Genetically engineered mouse models of diffuse gliomas

Brain Research Bulletin

Volumn 88, Issue 1, 2012, Pages 72-79

  Schmid, Ralf S ^a   Vitucci, Mark ^a   Miller, C Ryan ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Genetically engineered mouse models; Glioblastoma; Glioma; Gliomagenesis

Indexed keywords

AFIMOXIFENE; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; TEMOZOLOMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN TUMOR; CANCER RESEARCH; CANCER STEM CELL; COMPARATIVE STUDY; DRUG EFFICACY; DRUG SCREENING; GENETIC ENGINEERING; GENETICALLY ENGINEERED MOUSE MODEL; GENOMICS; GLIOMA; HIGH THROUGHPUT SEQUENCING; HISTOPATHOLOGY; HUMAN; MOLECULARLY TARGETED THERAPY; MOUSE; NEUROSCIENCE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; REVIEW; TRANSLATIONAL RESEARCH; TUMOR CLASSIFICATION; TUMOR MODEL;

ANIMALS; BRAIN NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; COMPARATIVE GENOMIC HYBRIDIZATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENETIC ENGINEERING; GLIOMA; HUMANS; MICE; MICE, NEUROLOGIC MUTANTS;

EID: 84860488219     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.06.002     Document Type: Review

References (118)

1. Abel T.W., Clark C., Bierie B., Chytil A., Aakre M., Gorska A., Moses H.L. GFAP-Cre-mediated activation of oncogenic K-ras results in expansion of the subventricular zone and infiltrating glioma. Mol. Cancer Res. 2009, 7:645-653.
2. Alcantara Llaguno S., Chen J., Kwon C.H., Jackson E.L., Li Y., Burns D.K., Alvarez-Buylla A., Parada L.F. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009, 15:45-56.
3. Alcantara Llaguno S.R., Chen J., Parada L.F. Signaling in malignant astrocytomas: role of neural stem cells and its therapeutic implications. Clin. Cancer Res. 2009, 15:7124-7129.
4. Bachoo R.M., Maher E.A., Ligon K.L., Sharpless N.E., Chan S.S., You M.J., Tang Y., DeFrances J., Stover E., Weissleder R., Rowitch D.H., Louis D.N., DePinho R.A. 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.
5. P. Bailey, H. Cushing, A classification of the tumors of the glioma subgroup on a histogenetic basis with a correlated study of prognosis, Philadelphia, 1926.
6. 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.
7. Barami K., Sloan A.E., Rojiani A., Schell M.J., Staller A., Brem S. Relationship of gliomas to the ventricular walls. J. Clin. Neurosci. 2009, 16:195-201.
8. Becher O.J., Holland E.C. Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res. 2006, 66:3355-3358.
9. Beckervordersandforth R., Tripathi P., Ninkovic J., Bayam E., Lepier A., Stempfhuber B., Kirchhoff F., Hirrlinger J., Haslinger A., Lie D.C., Beckers J., Yoder B., Irmler M., Gotz M. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 2010, 7:744-758.
10. Burchill S.A. What do, can and should we learn from models to evaluate potential anticancer agents?. Future Oncol. 2006, 2:201-211.
11. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., Barres B.A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
12. Carretero J., Shimamura T., Rikova K., Jackson A.L., Wilkerson M.D., Borgman C.L., Buttarazzi M.S., Sanofsky B.A., McNamara K.L., Brandstetter K.A., Walton Z.E., Gu T.L., Silva J.C., Crosby K., Shapiro G.I., Maira S.M., Ji H., Castrillon D.H., Kim C.F., Garcia-Echeverria C., Bardeesy N., Sharpless N.E., Hayes N.D., Kim W.Y., Engelman J.A., Wong K.K. Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 2010, 17:547-559.
13. Casper K.B., Jones K., McCarthy K.D. Characterization of astrocyte-specific conditional knockouts. Genesis 2007, 45:292-299.
14. CBTRUS, Primary brain and central nervous system tumors diagnosed in the United States in 2004-2007 CBTRUS (Central Brain Tumor Registry of the United States), Chicago, IL, 2011.
15. Charest A., Wilker E.W., McLaughlin M.E., Lane K., Gowda R., Coven S., McMahon K., Kovach S., Feng Y., Yaffe M.B., Jacks T., Housman D. 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.
