Mouse models of glioma pathogenesis: History and state of the art

Emerging Concepts in Neuro-Oncology

Volumn 9780857294586, Issue , 2013, Pages 87-107

  Brandner, Sebastian ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Brain tumor; Chemical carcinogenesis; Conditional gene inactivation; cre recombinase; Ethylnitrosourea; Gene knockout; Glioblastoma; Glioma; INK4a ARF locus; loxP site; Oligodendroglioma; p53 tumor suppressor gene; Point mutations; PTEN tumor suppressor gene; Retinoblastoma gene; Rous sarcoma virus; SV40; Transgenic mouse; Viral carcinogenesis

Indexed keywords

EID: 84884765875     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-85729-458-6_6     Document Type: Chapter

References (100)

1. Wechsler W, Kleihues P, Matsumot S., Zulch KJ, Ivankovi S, Preussma R. Pathology of experimental neurogenic tumors chemically induced during prenatal and postnatal life. Ann N Y Acad Sci. 1969; 159(A2):360.
2. Swenberg JA. Neoplasms of the nervous system. In: Foster H, Small J, JG F, editors. The mouse in biomedical research. New York: Academic; 1982. p. 529-37.
3. Fraser H, Mcconnell I. Experimental brain tumors. Lancet. 1975; 1(7897):44.
4. Hayes C, Kelly D, Murayama S., Komiyama A, Suzuki K, Popko B. Expression of the neu oncogene under the transcriptional control of the myelin basic-protein gene in transgenic mice - generation of transformed glial-cells. J Neurosci Res. 1992; 31(1):175-87.
5. Eibl RH, Kleihues P, Jat P.S., Wiestler OD. A model for primitive neuroectodermal tumors in transgenic neural transplants harboring the SV40 large T antigen. Am J Pathol. 1994; 144(3):556-64.
6. Cooper JA, Gould KL, Cartwright C.A., Hunter T. Tyr527 is phosphorylated in Pp60c-Src - implications for regulation. Science. 1986; 231(4744):1431-4.
7. Brugge J, Cotton P, Lustig A., Yonemoto W, Lipsich L, Coussens P., et al. Characterization of the altered form of the C-Src gene-product in neuronal cells. Genes Dev. 1987; 1(3):287-96.
8. Greenhouse JJ, Petropoulos CJ, Crittenden L.B., Hughes SH. Helper-independent retrovirus vectors with Rous-associated virus type-O long terminal repeats. J Virol. 1988; 62(12):4809-12.
9. Hughes SH, Greenhouse JJ, Petropoulos C.J., Sutrave P. Adapter plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J Virol. 1987; 61(10):3004-12.
10. Zhu Y, Guignard F, Zhao D., Liu L, Burns DK, Mason R.P., et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell. 2005; 8(2):119-30.
11. Abremski K, Hoess R. Bacteriophage P1 site-specific recombination. Purification and properties of the cre recombinase protein. J Biol Chem. 1984; 259(3): 1509-14.
12. Sternberg N, Hamilton D. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J Mol Biol. 1981; 150(4):467-86.
13. Sternberg N, Hamilton D, Hoess R. Bacteriophage P1 site-specific recombination. II. Recombination between loxP and the bacterial chromosome. J Mol Biol. 1981; 150(4):487-507.
14. Kuhn R, Schwenk F, Aguet M., Rajewsky K. Inducible gene targeting in mice. Science. 1995; 269(5229): 1427-9.
15. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumour suppression. Nat Genet. 1998; 19(4):348-55.
16. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, et al. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell. 1998; 95(1):29-39.
17. Li J, Yen C, Liaw D., Podsypanina K, Bose S, Wang S.I., et al. PTEN, a putative protein tyrosine phos-phatase gene mutated in human brain, breast, and prostate cancer. Science. 1997; 275(5308):1943-7.
