Cerebellar granule cells: Insights into proliferation, differentiation, and role in medulloblastoma pathogenesis

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 3, 2009, Pages 435-445

  Behesti, Hourinaz ^a   Marino, Silvia ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cell; Differentiation; Granule; Medulloblastoma; Proliferation

Indexed keywords

CYCLIN D1; PROTEIN P53; RETINOBLASTOMA PROTEIN;

BRAIN DEVELOPMENT; CELL CYCLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CEREBELLUM; EMBRYO DEVELOPMENT; GENE EXPRESSION; GRANULE CELL; HUMAN; MEDULLOBLASTOMA; MITOGENESIS; NONHUMAN; PATHOGENESIS; REGULATORY MECHANISM; SHORT SURVEY; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CEREBELLAR NEOPLASMS; CEREBELLUM; CYTOPLASMIC GRANULES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MEDULLOBLASTOMA; MICE; NEURONS; RATS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 58149301313     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2008.06.017     Document Type: Short Survey

References (139)

1. Ahn S., and Joyner A.L. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437 (2005) 894-897
2. Ajioka I., Martins R.A., Bayazitov I.T., Donovan S., Johnson D.A., Frase S., et al. Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131 (2007) 378-390
3. Alcaraz W.A., Gold D.A., Raponi E., Gent P.M., Concepcion D., and Hamilton B.A. Zfp423 controls proliferation and differentiation of neural precursors in cerebellar vermis formation. Proc Natl Acad Sci USA 103 (2006) 19424-19429
4. Alder J., Lee K.J., Jessell T.M., and Hatten M.E. Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nat Neurosci 2 (1999) 535-540
5. Aldosari N., Bigner S.H., Burger P.C., Becker L., Kepner J.L., Friedman H.S., et al. MYCC and MYCN oncogene amplification in medulloblastoma. A fluorescence in situ hybridization study on paraffin sections from the Children's Oncology Group. Arch Pathol Lab Med 126 (2002) 540-544
6. Altman J., and Bayer S.A. Development of the cerebellar system: in relation to its evolution, structure, and function (1997), CRC Press, Inc.
7. Angley C., Kumar M., Dinsio K.J., Hall A.K., and Siegel R.E. Signaling by bone morphogenetic proteins and Smad1 modulates the postnatal differentiation of cerebellar cells. J Neurosci 23 (2003) 260-268
8. Argenti B., Gallo R., Di Marcotullio L., Ferretti E., Napolitano M., Canterini S., et al. Hedgehog antagonist REN(KCTD11) regulates proliferation and apoptosis of developing granule cell progenitors. J Neurosci 25 (2005) 8338-8346
9. Aruga J., Inoue T., Hoshino J., and Mikoshiba K. Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22 (2002) 218-225
10. Aruga J., Minowa O., Yaginuma H., Kuno J., Nagai T., Noda T., et al. Mouse Zic1 is involved in cerebellar development. J Neurosci 18 (1998) 284-293
11. Badiali M., Pession A., Basso G., Andreini L., Rigobello L., Galassi E., et al. N-myc and c-myc oncogenes amplification in medulloblastomas. Evidence of particularly aggressive behavior of a tumor with c-myc amplification. Tumori 77 (1991) 118-121
12. Bansal R., Lakhina V., Remedios R., and Tole S. Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with Pdgfralpha, Olig2 and Plp/dm20: implications for oligodendrocyte development. Dev Neurosci 25 (2003) 83-95
13. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., et al. Math1 is essential for genesis of cerebellar granule neurons. Nature 390 (1997) 169-172
14. Bernards R., Shackleford G.M., Gerber M.R., Horowitz J.M., Friend S.H., Schartl M., et al. Structure and expression of the murine retinoblastoma gene and characterization of its encoded protein. Proc Natl Acad Sci USA 86 (1989) 6474-6478
15. Briscoe J., and Novitch B.G. Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos Trans R Soc Lond B Biol Sci 363 (2008) 57-70
16. Brown H.G., Kepner J.L., Perlman E.J., Friedman H.S., Strother D.R., Duffner P.K., et al. Large cell/anaplastic medulloblastomas: a Pediatric Oncology Group Study. J Neuropathol Exp Neurol 59 10 (2000) 857-865