16. Cheng L., Bao S., Rich J.N. Potential therapeutic implications of cancer stem cells in glioblastoma. Biochem. Pharmacol. 2010, 80:654-665.
17. Cheon D.J., Orsulic S. Mouse models of cancer. Annu. Rev. Pathol. Mech. Dis. 2011, 6:95-119.
18. Chow L.M., Endersby R., Zhu X., Rankin S., Qu C., Zhang J., Broniscer A., Ellison D.W., Baker S.J. Cooperativity within and among Pten, p53, and Rb pathways induces high-grade astrocytoma in adult brain. Cancer Cell 2011, 19:305-316.
19. Dai C., Celestino J.C., Okada Y., Louis D.N., Fuller G.N., Holland E.C. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 2001, 15:1913-1925.
20. de Vries N.A., Beijnen J.H., van Tellingen O. High-grade glioma mouse models and their applicability for preclinical testing. Cancer Treat. Rev. 2009, 35:714-723.
21. de Vries N.A., Bruggeman S.W., Hulsman D., de Vries H.I., Zevenhoven J., Buckle T., Hamans B.C., Leenders W.P., Beijnen J.H., van Lohuizen M., Berns A.J., van Tellingen O. Rapid and robust transgenic high-grade glioma mouse models for therapy intervention studies. Clin. Cancer Res. 2010, 16:3431-3441.
22. Di Cristofano A., Pesce B., Cordon-Cardo C., Pandolfi P.P. Pten is essential for embryonic development and tumour suppression. Nat. Genet. 1998, 19:348-355.
23. Ding H., Roncari L., Shannon P., Wu X., Lau N., Karaskova J., Gutmann D.H., Squire J.A., Nagy A., Guha A. 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.
24. Ding H., Shannon P., Lau N., Wu X., Roncari L., Baldwin R.L., Takebayashi H., Nagy A., Gutmann D.H., Guha A. Oligodendrogliomas result from the expression of an activated mutant epidermal growth factor receptor in a RAS transgenic mouse astrocytoma model. Cancer Res. 2003, 63:1106-1113.
25. Dunlap S.M., Celestino J., Wang H., Jiang R., Holland E.C., Fuller G.N., Zhang W. Insulin-like growth factor binding protein 2 promotes glioma development and progression. Proc. Natl. Acad. Sci. U.S.A. 2007.
26. Ellwood-Yen K., Graeber T.G., Wongvipat J., Iruela-Arispe M.L., Zhang J., Matusik R., Thomas G.V., Sawyers C.L. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003, 4:223-238.
27. Feil R., Wagner J., Metzger D., Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 1997, 237:752-757.
28. Freije W.A., Castro-Vargas F.E., Fang Z., Horvath S., Cloughesy T., Liau L.M., Mischel P.S., Nelson S.F. Gene expression profiling of gliomas strongly predicts survival. Cancer Res. 2004, 64:6503-6510.
29. Frese K.K., Tuveson D.A. Maximizing mouse cancer models. Nat. Rev. Cancer 2007, 7:645-658.
30. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., Hahn W.C., Ligon K.L., Louis D.N., Brennan C., Chin L., DePinho R.A., Cavenee W.K. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007, 21:2683-2710.
31. 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.
32. Gilbertson R.J. Mapping cancer origins. Cell 2011, 145:25-29.
33. Graeber T.G., Sawyers C.L. Cross-species comparisons of cancer signaling. Nat. Genet. 2005, 37:7-8.
34. Gravendeel L.A., Kouwenhoven M.C., Gevaert O., de Rooi J.J., Stubbs A.P., Duijm J.E., Daemen A., Bleeker F.E., Bralten L.B., Kloosterhof N.K., De Moor B., Eilers P.H., van der Spek P.J., Kros J.M., Sillevis Smitt P.A., van den Bent M.J., French P.J. Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res. 2009, 69:9065-9072.
35. Gutmann D.H., Hunter-Schaedle K., Shannon K.M. Harnessing preclinical mouse models to inform human clinical cancer trials. J. Clin. Invest. 2006, 116:847-852.
36. Haber D.A., Settleman J. Cancer: drivers and passengers. Nature 2007, 446:145-146.
37. Hadjipanayis C.G., Van Meir E.G. Brain cancer propagating cells: biology, genetics and targeted therapies. Trends Mol. Med. 2009, 15:519-530.
