Immunological considerations of modern animal models of malignant primary brain tumors

Journal of Translational Medicine

Volumn 7, Issue , 2009, Pages 84-

  Sughrue, Michael E ^a   Yang, Isaac ^a   Kane, Ari J ^a   Rutkowski, Martin J ^a   Fang, Shanna ^a   James, C David ^a   Parsa, Andrew T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; GENE PRODUCT; NESTIN; NITROSOUREA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN P53; TEMOZOLOMIDE; TUMOR SUPPRESSOR PROTEIN;

BRAIN TUMOR; CANCER IMMUNOTHERAPY; CYTOKINE PRODUCTION; GENE TARGETING; GLIOMA; IMMUNE DEFICIENCY; IMMUNE SYSTEM; INNATE IMMUNITY; KNOCKOUT GENE; MOUSE; NONHUMAN; PRIMARY TUMOR; PROMOTER REGION; RAT; REVIEW; RODENT; TISSUE SPECIFICITY; TUMOR IMMUNITY; TUMOR MODEL; TUMOR XENOGRAFT;

ANIMALS; BRAIN NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; GENE TARGETING; GLIOMA; HUMANS; NEOPLASM TRANSPLANTATION; PLATELET-DERIVED GROWTH FACTOR; PTEN PHOSPHOHYDROLASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 70449699924     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-7-84     Document Type: Review

References (86)

1. Stupp R, Mason WP, Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005, 352:987-996. 10.1056/NEJMoa043330, 15758009.
2. Parsa AT, Chakrabarti I, Hurley PT, Chi JH, Hall JS, Kaiser MG, Bruce JN. Limitations of the C6/Wistar rat intracerebral glioma model: implications for evaluating immunotherapy. Neurosurgery 2000, 47:993-999. discussion 999-1000, 10.1097/00006123-200010000-00050, 11014444.
3. Paek SH, Chung HT, Jeong SS, Park CK, Kim CY, Kim JE, Kim DG, Jung HW. Hearing preservation after gamma knife stereotactic radiosurgery of vestibular schwannoma. Cancer 2005, 104:580-590. 10.1002/cncr.21190, 15952200.
4. Barth RF. Rat brain tumor models in experimental neuro-oncology: the 9L, C6, T9, F98, RG2 (D74), RT-2 and CNS-1 gliomas. J Neurooncol 1998, 36:91-102. 10.1023/A:1005805203044, 9525831.
5. Delgado C, Hoa N, Callahan LL, Schiltz PM, Jahroudi RA, Zhang JG, Wepsic HT, Jadus MR. Generation of human innate immune responses towards membrane macrophage colony stimulating factor (mM-CSF) expressing U251 glioma cells within immunodeficient (NIH-nu/beige/xid) mice. Cytokine 2007, 38:165-176. 10.1016/j.cyto.2007.06.003, 17689258.
6. Kim HM, Kang JS, Lim J, Kim JY, Kim YJ, Lee SJ, Song S, Hong JT, Kim Y, Han SB. Antitumor activity of cytokine-induced killer cells in nude mouse xenograft model. Arch Pharm Res 2009, 32:781-787. 10.1007/s12272-009-1518-1, 19471894.
7. Wang P, Yu JP, Gao SY, An XM, Ren XB, Wang XG, Li WL. Experimental study on the treatment of intracerebral glioma xenograft with human cytokine-induced killer cells. Cell Immunol 2008, 253:59-65. 10.1016/j.cellimm.2008.04.014, 18522858.
8. Anderson RC, Elder JB, Brown MD, Mandigo CE, Parsa AT, Kim PD, Senatus P, Anderson DE, Bruce JN. Changes in the immunologic phenotype of human malignant glioma cells after passaging in vitro. Clinical Immunology 2002, 102:84-95. 10.1006/clim.2001.5152, 11781071.
9. Li A, Walling J, Kotliarov Y, Center A, Steed ME, Ahn SJ, Rosenblum M, Mikkelsen T, Zenklusen JC, Fine HA. 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. 10.1158/1541-7786.MCR-07-0280, 18184972.
