Widespread contribution of GDF7 lineage to cerebellar cell types and implications for hedgehog-driven medulloblastoma formation

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Cheng, Frances Y ^a   Huang, Xi ^a,c   Sarangi, Anuraag ^b   Ketova, Tatiana ^a   Cooper, Michael K ^b   Litingtung, Ying ^a   Chiang, Chin ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 12; CYCLIN D2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN PATCHED; RETINOBLASTOMA PROTEIN; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR SOX2; BONE MORPHOGENETIC PROTEIN; GDF7 PROTEIN, MOUSE; GROWTH DIFFERENTIATION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN CELL; BRUSH BORDER; CELL HYPERPLASIA; CELL LINEAGE; CEREBELLUM; CHOROID PLEXUS; CONTROLLED STUDY; EPITHELIUM CELL; GABAERGIC SYSTEM; GAIN OF FUNCTION MUTATION; GLIA CELL; GRANULE CELL; HISTOPATHOLOGY; INTERNEURON; LEPTOMENINX; MEDULLOBLASTOMA; MOTOR COORDINATION; MOUSE; NONHUMAN; ONCOGENESIS AND MALIGNANT TRANSFORMATION; PARENCHYMA; PHENOTYPE; POINT MUTATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; STEM CELL; SUBVENTRICULAR ZONE; WHITE MATTER; ANIMAL; CYTOLOGY; GLIA; HYPERPLASIA; METABOLISM; NERVE CELL; PATHOLOGY; TUMOR CELL CULTURE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; CEREBELLUM; GROWTH DIFFERENTIATION FACTORS; HEDGEHOG PROTEINS; HYPERPLASIA; MEDULLOBLASTOMA; MICE; NEUROGLIA; NEURONS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84860008993     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035541     Document Type: Article

References (62)