18. Su LK, Kinzler KW, Vogelstein B, Preisinger A.C., Moser AR, Luongo C, et al. Multiple intestinal neo-plasia caused by a mutation in the murine homolog of the Apc gene. Science. 1992; 256(5057):668-70.
19. Ashton-Rickardt PG, Dunlop MG, Nakamura Y, Morris R.G., Purdie CA, Steel CM, et al. High frequency of APC loss in sporadic colorectal carcinoma due to breaks clustered in 5q21-22. Oncogene. 1989; 4(10):1169-74.
20. Ichii S, Horii A, Nakatsuru S., Furuyama J, Utsunomiya J, Nakamura Y. Inactivation of both APC alleles in an early stage of colon adenomas in a patient with familial adenomatous polyposis (FAP). Hum Mol Genet. 1992; 1(6):387-90.
21. 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(23):3644-9.
22. Holland EC, Hively WP, DePinho R.A., Varmus HE. 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(23):3675-85.
23. Bates S, Phillips AC, Clark P.A., Stott F., Peters G, Ludwig RL, et al. p14ARF links the tumour suppressors RB and p53 [letter]. Nature. 1998; 395(6698): 124-5.
24. Palmero I, Pantoja C, Serrano M. p19ARF links the tumour suppressor p53 to Ras. Nature. 1998; 395(6698):125-6.
25. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific-inhibition of cyclin-D/Cdk4. Nature. 1993; 366(6456):704-7.
26. von Deimling A, von Ammon K, Schoenfeld D, Wiestler O.D., Seizinger BR, Louis DN. Subsets of glioblastoma multiforme defined by molecular genetic analysis. Brain Pathol. 1993; 3(1):19-26.
27. Watanabe K, Tachibana O, Sata K., Yonekawa Y, Kleihues P, Ohgaki H. Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblasto-mas. Brain Pathol. 1996; 6(3):217-23. discussion 23-4
28. Rabotti GF, Raine WA, Sellers RL. Brain tumors (gliomas) induced in hamsters by Bryans strain of Rous sarcoma virus. Science. 1965; 147(3657):505.
29. Mennel HD. Significance of experimental models in neurooncology. Neurosurg Rev. 1980; 3(2):129-37.
30. Malkin D, Li FP, Strong L.C., Fraumeni Jr JF, Nelson CE, Kim DH, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms [see comments]. Science. 1990; 250(4985):1233-8.
31. Ohgaki H, Eibl RH, Schwab M, Reichel M.B., Mariani L., Gehring M, et al. Mutations of the p53 tumor suppressor gene in neoplasms of the human nervous system. Mol Carcinog. 1993; 8(2):74-80.
32. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell. 1997; 88(3):323-31.
33. Jacks T, Fazeli A, Schmitt E.M., Bronson RT, Goodell MA, Weinberg RA. Effects of an Rb mutation in the mouse. Nature. 1992; 359(6393):295-300.
34. Murphree AL, Benedict WF. Retinoblastoma: clues to human oncogenesis. Science. 1984; 223(4640): 1028-33.
35. Alvarez Buylla A, Lois C. Neuronal stem cells in the brain of adult vertebrates. Stem Cells. 1995; 13(3):263-72.
36. Doetsch F, Caille I, Lim D.A., Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999; 97(6):703-16.
37. Jacques TS, Swales A, Brzozowski M.J., Henriquez NV, Linehan JM, Mirzadeh Z, et al. Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J. 2010; 29(1):222-35.
38. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M., Quinones-Hinojosa A, VandenBerg S, et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron. 2006; 51(2):187-99.
39. Peers JH. The response of the central nervous system to the application of carcinogenic hydrocarbons: I. Dibenzanthracene. Am J Pathol. 1939; 15(2): 261-272.3.
40. Peers JH. The response of the central nervous system to the application of carcinogenic hydrocarbons: II. Methylcholanthrene. Am J Pathol. 1940; 16(6): 799-816.5.