38. Herschkowitz J.I., Simin K., Weigman V.J., Mikaelian I., Usary J., Hu Z., Rasmussen K.E., Jones L.P., Assefnia S., Chandrasekharan S., Backlund M.G., Yin Y., Khramtsov A.I., Bastein R., Quackenbush J., Glazer R.I., Brown P.H., Green J.E., Kopelovich L., Furth P.A., Palazzo J.P., Olopade O.I., Bernard P.S., Churchill G.A., Van Dyke T., Perou C.M. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 2007, 8:R76.
39. Heyer J., Kwong L.N., Lowe S.W., Chin L. Non-germline genetically engineered mouse models for translational cancer research. Nat. Rev. Cancer 2010, 10:470-480.
40. Holland E.C., Celestino J., Dai C., Schaefer L., Sawaya R.E., Fuller G.N. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet. 2000, 25:55-57.
41. Holland E.C., Hively W.P., DePinho R.A., Varmus H.E. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 1998, 12:3675-3685.
42. Holland E.C., Li Y., Celestino J., Dai C., Schaefer L., Sawaya R.A., Fuller G.N. Astrocytes give rise to oligodendrogliomas and astrocytomas after gene transfer of polyoma virus middle T antigen in vivo. Am. J. Pathol. 2000, 157:1031-1037.
43. Holland E.C., Varmus H.E. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:1218-1223.
44. Hu X., Pandolfi P.P., Li Y., Koutcher J.A., Rosenblum M., Holland E.C. mTOR promotes survival and astrocytic characteristics induced by Pten/AKT signaling in glioblastoma. Neoplasia 2005, 7:356-368.
45. Huse J.T., Holland E.C. Genetically engineered mouse models of brain cancer and the promise of preclinical testing. Brain Pathol. 2009, 19:132-143.
46. Jacques T.S., Swales A., Brzozowski M.J., Henriquez N.V., Linehan J.M., Mirzadeh Z., O'Malley C., Naumann H., Alvarez-Buylla A., Brandner S. Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J. 2010, 29:222-235.
47. Johnson J.I., Decker S., Zaharevitz D., Rubinstein L.V., Venditti J.M., Schepartz S., Kalyandrug S., Christian M., Arbuck S., Hollingshead M., Sausville E.A. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 2001, 84:1424-1431.
48. Jonkers J., Berns A. Conditional mouse models of sporadic cancer. Nat. Rev. Cancer 2002, 2:251-265.
49. Joyner A.L., Zervas M. Genetic inducible fate mapping in mouse: establishing genetic lineages and defining genetic neuroanatomy in the nervous system. Dev. Dyn. 2006, 235:2376-2385.
50. Koutcher J.A., Hu X., Xu S., Gade T.P., Leeds N., Zhou X.J., Zagzag D., Holland E.C. 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.
51. Kwon C.H., Zhao D., Chen J., Alcantara S., Li Y., Burns D.K., Mason R.P., Lee E.Y., Wu H., Parada L.F. Pten haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res. 2008, 68:3286-3294.
52. Lassman A.B., Dai C., Fuller G.N., Vickers A.J., Holland E.C. Overexpression of c-MYC promotes an undifferentiated phenotype in cultured astrocytes and allows elevated Ras and Akt signaling to induce gliomas from GFAP-expressing cells in mice. Neuron Glia Biol. 2004, 1:157-163.
53. Lee J.S., Chu I.S., Mikaelyan A., Calvisi D.F., Heo J., Reddy J.K., Thorgeirsson S.S. Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat. Genet. 2004, 36:1306-1311.
54. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., Chen L., Chen T.M., Chin M.C., Chong J., Crook B.E., Czaplinska A., Dang C.N., Datta S., Dee N.R., Desaki A.L., Desta T., Diep E., Dolbeare T.A., Donelan M.J., Dong H.W., Dougherty J.G., Duncan B.J., Ebbert A.J., Eichele G., Estin L.K., Faber C., Facer B.A., Fields R., Fischer S.R., Fliss T.P., Frensley C., Gates S.N., Glattfelder K.J., Halverson K.R., Hart M.R., Hohmann J.G., Howell M.P., Jeung D.P., Johnson R.A., Karr P.T., Kawal R., Kidney J.M., Knapik R.H., Kuan C.L., Lake J.H., Laramee A.R., Larsen K.D., Lau C., Lemon T.A., Liang A.J., Liu Y., Luong L.T., Michaels J., Morgan J.J., Morgan R.J., Mortrud M.T., Mosqueda N.F., Ng L.L., Ng R., Orta G.J., Overly C.C., Pak T.H., Parry S.E., Pathak S.D., Pearson O.C., Puchalski R.B., Riley Z.L., Rockett H.R., Rowland S.A., Royall J.J., Ruiz M.J., Sarno N.R., Schaffnit K., Shapovalova N.V., Sivisay T., Slaughterbeck C.R., Smith S.C., Smith K.A., Smith B.I., Sodt A.J., Stewart N.N., Stumpf K.R., Sunkin S.M., Sutram M., Tam A., Teemer C.D., Thaller C., Thompson C.L., Varnam L.R., Visel A., Whitlock R.M., Wohnoutka P.E., Wolkey C.K., Wong V.Y., Wood M., Yaylaoglu M.B., Young R.C., Youngstrom B.L., Yuan X.F., Zhang B., Zwingman T.A., Jones A.R. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
55. Li A., Walling J., Ahn S., Kotliarov Y., Su Q., Quezado M., Oberholtzer J.C., Park J., Zenklusen J.C., Fine H.A. Unsupervised analysis of transcriptomic profiles reveals six glioma subtypes. Cancer Res. 2009, 69:2091-2099.
56. Li A., Walling J., Kotliarov Y., Center A., Steed M.E., Ahn S.J., Rosenblum M., Mikkelsen T., Zenklusen J.C., Fine H.A. Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol. Cancer Res. 2008, 6:21-30.
57. 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.
58. Maire C.L., Ligon K.L. Glioma models: new GEMMs add " class" with genomic and expression correlations. Cancer Cell 2011, 19:295-297.
59. Marusyk A., Polyak K. Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta 2010, 1805:105-117.
60. McConville P., Hambardzumyan D., Moody J.B., Leopold W.R., Kreger A.R., Woolliscroft M.J., Rehemtulla A., Ross B.D., Holland E.C. Magnetic resonance imaging determination of tumor grade and early response to temozolomide in a genetically engineered mouse model of glioma. Clin. Cancer Res. 2007, 13:2897-2904.
61. Metzger D., Chambon P. Site- and time-specific gene targeting in the mouse. Methods 2001, 24:71-80.
62. Miller C.R., Karpinich N.O., Zhang Q., Bullitt E., Kozlov S., Van Dyke T. Modeling astrocytomas in a family of inducible genetically engineered mice: implications for preclinical cancer drug development. CNS Cancer, Cancer Drug Discovery and Development 2009, 119-145. Humana Press. E.G. Van Meir (Ed.).
63. Miller C.R., Perry A. Glioblastoma. Arch. Pathol. Lab. Med. 2007, 131:397-406.
64. Miller C.R., Williams C.R., Buchsbaum D.J., Gillespie G.Y. Intratumoral 5-fluorouracil produced by cytosine deaminase/5-fluorocytosine gene therapy is effective for experimental human glioblastomas. Cancer Res. 2002, 62:773-780.
65. Molyneux G., Geyer F.C., Magnay F.A., McCarthy A., Kendrick H., Natrajan R., Mackay A., Grigoriadis A., Tutt A., Ashworth A., Reis-Filho J.S., Smalley M.J. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010, 7:403-417.
66. Murat A., Migliavacca E., Gorlia T., Lambiv W.L., Shay T., Hamou M.F., de Tribolet N., Regli L., Wick W., Kouwenhoven M.C., Hainfellner J.A., Heppner F.L., Dietrich P.Y., Zimmer Y., Cairncross J.G., Janzer R.C., Domany E., Delorenzi M., Stupp R., Hegi M.E. Stem cell-related " self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J. Clin. Oncol. 2008, 26:3015-3024.
67. 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., 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. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
68. Nutt C.L., Mani D.R., Betensky R.A., Tamayo P., Cairncross J.G., Ladd C., Pohl U., Hartmann C., McLaughlin M.E., Batchelor T.T., Black P.M., von Deimling A., Pomeroy S.L., Golub T.R., Louis D.N. Gene expression-based classification of malignant gliomas correlates better with survival than histological classification. Cancer Res. 2003, 63:1602-1607.