10. Barker M, Hoshino T, Gurcay O, Wilson CB, Nielsen SL, Downie R, Eliason J. Development of an animal brain tumor model and its response to therapy with 1,3-bis(2-chloroethyl)-1-nitrosourea. Cancer Research 1973, 33:976-986.
11. Kruse CA, Lillehei KO, Mitchell DH, Kleinschmidt-DeMasters B, Bellgrau D. Analysis of interleukin 2 and various effector cell populations in adoptive immunotherapy of 9L rat gliosarcoma: allogeneic cytotoxic T lymphocytes prevent tumor take. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:9577-9581. 10.1073/pnas.87.24.9577, 55215, 2263613.
12. Kruse CA, Mitchell DH, Kleinschmidt-DeMasters BK, Bellgrau D, Eule JM, Parra JR, Kong Q, Lillehei KO. Systemic chemotherapy combined with local adoptive immunotherapy cures rats bearing 9L gliosarcoma. Journal of Neuro-Oncology 1993, 15:97-112. 10.1007/BF01053931, 8509824.
13. Kruse CA, Schiltz PM, Bellgrau D, Kong Q, Kleinschmidt-DeMasters BK. Intracranial administrations of single or multiple source allogeneic cytotoxic T lymphocytes: chronic therapy for primary brain tumors. Journal of Neuro-Oncology 1994, 19:161-168. 10.1007/BF01306458, 7964992.
14. Kruse CA, Molleston MC, Parks EP, Schiltz PM, Kleinschmidt-DeMasters BK, Hickey WF. A rat glioma model, CNS-1, with invasive characteristics similar to those of human gliomas: a comparison to 9L gliosarcoma. Journal of Neuro-Oncology 1994, 22:191-200. 10.1007/BF01052919, 7760095.
15. Kruse CA, Kong Q, Schiltz PM, Kleinschmidt-DeMasters BK. Migration of activated lymphocytes when adoptively transferred into cannulated rat brain. Journal of Neuroimmunology 1994, 55:11-21. 10.1016/0165-5728(94)90142-2, 7962481.
16. Blume M. Immune response to a transplantable intracerebral glioma in rats. Recent Progress in Neurologic Surgery 1974, 129-134. Amsterdam: Excerpta Medica, Sane K ISaLD.
17. Glick RP, Lichtor T, de Zoeten E, Deshmukh P, Cohen EP. Prolongation of survival of mice with glioma treated with semiallogeneic fibroblasts secreting interleukin-2. Neurosurgery 1999, 45:867-874. 10.1097/00006123-199910000-00028, 10515482.
18. Wu A, Oh S, Wiesner SM, Ericson K, Chen L, Hall WA, Champoux PE, Low WC, Ohlfest JR. Persistence of CD133+ cells in human and mouse glioma cell lines: detailed characterization of GL261 glioma cells with cancer stem cell-like properties. Stem Cells Dev 2008, 17:173-184. 10.1089/scd.2007.0133, 18271701.
19. Zhang M, Song T, Yang L, Chen R, Wu L, Yang Z, Fang J. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res 2008, 27:85. 10.1186/1756-9966-27-85, 2633002, 19108713.
20. Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, Hutnick L, Krueger RC, Fan G. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA 2008, 105:1026-1031. 10.1073/pnas.0710000105, 2242680, 18195354.
21. Abdouh M, Facchino S, Chatoo W, Balasingam V, Ferreira J, Bernier G. BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 2009, 29:8884-8896. 10.1523/JNEUROSCI.0968-09.2009, 19605626.
22. Reilly KM, Loisel DA, Bronson RT, McLaughlin ME, Jacks T. Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nature Genetics 2000, 26:109-113. 10.1038/79075, 10973261.
23. Wetmore C, Eberhart DE, Curran T. Loss of p53 but not ARF accelerates medulloblastoma in mice heterozygous for patched. Cancer Research 2001, 61:513-516.