41. Seligman AM, Shear M. Studies in carcinogenesis. VIII. Experimental production of brain tumors in mice with methylcholanthrene. Am J Cancer. 1939; 37:364-95.
42. Zimmerman HM, Arnold H. Experimental brain tumors: II. Tumors produced with benzpyrene. Am J Pathol. 1943; 19(6):939-55.
43. Zimmerman HM, Arnold H. Experimental brain tumors. I. Tumors produced with methylcholanthrene. Cancer Res. 1941; 1(12):919.
44. Magee PN, Barnes JM. The production of malignant primary hepatic tumours in the rat by feeding dimeth-ylnitrosamine. Br J Cancer. 1956; 10(1):114.
45. Mennel HD, Zulch KJ. Formal pathogenesis of experimentally induced brain tumors. Acta Neuropathol. 1972; 21(2):140-53.
46. Mukai N, Kobayash S, Oguri M. Ultrastructuralfindings in medulloepitheliomatous neoplasms induced by human adenovirus 12 in rodents. Acta Neuropathol. 1974; 28(4):293-304.
47. Kumanish T, Ikuta F, Yamamoto T. Brain tumors induced by Rous-sarcoma virus, Schmidt-Ruppin strain. 3. Morphology of brain tumors induced in adult mice. J Natl Cancer Inst. 1973; 50(1):95-109.
48. Jänisch W, Schreiber D. In: Bigner DD, Swenberg JA, editors. Methods of inducing experimental nervous system tumors: Simian sarcoma virus. Experimental tumors of the central nervous system. Kalamazoo, Michigan: Upjohn Company; 1977. p. 36.
49. Rabotti GF, Anderson WR, Sellers RL. Oncogenic activity of Mill Hill (Harris) strain of Rous sarcoma virus for hamsters. Nature. 1965; 206(4987):946.
50. Brinster RL, Chen HY, Messing A, Vandyke T., Levine AJ, Palmiter RD. Transgenic mice harboring Sv40 T-antigen genes develop characteristic brain-tumors. Cell. 1984; 37(2):367-79.
51. Palmiter RD, Chen HY, Messing A, Brinster RL. Sv40 Enhancer and large-T antigen are instrumental in development of choroid-plexus tumors in transgenic mice. Nature. 1985; 316(6027):457-60.
52. 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(17):2005-13.
53. Maddalena AS, Hainfellner JA, Hegi M.E., Glatzel M., Aguzzi A. No complementation between TP53 or RB-1 and v-src in astrocytomas of GFAP-v-src trans-genic mice. Brain Pathol. 1999; 9(4):627-37.
54. 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(1):55-7.
55. Uhrbom L, Kastemar M, Johansson F.K., Westermark B., Holland EC. Cell type-specific tumor suppression by Ink4a and Arf in Kras-induced mouse gliomagenesis. Cancer Res. 2005; 65(6):2065-9.
56. Robinson JP, Vanbrocklin MW, Lastwika K.J., McKinney AJ, Brandner S, Holmen SL. Activated MEK cooperates with Ink4a/Arf loss or Akt activation to induce gliomas in vivo. Oncogene. 2011; 30(11):1341-50.
57. Holmen SL, Williams BO. Essential role for Ras signaling in glioblastoma maintenance. Cancer Res. 2005; 65(18):8250-5.
58. Robinson JP, VanBrocklin MW, Guilbeault A.R., Signorelli DL, Brandner S, Holmen SL. Activated BRAF induces gliomas in mice when combined with Ink4a/Arf loss or Akt activation. Oncogene. 2010; 29(3):335-44.
59. Reilly KM, Loisel DA, Bronson R.T., McLaughlin ME, Jacks T. Nf1; Trp53 mutant mice develop glioblas-toma with evidence of strain-specific effects. Nat Genet. 2000; 26(1):109-13.
60. Xiao A, Wu H, Pandolfi P.P., 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(2):157-68.
61. Xiao A, Yin C, Yang C., Di Cristofano A, Pandolfi PP, Van Dyke T. Somatic induction of Pten loss in a pre-clinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res. 2005; 65(12):5172-80.