69. Ohgaki H., Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am. J. Pathol. 2007, 170:1445-1453.
70. Orsulic S. An RCAS-TVA-based approach to designer mouse models. Mamm. Genome 2002, 13:543-547.
71. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., Olivi A., McLendon R., Rasheed B.A., Keir S., Nikolskaya T., Nikolsky Y., Busam D.A., Tekleab H., Diaz L.A., Hartigan J., Smith D.R., Strausberg R.L., Marie S.K., Shinjo S.M., Yan H., Riggins G.J., Bigner D.D., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
72. Persson A.I., Petritsch C., Swartling F.J., Itsara M., Sim F.J., Auvergne R., Goldenberg D.D., Vandenberg S.R., Nguyen K.N., Yakovenko S., Ayers-Ringler J., Nishiyama A., Stallcup W.B., Berger M.S., Bergers G., McKnight T.R., Goldman S.A., Weiss W.A. Non-stem cell origin for oligodendroglioma. Cancer Cell 2010, 18:669-682.
73. 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.
74. Quinones-Hinojosa A., Chaichana K. The human subventricular zone: a source of new cells and a potential source of brain tumors. Exp. Neurol. 2007, 205:313-324.
75. Reilly K.M., Loisel D.A., Bronson R.T., McLaughlin M.E., Jacks T. Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat. Genet. 2000, 26:109-113.
76. Reilly K.M., Tuskan R.G., Christy E., Loisel D.A., Ledger J., Bronson R.T., Smith C.D., Tsang S., Munroe D.J., Jacks T. Susceptibility to astrocytoma in mice mutant for Nf1 and Trp53 is linked to chromosome 11 and subject to epigenetic effects. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13008-13013.
77. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
78. Sanai N., Alvarez-Buylla A., Berger M.S. Neural stem cells and the origin of gliomas. N. Engl. J. Med. 2005, 353:811-822.
79. Serrano M., Lee H., Chin L., Cordon-Cardo C., Beach D., DePinho R.A. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996, 85:27-37.
80. Shannon P., Sabha N., Lau N., Kamnasaran D., Gutmann D.H., Guha A. Pathological and molecular progression of astrocytomas in a GFAP:12 V-Ha-Ras mouse astrocytoma model. Am. J. Pathol. 2005, 167:859-867.
81. Sharpless N.E., Depinho R.A. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat. Rev. Drug Discov. 2006, 5:741-754.
82. Shih A.H., Dai C., Hu X., Rosenblum M.K., Koutcher J.A., Holland E.C. Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis. Cancer Res. 2004, 64:4783-4789.
83. Shirahata M., Iwao-Koizumi K., Saito S., Ueno N., Oda M., Hashimoto N., Takahashi J.A., Kato K. Gene expression-based molecular diagnostic system for malignant gliomas is superior to histological diagnosis. Clin. Cancer Res. 2007, 13:7341-7356.
84. Siebzehnrubl F.A., Reynolds B.A., Vescovi A., Steindler D.A., Deleyrolle L.P. The origins of glioma: E Pluribus Unum?. Glia 2011, 59:1135-1147.
85. 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.
86. 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.
87. Stiles C.D., Rowitch D.H. Glioma stem cells: a midterm exam. Neuron 2008, 58:832-846.
88. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J., Janzer R.C., Ludwin S.K., Allgeier A., Fisher B., Belanger K., Hau P., Brandes A.A., Gijtenbeek J., Marosi C., Vecht C.J., Mokhtari K., Wesseling P., Villa S., Eisenhauer E., Gorlia T., Weller M., Lacombe D., Cairncross J.G., Mirimanoff R.O. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10:459-466.
89. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., 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. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
90. Sweet-Cordero A., Mukherjee S., Subramanian A., You H., Roix J.J., Ladd-Acosta C., Mesirov J., Golub T.R., Jacks T. An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat. Genet. 2005, 37:48-55.
91. TCGA Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068.
92. Tchougounova E., Kastemar M., Brasater D., Holland E.C., Westermark B., Uhrbom L. Loss of Arf causes tumor progression of PDGFB-induced oligodendroglioma. Oncogene 2007, 26:6289-6296.
93. Theurillat J.P., Hainfellner J., Maddalena A., Weissenberger J., Aguzzi A. Early induction of angiogenetic signals in gliomas of GFAP-v-src transgenic mice. Am. J. Pathol. 1999, 154:581-590.
94. Uhrbom L., Dai C., Celestino J.C., Rosenblum M.K., Fuller G.N., Holland E.C. 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.
95. 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.