24. Weiss WA, Burns MJ, Hackett C, Aldape K, Hill JR, Kuriyama H, Kuriyama N, Milshteyn N, Roberts T, Wendland MF. Genetic determinants of malignancy in a mouse model for oligodendroglioma. Cancer Research 2003, 63:1589-1595.
25. Donehower LA. The p53-deficient mouse: a model for basic and applied cancer studies. Seminars in Cancer Biology 1996, 7:269-278. 10.1006/scbi.1996.0035, 9110404.
26. Okazuka K, Wakabayashi Y, Kashihara M, Inoue J, Sato T, Yokoyama M, Aizawa S, Aizawa Y, Mishima Y, Kominami R. p53 prevents maturation of T cell development to the immature CD4-CD8+ stage in Bcl11b-/- mice. Biochemical & Biophysical Research Communications 2005, 328:545-549.
27. Sulic S, Panic L, Barkic M, Mercep M, Uzelac M, Volarevic S. Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev 2005, 19:3070-3082. 1315409, 16357222, 10.1101/gad.359305.
28. Hu L, Aizawa S, Tokuhisa T. p53 Controls Proliferation of Early B Lineage Cells by a P21 (WAF1/Cip1)-Independent Pathway. Biochemical and Biophysical Research Communications 1995, 206:948-954. 10.1006/bbrc.1995.1134, 7832809.
29. Li T, Ramirez K, Palacios R. Distinct patterns of Fas cell surface expression during development of T- or B-lymphocyte lineages in normal, scid, and mutant mice lacking or overexpressing p53, bcl-2, or rag-2 genes. Cell Growth & Differentiation 1996, 7:107-114.
30. Ohkusu-Tsukada K, Tsukada T, Isobe K. Accelerated Development and Aging of the Immune System in p53-Deficient Mice. J Immunol 1999, 163:1966-1972.
31. Zimmers TA, Jin X, Hsiao EC, McGrath SA, Esquela AF, Koniaris LG. Growth Differentiation Factor-15/Macrophage Inhibitory Cytokine-1 Induction After Kidney and Lung Injury. Shock 2005, 23:543-548.
32. Komarova EA, Krivokrysenko V, Wang K, Neznanov N, Chernov MV, Komarov PG, Brennan M-L, Golovkina TV, Rokhlin O, Kuprash DV. p53 is a suppressor of inflammatory response in mice. FASEB J 2005, 15811878.
33. Morand EF. New therapeutic target in inflammatory disease: macrophage migration inhibitory factor. Internal Medicine Journal 2005, 35:419-426. 10.1111/j.1445-5994.2005.00853.x, 15958113.
34. Hodge DR, Peng B, Cherry JC, Hurt EM, Fox SD, Kelley JA, Munroe DJ, Farrar WL. Interleukin 6 Supports the Maintenance of p53 Tumor Suppressor Gene Promoter Methylation. Cancer Res 2005, 65:4673-4682. 15930285, 10.1158/0008-5472.CAN-04-3589.
35. Porta C, Hadj-Slimane R, Nejmeddine M, Pampin M, Tovey MG, Espert L, Alvarez S, Chelbi-Alix MK. Interferons [alpha] and [gamma] induce p53-dependent and p53-independent apoptosis, respectively. 2004, 24:605-615.
36. Shin-Ya M, Hirai H, Satoh E, Kishida T, Asada H, Aoki F, Tsukamoto M, Imanishi J, Mazda O. Intracellular interferon triggers Jak/Stat signaling cascade and induces p53-dependent antiviral protection. Biochemical and Biophysical Research Communications 2005, 329:1139-1146. 10.1016/j.bbrc.2005.02.088, 15752772.
37. Gomez J, Garcia-Domingo D, Martinez AC, Rebollo A. Role of NF-kappaB in the control of apoptotic and proliferative responses in IL-2-responsive T cells. Frontiers in Bioscience 1997, 2:d49-60.