17. Bruggeman S.W., Valk-Lingbeek M.E., van der Stoop P.P., Jacobs J.J., Kieboom K., Tanger E., et al. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev 19 (2005) 1438-1443
18. Cai C.L., Zhou W., Yang L., Bu L., Qyang Y., Zhang X., et al. T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development 132 (2005) 2475-2487
19. Chidambaram A., Goldstein A.M., Gailani M.R., Gerrard B., Bale S.J., DiGiovanna J.J., et al. Mutations in the human homologue of the Drosophila patched gene in Caucasian and African-American nevoid basal cell carcinoma syndrome patients. Cancer Res 56 (1996) 4599-4601
20. Chizhikov V.V., Lindgren A.G., Currle D.S., Rose M.F., Monuki E.S., and Millen K.J. The roof plate regulates cerebellar cell-type specification and proliferation. Development 133 (2006) 2793-2804
21. Choi Y., Borghesani P.R., Chan J.A., and Segal R.A. Migration from a mitogenic niche promotes cell-cycle exit. J Neurosci 25 (2005) 10437-10445
22. Ciemerych M.A., Kenney A.M., Sicinska E., Kalaszczynska I., Bronson R.T., Rowitch D.H., et al. Development of mice expressing a single D-type cyclin. Genes Dev 16 (2002) 3277-3289
23. Clarke A.R., Maandag E.R., van Roon M., van der Lugt N.M., van der Valk M., Hooper M.L., et al. Requirement for a functional Rb-1 gene in murine development. Nature 359 (1992) 328-330
24. Cobrinik D., Lee M.H., Hannon G., Mulligan G., Bronson R.T., Dyson N., et al. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 10 (1996) 1633-1644
25. Corrales J.D., Blaess S., Mahoney E.M., and Joyner A.L. The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133 (2006) 1811-1821
26. Corrales J.D., Rocco G.L., Blaess S., Guo Q., and Joyner A.L. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131 (2004) 5581-5590
27. Cui H., Meng Y., and Bulleit R.F. Inhibition of glycogen synthase kinase 3beta activity regulates proliferation of cultured cerebellar granule cells. Brain Res Dev Brain Res 111 (1998) 177-188
28. Dahmane N., and Ruiz i Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126 (1999) 3089-3100
29. Dakubo G.D., Mazerolle C.J., and Wallace V.A. Expression of Notch and Wnt pathway components and activation of Notch signaling in medulloblastomas from heterozygous patched mice. J Neurooncol 79 (2006) 221-227
30. Deng C., Zhang P., Harper J.W., Elledge S.J., and Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82 (1995) 675-684
31. Di Marcotullio L., Ferretti E., De Smaele E., Argenti B., Mincione C., Zazzeroni F., et al. REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc Natl Acad Sci USA 101 (2004) 10833-10838
32. Donehower L.A., Harvey M., Slagle B.L., McArthur M.J., Montgomery Jr. C.A., Butel J.S., et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356 (1992) 215-221
33. Duplan S.M., Theoret Y., and Kenigsberg R.L. Antitumor activity of fibroblast growth factors (FGFs) for medulloblastoma may correlate with FGF receptor expression and tumor variant. Clin Cancer Res 8 (2002) 246-257
34. Eberhart C.G., Tihan T., and Burger P.C. Nuclear localization and mutation of beta-catenin in medulloblastomas. J Neuropathol Exp Neurol 59 (2000) 333-337
35. Fogarty M.P., Emmenegger B.A., Grasfeder L.L., Oliver T.G., and Wechsler-Reya R.J. Fibroblast growth factor blocks Sonic hedgehog signaling in neuronal precursors and tumor cells. Proc Natl Acad Sci USA 104 (2007) 2973-2978
36. Fogarty M.P., Kessler J.D., and Wechsler-Reya R.J. Morphing into cancer: the role of developmental signaling pathways in brain tumor formation. J Neurobiol 64 (2005) 458-475
37. Friedel R.H., Kerjan G., Rayburn H., Schuller U., Sotelo C., Tessier-Lavigne M., et al. Plexin-B2 controls the development of cerebellar granule cells. J Neurosci 27 (2007) 3921-3932
38. Gailani M.R., Stahle-Backdahl M., Leffell D.J., Glynn M., Zaphiropoulos P.G., Pressman C., et al. The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas. Nat Genet 14 (1996) 78-81
39. Gazit R., Krizhanovsky V., and Ben-Arie N. Math1 controls cerebellar granule cell differentiation by regulating multiple components of the Notch signaling pathway. Development 131 (2004) 903-913
40. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., and Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 10 (1996) 301-312
41. Goodrich L.V., Milenkovic L., Higgins K.M., and Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 (1997) 1109-1113
42. Gorlin R.J. Nevoid basal-cell carcinoma syndrome. Medicine (Baltimore) 66 (1987) 98-113
43. Hahn H., Wicking C., Zaphiropoulous P.G., Gailani M.R., Shanley S., Chidambaram A., et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85 (1996) 841-851
44. Hahn H., Wojnowski L., Specht K., Kappler R., Calzada-Wack J., Potter D., et al. Patched target Igf2 is indispensable for the formation of medulloblastoma and rhabdomyosarcoma. J Biol Chem 275 (2000) 28341-28344
45. Hallahan A.R., Pritchard J.I., Hansen S., Benson M., Stoeck J., Hatton B.A., et al. The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer Res 64 (2004) 7794-7800
46. Hartmann W., Koch A., Brune H., Waha A., Schuller U., Dani I., et al. Insulin-like growth factor II is involved in the proliferation control of medulloblastoma and its cerebellar precursor cells. Am J Pathol 166 (2005) 1153-1162
47. Hatten M.E., Alder J., Zimmerman K., and Heintz N. Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7 (1997) 40-47
48. Hatten M.E., Lynch M., Rydel R.E., Sanchez J., Joseph-Silverstein J., Moscatelli D., et al. In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol 125 (1988) 280-289
49. Hatton B.A., Knoepfler P.S., Kenney A.M., Rowitch D.H., de Alboran I.M., Olson J.M., et al. N-myc is an essential downstream effector of Shh signaling during both normal and neoplastic cerebellar growth. Cancer Res 66 (2006) 8655-8661
50. Hattori Y., Miyake A., Mikami T., Ohta M., and Itoh N. Transient expression of FGF-5 mRNA in the rat cerebellar cortex during post-natal development. Brain Res Mol Brain Res 47 (1997) 262-266
51. Helms A.W., Gowan K., Abney A., Savage T., and Johnson J.E. Overexpression of MATH1 disrupts the coordination of neural differentiation in cerebellum development. Mol Cell Neurosci 17 (2001) 671-682
52. Huang H., Mahler-Araujo B.M., Sankila A., Chimelli L., Yonekawa Y., Kleihues P., et al. APC mutations in sporadic medulloblastomas. Am J Pathol 156 (2000) 433-437
53. Huard J.M., Forster C.C., Carter M.L., Sicinski P., and Ross M.E. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126 (1999) 1927-1935
54. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15 (2001) 3059-3087
55. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., and Weinberg R.A. Effects of an Rb mutation in the mouse. Nature 359 (1992) 295-300
56. Jacks T., Remington L., Williams B.O., Schmitt E.M., Halachmi S., Bronson R.T., et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol 4 (1994) 1-7
57. Jiang Z., Zacksenhaus E., Gallie B.L., and Phillips R.A. The retinoblastoma gene family is differentially expressed during embryogenesis. Oncogene 14 (1997) 1789-1797
58. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., et al. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272 (1996) 1668-1671
59. Kadin M.E., Rubinstein L.J., and Nelson J.S. Neonatal cerebellar medulloblastoma originating from the fetal external granular layer. J Neuropathol Exp Neurol 29 (1970) 583-600
60. Kamijo T., Zindy F., Roussel M.F., Quelle D.E., Downing J.R., Ashmun R.A., et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91 (1997) 649-659
61. Katsetos C.D., and Burger P.C. Medulloblastoma. Semin Diagn Pathol 11 (1994) 85-97
62. Kenigsberg R.L., Hong Y., Yao H., Lemieux N., Michaud J., Tautu C., et al. Effects of basic fibroblast growth factor on the differentiation, growth, and viability of a new human medulloblastoma cell line (UM-MB1). Am J Pathol 151 (1997) 867-881
63. Kenney A.M., Cole M.D., and Rowitch D.H. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130 (2003) 15-28
64. Knoepfler P.S., Cheng P.F., and Eisenman R.N. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 16 (2002) 2699-2712
65. Krimpenfort P., Ijpenberg A., Song J.Y., van der Valk M., Nawijn M., Zevenhoven J., et al. p15Ink4b is a critical tumour suppressor in the absence of p16Ink4a. Nature 448 (2007) 943-946