62. 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(7216):1129-33.
63. Kwon CH, Zhao D, Chen J., Alcantara S, Li Y, Burns D.K., et al. Pten haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res. 2008; 68(9):3286-94.
64. Alcantara Llaguno S, Chen J, Kwon C.H., Jackson EL, Li Y, Burns DK. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell. 2009; 15(1):45-56.
65. Chow LM, Endersby R, Zhu X., Rankin S, Qu C, Zhang J., et al. Cooperativity within and among Pten, p53, and Rb pathways induces high-grade astrocy-toma in adult brain. Cancer Cell. 2011; 19(3):305-16.
66. Boorman GA. Brain-tumors in Man and animals - report of a workshop. Environ Health Perspect. 1986; 68:155-73.
67. Fuller C, Helton K, Dalton J., Fouladi M, Kun L, Burger P. Polar spongioblastoma of the spinal cord: a case report. Pediatr Dev Pathol. 2006; 9(1):75-80.
68. Brodie BB, Gillette JR, Ladu BN. Enzymatic metabolism of drugs and other foreign compounds. Annu Rev Biochem. 1958; 27:427-54.
69. Druckrey H, Preussmann R, Ivankovic S., Schmahl D. Organotropic carcinogenic effects of 65 various N-nitroso-compounds on BD rats. Z Krebsforsch. 1967; 69(2):103-201.
70. Zimmerman HM. Brain tumors - their incidence and classification in man and their experimental production. Ann N Y Acad Sci. 1969; 159(A2):337.
71. Trentin JJ, Yabe Y, Taylor G. The quest for human cancer viruses. Science. 1962; 137(3533):835-41.
72. Huebner RJ, Rowe WP, Lane WT. Oncogenic effects in hamsters of human adenovirus types 12 and 18. Proc Natl Acad Sci U S A. 1962; 48(12):2051.
73. Rabotti GF, Grove AS, Sellers R.L., Anderson WR. Induction of multiple brain tumours (gliomata and leptomeningeal sarcomata) in dogs by Rous sarcoma virus. Nature. 1966; 209(5026):884.
74. Rabotti GF, Sellers RL, Anderson WA. Leptomeningeal sarcomata and gliomata induced in rabbits by Rous sarcoma virus. Nature. 1966; 209(5022):524.
75. Jaenisch R, Mintz B. Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preim-plantation blastocysts injected with viral DNA. Proc Natl Acad Sci U S A. 1974; 71(4):1250-4.
76. Green MR. When the products of oncogenes and anti-oncogenes meet. Cell. 1989; 56(1):1-3.
77. Peden KWC, Srinivasan A, Farber J.M., Pipas JM. Mutants with changes within or near a hydrophobic region of simian virus-40 large tumor-antigen are defective for binding cellular protein-P53. Virology. 1989; 168(1):13-21.
78. Decaprio JA, Ludlow JW, Figge J, Shew J.Y., Huang CM, Lee WH, et al. Sv40 Large tumor-antigen forms a specific complex with the product of the retinoblas-toma susceptibility gene. Cell. 1988; 54(2):275-83.
79. Ewen ME, Ludlow JW, Marsilio E, Decaprio J.A., Millikan RC, Cheng SH, et al. An N-terminal transformation-governing sequence of Sv40 large T-antigen contributes to the binding of both P110rb and a 2nd cellular protein, P120. Cell. 1989; 58(2):257-67.
80. Symonds H, Krall L, Remington L., Saenzrobles M, Lowe S, Jacks T., et al. P53-Dependent apoptosis suppresses tumor-growth and progression in-vivo. Cell. 1994; 78(4):703-11.
81. Gotz W, Theuring F, Schachenmayr W., Korf HW. Midline brain-tumors in Msv-Sv 40-transgenic mice originate from the pineal organ. Acta Neuropathol. 1992; 83(3):308-14.