38. Maas K, Westfall M, Pietenpol J, Olsen NJ, Aune T. Reduced p53 in peripheral blood mononuclear cells from patients with rheumatoid arthritis is associated with loss of radiation-induced apoptosis. Arthritis & Rheumatism 2005, 52:1047-1057.
39. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes[see comment]. Nature 1993, 362:847-849. 10.1038/362847a0, 8479522.
40. Kuan AP, Cohen PL. p53 is required for spontaneous autoantibody production in B6/lpr lupus mice. European Journal of Immunology 2005, 35:1653-1660. 10.1002/eji.200525982, 15789337.
41. Mann-Chandler MN, Kashyap M, Wright HV, Norozian F, Barnstein BO, Gingras S, Parganas E, Ryan JJ. IFN-{gamma} Induces Apoptosis in Developing Mast Cells. J Immunol 2005, 175:3000-3005.
42. Chiu IM, Touhalisky K, Liu Y, Yates A, Frostholm A. Tumorigenesis in transgenic mice in which the SV40 T antigen is driven by the brain-specific FGF1 promoter. Oncogene 2000, 19:6229-6239. 10.1038/sj.onc.1204021, 11175337.
43. Krynska B, Otte J, Franks R, Khalili K, Croul S. Human ubiquitous JCV(CY) T-antigen gene induces brain tumors in experimental animals. Oncogene 1999, 18:39-46. 10.1038/sj.onc.1202278, 9926918.
44. Ivanchuk SM, Mondal S, Dirks PB, Rutka JT. The INK4A/ARF Locus: Role in Cell Cycle Control and Apoptosis and Implications for Glioma Growth. Journal of Neuro-Oncology 2001, 51:219-229. 10.1023/A:1010632309113, 11407594.
45. Dai C, Krantz SB. Increased expression of the INK4a/ARF locus in polycythemia vera. Blood 2001, 97:3424-3432. 10.1182/blood.V97.11.3424, 11369633.
46. Holland EC, Hively WP, DePinho RA, 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 & Development 1998, 12:3675-3685. 317252, 9851974, 10.1101/gad.12.23.3675.
47. 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 Research 2002, 62:5551-5558.
48. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, Grosveld G, Sherr CJ. Tumor Suppression at the Mouse INK4a Locus Mediated by the Alternative Reading Frame Product p19 ARF. Cell 1997, 91:649-659. 10.1016/S0092-8674(00)80452-3, 9393858.
49. Migliaccio M, Raj K, Menzel O, Rufer N. Mechanisms that limit the in vitro proliferative potential of human CD8+ T lymphocytes. Journal of Immunology 2005, 174:3335-3343.
50. Scheuring UJ, Sabzevari H, Theofilopoulos AN. Proliferative arrest and cell cycle regulation in CD8(+)CD28(-) versus CD8(+)CD28(+) T cells. Human Immunology 2002, 63:1000-1009. 10.1016/S0198-8859(02)00683-3, 12392852.
51. Wang JP, Chang LC, Hsu MF, Lin CN. The blockade of formyl peptide-induced respiratory burst by 2',5'-dihydroxy-2-furfurylchalcone involves phospholipase D signaling in neutrophils. Naunyn-Schmiedebergs Archives of Pharmacology 2003, 368:166-174.
52. Wang JP, Chang LC, Hsu MF, Chen SC, Kuo SC. Inhibition of formyl-methionyl-leucyl-phenylalanine-stimulated respiratory burst by cirsimaritin involves inhibition of phospholipase D signaling in rat neutrophils. Naunyn-Schmiedebergs Archives of Pharmacology 2002, 366:307-314.
53. Leslie NR, Downes CP. PTEN function: how normal cells control it and tumour cells lose it. Biochemical Journal 2004, 382:1-11. 1133909, 15193142, 10.1042/BJ20040825.
54. 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. 10.1016/S1535-6108(02)00029-6, 12086874.