66. Latres E., Malumbres M., Sotillo R., Martin J., Ortega S., Martin-Caballero J., et al. Limited overlapping roles of P15(INK4b) and P18(INK4c) cell cycle inhibitors in proliferation and tumorigenesis. EMBO J 19 (2000) 3496-3506
67. Lee A., Kessler J.D., Read T.A., Kaiser C., Corbeil D., Huttner W.B., et al. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 8 (2005) 723-729
68. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., et al. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359 (1992) 288-294
69. Lee M.H., Williams B.O., Mulligan G., Mukai S., Bronson R.T., Dyson N., et al. Targeted disruption of p107: functional overlap between p107 and Rb. Genes Dev 10 (1996) 1621-1632
70. Lee W.H., Bookstein R., Hong F., Young L.J., Shew J.Y., and Lee E.Y. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 235 (1987) 1394-1399
71. Lee Y., Kawagoe R., Sasai K., Li Y., Russell H.R., Curran T., et al. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 26 (2007) 6442-6447
72. Lee Y., Miller H.L., Jensen P., Hernan R., Connelly M., Wetmore C., et al. A molecular fingerprint for medulloblastoma. Cancer Res 63 (2003) 5428-5437
73. Leung C., Lingbeek M., Shakhova O., Liu J., Tanger E., Saremaslani P., et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 428 (2004) 337-341
74. Lewis P.M., Gritli-Linde A., Smeyne R., Kottmann A., and McMahon A.P. Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev Biol 270 (2004) 393-410
75. Lutolf S., Radtke F., Aguet M., Suter U., and Taylor V. Notch1 is required for neuronal and glial differentiation in the cerebellum. Development 129 (2002) 373-385
76. Machold R., Hayashi S., Rutlin M., Muzumdar M.D., Nery S., Corbin J.G., et al. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39 (2003) 937-950
77. Marigo V., Scott M.P., Johnson R.L., Goodrich L.V., and Tabin C.J. Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122 (1996) 1225-1233
78. Marino S. Medulloblastoma: developmental mechanisms out of control. Trends Mol Med 11 (2005) 17-22
79. Marino S., Hoogervoorst D., Brandner S., and Berns A. Rb and p107 are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development 130 (2003) 3359-3368
80. Marino S., Vooijs M., van Der Gulden H., Jonkers J., and 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 14 (2000) 994-1004
81. McAndrew P.E., Frostholm A., Evans J.E., Zdilar D., Goldowitz D., Chiu I.M., et al. Novel receptor protein tyrosine phosphatase (RPTPrho) and acidic fibroblast growth factor (FGF-1) transcripts delineate a rostrocaudal boundary in the granule cell layer of the murine cerebellar cortex. J Comp Neurol 391 (1998) 444-455
82. McMahon A.P., and Bradley A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62 (1990) 1073-1085
83. Miyake A., Minami M., Satoh M., Ohta M., and Itoh N. Transient expression of FGF receptor-4 mRNA in the rat cerebellum during postnatal development. Brain Res Mol Brain Res 31 (1995) 95-100
84. Miyazawa K., Himi T., Garcia V., Yamagishi H., Sato S., and Ishizaki Y. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 20 (2000) 5756-5763
85. Muzumdar M.D., Luo L., and Zong H. Modeling sporadic loss of heterozygosity in mice by using mosaic analysis with double markers (MADM). Proc Natl Acad Sci USA 104 (2007) 4495-4500
86. Nurse P. A long twentieth century of the cell cycle and beyond. Cell 100 (2000) 71-78
87. Oh L.Y., Denninger A., Colvin J.S., Vyas A., Tole S., Ornitz D.M., et al. Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci 23 (2003) 883-894
88. Oliver T.G., Grasfeder L.L., Carroll A.L., Kaiser C., Gillingham C.L., Lin S.M., et al. Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 100 (2003) 7331-7336
89. Oliver T.G., Read T.A., Kessler J.D., Mehmeti A., Wells J.F., Huynh T.T., et al. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 132 (2005) 2425-2439
90. Orii K.E., Lee Y., Kondo N., and McKinnon P.J. Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc Natl Acad Sci USA 103 (2006) 10017-10022
