The farnesyltransferase inhibitor R115777 reduces hypoxia and matrix metalloproteinase 2 expression in human glioma xenograft. Clin Cancer Res. 2003;9:6062–6068
  65. Feldkamp MM, Lau N, Roncari L, Guha A. Isotype-specific Ras. GTP-levels predict the efficacy of farnesyl transferase inhibitors against human astrocytomas regardless of Ras mutational status. Cancer Res. 2001;61:4425–4431
  66. Geoerger B, Kerr K, Tang CB, Fung KM, Powell B, Sutton LN, et al. Antitumor activity of the rapamycin analog CCI-779 in human primitive neuroectodermal tumor/medulloblastoma models as single agent and in combination chemotherapy. Cancer Res. 2001;61:1527–1532
  67. Momota H, Nerio E, Holland EC. Perifosine inhibits multiple signaling pathways in glial progenitors and cooperates with temozolomide to arrest cell proliferation in gliomas in vivo. Cancer Res. 2005;65:7429–7435
  68. Hu X, Pandolfi PP, Li Y, Koutcher JA, Rosenblum M, Holland EC. MTOR promotes survival and astrocytic characteristics induced by Pten/AKT signaling in glioblastoma. Neoplasia. 2005;7:356–368
  69. Koutcher JA, Hu X, Xu S, Gade TP, Leeds N, Zhou XJ, et al. MRI of mouse models for gliomas shows similarities to humans and can be used to identify mice for preclinical trials. Neoplasia. 2002;4:480–485
  70. Enochs WS, Harsh G, Hochberg F, Weissleder R. Improved delineation of human brain tumors on MR images using a long-circulating, superparamagnetic iron oxide agent. J Magn Reson Imaging. 1999;9:228–232
  71. Gambarota G, Leenders WP, Maass C, Wesseling P, van der Kogel B, van Tellingen O, et al. Characterisation of tumour vasculature in mouse brain by USPIO contrast-enhanced MRI. Brit J Cancer. 2008;98:1784–1789
  72. Rehemtulla A, Stegman LD, Cardozo SJ, Gupta S, Hall DE, Contag CH, et al. Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia. 2000;2:491–495
  73. Kemper EM, Leenders W, Kusters B, Lyons S, Buckle T, Heerschap A, et al. Development of luciferase tagged brain tumour models in mice for chemotherapy intervention studies. Eur J Cancer. 2006;42:3294–3303
  74. Lyons SK, Meuwissen R, Krimpenfort P, Berns A. The generation of a conditional reporter that enables bioluminescence imaging of Cre/loxP-dependent tumorigenesis in mice. Cancer Res. 2003;63:7042–7046
  75. Uhrbom L, Nerio E, Holland EC. Dissecting tumor maintenance requirements using bioluminescence imaging of cell proliferation in a mouse glioma model. Nat Med. 2004;10:1257–1260
  76. Hoffman RM. Imaging in mice with fluorescent proteins: from macro to subcellular. Sensors. 2008;8:1157–1173
  77. Wolburg H, Lippoldt A. Tight junctions of the blood–brain barrier: development, composition and regulation. Vascul Pharmacol. 2002;38:323–337
  78. Deeken JF, Loscher W. The blood–brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res. 2007;13:1663–1674
  79. de Vries NA, Zhao J, Kroon E, Buckle T, Beijnen JH, van Tellingen O. P-glycoprotein and breast cancer resistance protein: two dominant transporters working together in limiting the brain penetration of topotecan. Clin Cancer Res. 2007;13:6440–6449
  80. Hann B, Balmain A. Building ‘validated’ mouse models of human cancer. Curr Opin Cell Biol. 2001;13:778–784
  81. Sharpless NE, DePinho RA. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov. 2006;5:741–754
  82. Sathornsumetee S, Reardon DA, Desjardins A, Quinn JA, Vredenburgh JJ, Rich JN. Molecularly targeted therapy for malignant glioma. Cancer. 2007;110:13–24
  83. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359:492–507
  84. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA. 2000;97:12846–12851
  85. Joo KM, Kim SY, Jin X, Song SY, Kong DS, Lee JI, et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest. 2008;88:808–815
  86. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ, et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell. 2002;1:269–277

PII: S0305-7372(09)00124-8

doi: 10.1016/j.ctrv.2009.08.011

Cancer Treatment Reviews
Volume 35, Issue 8 , Pages 714-723 , December 2009