55. Hagenbeek TJ, Naspetti M, Malergue F, Garcon F, Nunes JA, Cleutjens KB, Trapman J, Krimpenfort P, Spits H. The Loss of PTEN Allows TCR {alpha}{beta} Lineage Thymocytes to Bypass IL-7 and Pre-TCR-mediated Signaling. J Exp Med 2004, 200:883-894. 2213281, 15452180, 10.1084/jem.20040495.
56. Suzuki A, de la Pompa JL, Stambolic V, Elia AJ, Sasaki T, del Barco Barrantes I, Ho A, Wakeham A, Itie A, Khoo W. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Current Biology 1998, 8:1169-1178. 10.1016/S0960-9822(07)00488-5, 9799734.
57. Stambolic V, Tsao MS, Macpherson D, Suzuki A, Chapman WB, Mak TW. High incidence of breast and endometrial neoplasia resembling human Cowden syndrome in pten +/- mice. Cancer Research 2000, 60:3605-3611.
58. Luo J, Sobkiw CL, Logsdon NM, Watt JM, Signoretti S, O'Connell F, Shin E, Shim Y, Pao L, Neel BG. Modulation of epithelial neoplasia and lymphoid hyperplasia in PTEN +/- mice by the p85 regulatory subunits of phosphoinositide 3-kinase. PNAS 2005, 102:10238-10243. 1174923,1174923, 16006513, 10.1073/pnas.0504378102.
59. Gao P, Wange RL, Zhang N, Oppenheim JJ, Howard OMZ. Negative regulation of CXCR4-mediated chemotaxis by the lipid phosphatase activity of tumor suppressor PTEN. Blood 2005, 106:2619-2626. 1895312, 15994292, 10.1182/blood-2004-08-3362.
60. Lacalle RA, Gomez-Mouton C, Barber DF, Jimenez-Baranda S, Mira E, Martinez AC, Carrera AC, Manes S. PTEN regulates motility but not directionality during leukocyte chemotaxis. Journal of Cell Science 2004, 117:6207-6215. 10.1242/jcs.01545, 15564381.
61. Libermann TA, Nusbaum HR, Razon N, Kris R, Lax I, Soreq H, Whittle N, Waterfield MD, Ullrich A, Schlessinger J. Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin. Nature 1985, 313:144-147. 10.1038/313144a0, 2981413.
62. Reifenberger J, Reifenberger G, Ichimura K, Schmidt EE, Wechsler W, Collins VP. Epidermal growth factor receptor expression in oligodendroglial tumors. American Journal of Pathology 1996, 149:29-35. 1865223, 8686753.
63. Yan S-F, Fujita T, Lu J, Okada K, Shan Zou Y, Mackman N, Pinsky DJ, Stern DM. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. 2000, 6:1355-1361.
64. Lewkowicz P, Tchorzewski H, Dytnerska K, Banasik M, Lewkowicz N. Epidermal growth factor enhances TNF-alpha-induced priming of human neutrophils. Immunology Letters 2005, 96:203-210. 10.1016/j.imlet.2004.08.012, 15585324.
65. Lamb DJ, Modjtahedi H, Plant NJ, Ferns GA. EGF mediates monocyte chemotaxis and macrophage proliferation and EGF receptor is expressed in atherosclerotic plaques. Atherosclerosis 2004, 176:21-26. 10.1016/j.atherosclerosis.2004.04.012, 15306170.
66. Watanabe S, Yoshimura A, Inui K, Yokota N, Liu Y, Sugenoya Y, Morita H, Ideura T. Acquisition of the monocyte/macrophage phenotype in human mesangial cells. Journal of Laboratory & Clinical Medicine 2001, 138:193-199.
67. Hamilton LM, Torres-Lozano C, Puddicombe SM, Richter A, Kimber I, Dearman RJ, Vrugt B, Aalbers R, Holgate ST, Djukanovic R. The role of the epidermal growth factor receptor in sustaining neutrophil inflammation in severe asthma. Clinical & Experimental Allergy 2003, 33:233-240.
68. Kim JH, Jung KH, Han JH, Shim JJ, In KH, Kang KH, Yoo SH. Relation of epidermal growth factor receptor expression to mucus hypersecretion in diffuse panbronchiolitis. Chest 2004, 126:888-895. 10.1378/chest.126.3.888, 15364771.