91. Ozawa K., Uruno T., Miyakawa K., Seo M., and Imamura T. Expression of the fibroblast growth factor family and their receptor family genes during mouse brain development. Brain Res Mol Brain Res 41 (1996) 279-288
92. Palma V., and Ruiz i Altaba A. Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131 (2004) 337-345
93. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.C., et al. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127 (2000) 1593-1605
94. Patapoutian A., and Reichardt L.F. Roles of Wnt proteins in neural development and maintenance. Curr Opin Neurobiol 10 (2000) 392-399
95. Pietsch T., Waha A., Koch A., Kraus J., Albrecht S., Tonn J., et al. Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res 57 (1997) 2085-2088
96. Pogoriler J., Millen K., Utset M., and Du W. Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation. Development 133 (2006) 3929-3937
97. Pomeroy S.L., Tamayo P., Gaasenbeek M., Sturla L.M., Angelo M., McLaughlin M.E., et al. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415 (2002) 436-442
98. Raffel C., Jenkins R.B., Frederick L., Hebrink D., Alderete B., Fults D.W., et al. Sporadic medulloblastomas contain PTCH mutations. Cancer Res 57 (1997) 842-845
99. Rao G., Pedone C.A., Del Valle L., Reiss K., Holland E.C., and Fults D.W. Sonic hedgehog and insulin-like growth factor signaling synergize to induce medulloblastoma formation from nestin-expressing neural progenitors in mice. Oncogene 23 (2004) 6156-6162
100. Reifenberger J., Wolter M., Weber R.G., Megahed M., Ruzicka T., Lichter P., et al. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res 58 (1998) 1798-1803
101. Rios I., Alvarez-Rodriguez R., Marti E., and Pons S. Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling. Development 131 (2004) 3159-3168
102. Ross M.E., Carter M.L., and Lee J.H. MN20, a D2 cyclin, is transiently expressed in selected neural populations during embryogenesis. J Neurosci 16 (1996) 210-219
103. Sasai K., Romer J.T., Kimura H., Eberhart D.E., Rice D.S., and Curran T. Medulloblastomas derived from Cxcr6 mutant mice respond to treatment with a smoothened inhibitor. Cancer Res 67 (2007) 3871-3877
104. Schuller U., and Rowitch D.H. Beta-catenin function is required for cerebellar morphogenesis. Brain Res 1140 (2007) 161-169
105. Sengupta S., and Harris C.C. p53: traffic cop at the crossroads of DNA repair and recombination. Nat Rev Mol Cell Biol 6 (2005) 44-55
106. Serrano M., Lee H., Chin L., Cordon-Cardo C., Beach D., and DePinho R.A. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85 (1996) 27-37
107. Shakhova O., Leung C., van Montfort E., Berns A., and Marino S. Lack of Rb and p53 delays cerebellar development and predisposes to large cell anaplastic medulloblastoma through amplification of N-Myc and Ptch2. Cancer Res 66 (2006) 5190-5200
108. Shambaugh III G.E., Haines III G.K., Koch A., Lee E.J., Zhou J., and Pestell R. Immunohistochemical examination of the INK4 and Cip inhibitors in the rat neonatal cerebellum: cellular localization and the impact of protein calorie malnutrition. Brain Res 855 (2000) 11-22
109. Sillitoe R.V., and Joyner A.L. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23 (2007) 549-577
110. Smeyne R.J., Chu T., Lewin A., Bian F., Sanlioglu S., Kunsch C., et al. Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 6 (1995) 230-251
111. Soerensen J., Jakupoglu C., Beck H., Forster H., Schmidt J., Schmahl W., et al. The role of thioredoxin reductases in brain development. PLoS ONE 3 (2008) e1813
112. Solecki D.J., Liu X.L., Tomoda T., Fang Y., and Hatten M.E. Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 31 (2001) 557-568
113. Sotelo C. Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72 (2004) 295-339
114. Taylor M.D., Liu L., Raffel C., Hui C.C., Mainprize T.G., Zhang X., et al. Mutations in SUFU predispose to medulloblastoma. Nat Genet 31 (2002) 306-310
115. Thomas K.R., and Capecchi M.R. Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346 (1990) 847-850
116. -/-) mice. Am J Pathol 162 (2003) 343-352