82. Danks RA, Orian JM, Gonzales M.F., Tan SS, Alexander B, Mikoshiba K, et al. Transformation of astrocytes in transgenic mice expressing Sv40 T-antigen under the transcriptional control of the glialfibrillary acidic protein promoter. Cancer Res. 1995; 55(19):4302-10.
83. Theurillat JP, Hainfellner J, Maddalena A., Weissenberger J, Aguzzi A. Early induction of angio-genetic signals in gliomas of GFAP-v-src transgenic mice. Am J Pathol. 1999; 154(2):581-90.
84. Holland EC, Varmus HE. 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(3):1218-23.
85. Schindler G, Capper D, Meyer J., Janzarik W, Omran H, Herold-Mende C. Analysis of BRAF V600E mutation in 1,320 nervous system tumors reveals high mutation frequencies in pleomorphic xanthoastrocytoma, ganglioglioma and extra-cerebellar pilocytic astrocy-toma. Acta Neuropathol. 2011; 121(3):397-405.
86. Moser AR, Shoemaker AR, Connelly C.S., Clipson L., Gould KA, Luongo C, et al. Homozygosity for the Min allele of Apc results in disruption of mouse development prior to gastrulation. Dev Dyn. 1995; 203(4):422-33.
87. Oshima M, Oshima H, Kitagawa K., Kobayashi M, Itakura C, Taketo M. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc Natl Acad Sci U S A. 1995; 92(10):4482-6.
88. Fodde R, Edelmann W, Yang K., Vanleeuwen C, Carlson C, Renault B., et al. A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc Natl Acad Sci U S A. 1994; 91(19):8969-73.
89. Suzuki A, de la Pompa JL, Stambolic V, Elia AJ, Sasaki T, Barrantes ID, et al. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr Biol. 1998; 8(21):1169-78.
90. Gu H, Zou YR, Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-IoxP-mediated gene targeting. Cell. 1993; 73(6):1155-64.
91. Gu H, Marth JD, Orban P.C., Mossmann H., Rajewsky K. Deletion of a DNA-polymerase-beta gene segment in T-cells using cell-type-specific gene targeting. Science. 1994; 265(5168):103-6.
92. 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(4):404-11.
93. 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(4):396-403.
94. Groszer M, Erickson R, Scripture-Adams D, Lesche R., Trumpp A, Zack JA. Negative regulation of neural stem/progenitor cell proliferation by the pten tumor suppressor gene in vivo. Science. 2001; 294(5549):2186-9.
95. Marino S, Krimpenfort P, Leung C., van der Korput HA, Trapman J, Camenisch I, et al. PTEN is essential for cell migration but not for fate determination and tumourigenesis in the cerebellum. Development. 2002; 129(14):3513-22.
96. Anton M, Graham FL. Site-specific recombination mediated by an adenovirus vector expressing the cre recombinase protein: a molecular switch for control of gene expression. J Virol. 1995; 69(8): 4600-6.
97. Kaspar BK, Vissel B, Bengoechea T., Crone S, Randolph-Moore L, Muller R, et al. Adeno-associated virus effectively mediates conditional gene modification in the brain. Proc Natl Acad Sci U S A. 2002; 99(4):2320-5.
98. Ahmed BY, Chakravarthy S, Eggers R., Hermens WT, Zhang JY, Niclou SP, et al. Efficient delivery of Cre-recombinase to neurons in vivo and stable trans-duction of neurons using adeno-associated and lenti-viral vectors. BMC Neurosci. 2004; 5:4.
99. Wang H, Xie H, Zhang H., Das SK, Dey SK. Conditional gene recombination by adenovirus-driven Cre in the mouse uterus. Genesis. 2006; 44(2):51-6.
100. Mori T, Tanaka K, Buffo A., Wurst W, Kuhn R, Gotz M. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. Glia. 2006; 54(1):21-34.