69. Mascia F, Mariani V, Girolomoni G, Pastore S. Blockade of the EGF receptor induces a deranged chemokine expression in keratinocytes leading to enhanced skin inflammation. American Journal of Pathology 2003, 163:303-312. 1868171, 12819035.
70. Nelin LD, Chicoine LG, Reber KM, English BK, Young TL, Liu Y. Cytokine-induced endothelial arginase expression is dependent on epidermal growth factor receptor. American Journal of Respiratory Cell & Molecular Biology 2005, 33:394-401.
71. Ding H, Shannon P, Lau N, Wu X, Roncari L, Baldwin RL, Takebayashi H, Nagy A, Gutmann DH, Guha A. Oligodendrogliomas result from the expression of an activated mutant epidermal growth factor receptor in a RAS transgenic mouse astrocytoma model. Cancer Research 2003, 63:1106-1113.
72. Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin C, Westermark B, Nister M. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 1992, 52:3213-3219.
73. Hesselager G, Uhrbom L, Westermark B, Nister M. Complementary Effects of Platelet-derived Growth Factor Autocrine Stimulation and p53 or Ink4a-Arf Deletion in a Mouse Glioma Model. Cancer Res 2003, 63:4305-4309.
74. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 2001, 15:1913-1925. 312748, 11485986, 10.1101/gad.903001.
75. Wei Q, Clarke L, Scheidenhelm DK, Qian B, Tong A, Sabha N, Karim Z, Bock NA, Reti R, Swoboda R. 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. 10.1158/0008-5472.CAN-06-0712, 16885338.
76. Kwon CH, Zhao D, Chen J, Alcantara S, Li Y, Burns DK, Mason RP, Lee EY, Wu H, Parada LF. Pten haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res 2008, 68:3286-3294. 2760841, 18451155, 10.1158/0008-5472.CAN-07-6867.
77. Schuller U, Heine VM, Mao J, Kho AT, Dillon AK, Han YG, Huillard E, Sun T, Ligon AH, Qian Y. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008, 14:123-134. 2597270, 18691547, 10.1016/j.ccr.2008.07.005.
78. 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. 1501155, 15967113, 10.1593/neo.04595.
79. Yan CT, Kaushal D, Murphy M, Zhang Y, Datta A, Chen C, Monroe B, Mostoslavsky G, Coakley K, Gao Y. XRCC4 suppresses medulloblastomas with recurrent translocations in p53-deficient mice. Proc Natl Acad Sci USA 2006, 103:7378-7383. 1464348, 16670198, 10.1073/pnas.0601938103.
80. Xiao A, Yin C, Yang C, Di Cristofano A, Pandolfi PP, 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. 10.1158/0008-5472.CAN-04-3902, 15958561.
81. Yang ZJ, Ellis T, Markant SL, Read TA, Kessler JD, Bourboulas M, Schuller U, Machold R, Fishell G, Rowitch DH. Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 2008, 14:135-145. 2538687, 18691548, 10.1016/j.ccr.2008.07.003.
82. Marino S, Vooijs M, 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. 316543, 10783170.
83. Frappart PO, Lee Y, Lamont J, McKinnon PJ. BRCA2 is required for neurogenesis and suppression of medulloblastoma. EMBO J 2007, 26:2732-2742. 1888666, 17476307, 10.1038/sj.emboj.7601703.
84. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, Perry SR, Tonon G, Chu GC, Ding Z. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455:1129-1133. 10.1038/nature07443, 18948956.
85. Huse JT, Holland EC. Genetically engineered mouse models of brain cancer and the promise of preclinical testing. Brain Pathol 2009, 19:132-143. 2659383, 19076778, 10.1111/j.1750-3639.2008.00234.x.
86. Rao G, Pedone CA, Coffin CM, Holland EC, Fults DW. c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice. Neoplasia 2003, 5:198-204. 1502413, 12869303.