117. Unden A.B., Holmberg E., Lundh-Rozell B., Stahle-Backdahl M., Zaphiropoulos P.G., Toftgard R., et al. Mutations in the human homologue of Drosophila patched (PTCH) in basal cell carcinomas and the Gorlin syndrome: different in vivo mechanisms of PTCH inactivation. Cancer Res 56 (1996) 4562-4565
118. Uziel T., Zindy F., Xie S., Lee Y., Forget A., Magdaleno S., et al. The tumor suppressors Ink4c and p53 collaborate independently with Patched to suppress medulloblastoma formation. Genes Dev 19 (2005) 2656-2667
119. Vaillant C., Michos O., Orolicki S., Brellier F., Taieb S., Moreno E., et al. Protease nexin 1 and its receptor LRP modulate SHH signalling during cerebellar development. Development 134 (2007) 1745-1754
120. van Lookeren Campagne M., and Gill R. Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J Comp Neurol 397 (1998) 181-198
121. Wallace V.A. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9 (1999) 445-448
122. Wang Q., McEwen D.G., and Ornitz D.M. Subcellular and developmental expression of alternatively spliced forms of fibroblast growth factor 14. Mech Dev 90 (2000) 283-287
123. Wang Y., Huso D., Cahill H., Ryugo D., and Nathans J. Progressive cerebellar, auditory, and esophageal dysfunction caused by targeted disruption of the frizzled-4 gene. J Neurosci 21 (2001) 4761-4771
124. Wechsler-Reya R., and Scott M.P. The developmental biology of brain tumors. Annu Rev Neurosci 24 (2001) 385-428
125. Wechsler-Reya R.J. Caught in the matrix: how vitronectin controls neuronal differentiation. Trends Neurosci 24 (2001) 680-682
126. Wechsler-Reya R.J., and Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22 (1999) 103-114
127. Wolter M., Reifenberger J., Sommer C., Ruzicka T., and Reifenberger G. Mutations in the human homologue of the Drosophila segment polarity gene patched (PTCH) in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res 57 (1997) 2581-2585
128. Xie J., Johnson R.L., Zhang X., Bare J.W., Waldman F.M., Cogen P.H., et al. Mutations of the PATCHED gene in several types of sporadic extracutaneous tumors. Cancer Res 57 (1997) 2369-2372
129. Xu J., Liu Z., and Ornitz D.M. Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127 (2000) 1833-1843
130. Yamamoto H., Ochiya T., Takahama Y., Ishii Y., Osumi N., Sakamoto H., et al. Detection of spatial localization of Hst-1/Fgf-4 gene expression in brain and testis from adult mice. Oncogene 19 (2000) 3805-3810
131. Yan C.T., Kaushal D., Murphy M., Zhang Y., Datta A., Chen C., et al. XRCC4 suppresses medulloblastomas with recurrent translocations in p53-deficient mice. Proc Natl Acad Sci USA 103 (2006) 7378-7383
132. Yan Y., Frisen J., Lee M.H., Massague J., and Barbacid M. Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev 11 (1997) 973-983
133. Yun J.S., Rust J.M., Ishimaru T., and Diaz E. A novel role of the Mad family member Mad3 in cerebellar granule neuron precursor proliferation. Mol Cell Biol 27 (2007) 8178-8189
134. Zhang P., Liegeois N.J., Wong C., Finegold M., Hou H., Thompson J.C., et al. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387 (1997) 151-158
135. Zindy F., Knoepfler P.S., Xie S., Sherr C.J., Eisenman R.N., and Roussel M.F. N-Myc and the cyclin-dependent kinase inhibitors p18Ink4c and p27Kip1 coordinately regulate cerebellar development. Proc Natl Acad Sci USA 103 (2006) 11579-11583
136. Zindy F., Soares H., Herzog K.H., Morgan J., Sherr C.J., and Roussel M.F. Expression of INK4 inhibitors of cyclin D-dependent kinases during mouse brain development. Cell Growth Differ 8 (1997) 1139-1150
137. Zindy F., Uziel T., Ayrault O., Calabrese C., Valentine M., Rehg J.E., et al. Genetic alterations in mouse medulloblastomas and generation of tumors de novo from primary cerebellar granule neuron precursors. Cancer Res 67 (2007) 2676-2684
138. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., and Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393 (1998) 595-599
139. Zurawel R.H., Chiappa S.A., Allen C., and Raffel C. Sporadic medulloblastomas contain oncogenic beta-catenin mutations. Cancer Res 58 (1998) 896-899