96. Uhrbom L., Kastemar M., Johansson F.K., Westermark B., Holland E.C. Cell type-specific tumor suppression by Ink4a and Arf in Kras-induced mouse gliomagenesis. Cancer Res. 2005, 65:2065-2069.
97. Uhrbom L., Nerio E., Holland E.C. Dissecting tumor maintenance requirements using bioluminescence imaging of cell proliferation in a mouse glioma model. Nat. Med. 2004, 10:1257-1260.
98. Van Dyke T., Jacks T. Cancer modeling in the modern era: progress and challenges. Cell 2002, 108:135-144.
99. Verhaak R.G., 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.
100. Visvader J.E. Cells of origin in cancer. Nature 2011, 469:314-322.
101. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8:755-768.
102. Vitucci M., Hayes D.N., Miller C.R. Gene expression profiling of gliomas: merging genomic and histopathological classification for personalised therapy. Br. J. Cancer 2011, 104:545-553.
103. Voskoglou-Nomikos T., Pater J.L., Seymour L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin. Cancer Res. 2003, 9:4227-4239.
104. Ward R.J., Dirks P.B. Cancer stem cells: at the headwaters of tumor development. Annu. Rev. Pathol. Mech. Dis. 2007, 2:175-189.
105. Wei Q., Clarke L., Scheidenhelm D.K., Qian B., Tong A., Sabha N., Karim Z., Bock N.A., Reti R., Swoboda R., Purev E., Lavoie J.F., Bajenaru M.L., Shannon P., Herlyn D., Kaplan D., Henkelman R.M., Gutmann D.H., Guha A. 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.
106. Weiss W.A., Burns M.J., Hackett C., Aldape K., Hill J.R., Kuriyama H., Kuriyama N., Milshteyn N., Roberts T., Wendland M.F., DePinho R., Israel M.A. Genetic determinants of malignancy in a mouse model for oligodendroglioma. Cancer Res. 2003, 63:1589-1595.
107. Weissenberger J., Steinbach J.P., 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.
108. Wen P.Y., Kesari S. Malignant gliomas in adults. N. Engl. J. Med. 2008, 359:492-507.
109. Xiao A., Wu H., Pandolfi P.P., Louis D.N., 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.
110. Xiao A., Yin C., Yang C., Di Cristofano A., Pandolfi P.P., Van Dyke T. Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res. 2005, 65:5172-5180.
111. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., Kos I., Batinic-Haberle I., Jones S., Riggins G.J., Friedman H., Friedman A., Reardon D., Herndon J., Kinzler K.W., Velculescu V.E., Vogelstein B., Bigner D.D. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009, 360:765-773.
112. Zeppernick F., Ahmadi R., Campos B., Dictus C., Helmke B.M., Becker N., Lichter P., Unterberg A., Radlwimmer B., Herold-Mende C.C. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin. Cancer Res. 2008, 14:123-129.
113. Zhu H., Acquaviva J., Ramachandran P., Boskovitz A., Woolfenden S., Pfannl R., Bronson R.T., Chen J.W., Weissleder R., Housman D.E., Charest A. Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2712-2716.
114. Zhu H., Woolfenden S., Bronson R.T., Jaffer Z.M., Barluenga S., Winssinger N., Rubenstein A.E., Chen R., Charest A. The novel Hsp90 inhibitor NXD30001 induces tumor regression in a genetically engineered mouse model of glioblastoma multiforme. Mol. Cancer Ther. 2010, 9:2618-2626.
115. Zhu Y., Guignard F., Zhao D., Liu L., Burns D.K., Mason R.P., Messing A., Parada L.F. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 2005, 8:119-130.
116. Zhu Y., Harada T., Liu L., Lush M.E., Guignard F., Harada C., Burns D.K., Bajenaru M.L., Gutmann D.H., Parada L.F. Inactivation of NF1 in CNS causes increased glial progenitor proliferation and optic glioma formation. Development 2005, 132:5577-5588.
117. Zindy F., Uziel T., Ayrault O., Calabrese C., Valentine M., Rehg J.E., Gilbertson R.J., Sherr C.J., Roussel M.F. Genetic alterations in mouse medulloblastomas and generation of tumors de novo from primary cerebellar granule neuron precursors. Cancer Res. 2007, 67:2676-2684.
118. Zuo Y., Lubischer J.L., Kang H., Tian L., Mikesh M., Marks A., Scofield V.L., Maika S., Newman C., Krieg P., Thompson W.J. Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. J. Neurosci. 2004, 24:10999-11009.