1. Chizhikov VV, Millen KJ, (2004) Mechanisms of roof plate formation in the vertebrate CNS. Nature Reviews Neuroscience 5: 808-812.
2. Millonig JH, Millen KJ, Hatten ME, (2000) The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403: 764-769.
3. Lee K, Dietrich P, Jessell T, (2000) Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403: 734-740.
4. Lee KJ, Mendelsohn M, Jessell TM, (1998) Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes & development 12: 3394-3407.
5. Chizhikov V, Lindgren A, Currle D, Rose M, Monuki E, et al. (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development 133: 2793.
6. Lo L, Dormand EL, Anderson DJ, (2005) Late-emigrating neural crest cells in the roof plate are restricted to a sensory fate by GDF7. Proc Natl Acad Sci U S A 102: 7192-7197.
7. Monuki ES, Porter FD, Walsh CA, (2001) Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32: 591-604.
8. Awatramani R, Soriano P, Rodriguez C, Mai J, Dymecki S, (2003) Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nature Genetics 35: 70-75.
9. Currle D, Cheng X, Hsu C, Monuki E, (2005) Direct and indirect roles of CNS dorsal midline cells in choroid plexus epithelia formation. Development 132: 3549.
10. Hunter N, Dymecki S, (2007) Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus. Development 134: 3449.
11. Landsberg R, Awatramani R, Hunter N, Farago A, DiPietrantonio H, et al. (2005) Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48: 933-947.
12. Chizhikov VV, Lindgren AG, Mishima Y, Roberts RW, Aldinger KA, et al. (2010) Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proceedings of the National Academy of Sciences 107: 10725-10730.
13. Machold R, Fishell G, (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48: 17-24.
14. Wang V, Rose M, Zoghbi H, (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48: 31-43.
15. Thompson MC, (2006) Genomics Identifies Medulloblastoma Subgroups That Are Enriched for Specific Genetic Alterations. Journal of Clinical Oncology 24: 1924-1931.
16. Kool M, Koster J, Bunt J, Hasselt NE, Lakeman A, et al. (2008) Integrated Genomics Identifies Five Medulloblastoma Subtypes with Distinct Genetic Profiles, Pathway Signatures and Clinicopathological Features. PLoS ONE 3: e3088.
17. Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, et al. (2011) Medulloblastoma Comprises Four Distinct Molecular Variants. Journal of Clinical Oncology 29: 1408-1414.
18. Taylor MD, Northcott PA, Korshunov A, Remke M, Cho Y-J, et al. (2011) Molecular subgroups of medulloblastoma: the current consensus. Acta neuropathologica.
19. Kool M, Korshunov A, Remke M, Jones DTW, Schlanstein M, et al. (2012) Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta neuropathologica.
20. Cho Y-J, Tsherniak A, Tamayo P, Santagata S, Ligon A, et al. (2011) Integrative genomic analysis of medulloblastoma identifies a molecular subgroup that drives poor clinical outcome. Journal of Clinical Oncology 29: 1424-1430.
21. Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, et al. (2010) Subtypes of medulloblastoma have distinct developmental origins. Nature 468: 1-5.
22. Wechsler-Reya R, Scott M, (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22: 103-114.
23. Wallace V, (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Current Biology 9: 445-448.
24. Sillitoe RV, Joyner AL, (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annual review of cell and developmental biology 23: 549-577.
25. Dahmane N, Ruiz i Altaba A, (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126: 3089-3100.
26. Gilbertson R, Ellison D, (2008) The origins of medulloblastoma subtypes.
27. Yang Z, Ellis T, Markant S, Read T, Kessler J, et al. (2008) Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 14: 135-145.
28. Schüller U, Heine V, Mao J, Kho A, Dillon A, et al. (2008) Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14: 123-134.
29. Rao G, Pedone C, Coffin C, Holland E, Fults D, (2003) c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice. Neoplasia (New York, NY) 5: 198.
30. Rao G, Pedone C, Del Valle L, Reiss K, Holland E, et al. (2004) Sonic hedgehog and insulin-like growth factor signaling synergize to induce medulloblastoma formation from nestin-expressing neural progenitors in mice. Oncogene 23: 6156-6162.
31. Huang X, Ketova T, Fleming JT, Wang H, Dey SK, et al. (2009) Sonic hedgehog signaling regulates a novel epithelial progenitor domain of the hindbrain choroid plexus. Development 136: 2535-2543.
32. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, et al. (1998) Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391: 90-92.
33. Jeong J, Mao J, Tenzen T, Kottmann A, McMahon A, (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes & development 18: 937.
34. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP, (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18: 937-951.
35. Kenney A, Widlund H, Rowitch D, (2004) Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131: 217.
36. Hatton B, Knoepfler P, Kenney A, Rowitch D, de Alboran I, et al. (2006) N-myc is an essential downstream effector of Shh signaling during both normal and neoplastic cerebellar growth. Cancer Research 66: 8655.
37. Kenney A, Cole M, Rowitch D, (2003) Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130: 15.
38. Thomas WD, Chen J, Gao YR, Cheung B, Koach J, et al. (2009) Patched1 deletion increases N-Myc protein stability as a mechanism of medulloblastoma initiation and progression. Oncogene 28: 1605-1615.
39. Kessler JD, Hasegawa H, Brun SN, Yang ZJ, Dutton JW, et al. (2009) N-myc alters the fate of preneoplastic cells in a mouse model of medulloblastoma. Genes Dev 23: 157-170.
40. Johnson R, Rothman A, Xie J, Goodrich L, Bare J, et al. (1996) Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272: 1668.
41. Berman D, Karhadkar S, Hallahan A, Pritchard J, Eberhart C, et al. (2002) Medulloblastoma growth inhibition by hedgehog pathway blockade. Science's STKE 297: 1559.
42. Ward RJ, Lee L, Graham K, Satkunendran T, Yoshikawa K, et al. (2009) Multipotent CD15+ Cancer Stem Cells in Patched-1-Deficient Mouse Medulloblastoma. Cancer Research 69: 4682-4690.
43. Hunter NL, Dymecki SM, (2007) Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus. Development 134: 3449-3460.
44. Anthony TE, Klein C, Fishell G, Heintz N, (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41: 881-890.
45. Englund C, Kowalczyk T, Daza RAM, Dagan A, Lau C, et al. (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. Journal of Neuroscience 26: 9184-9195.
46. Zhang Y, Niu B, Yu D, Cheng X, Liu B, et al. (2010) Radial glial cells and the lamination of the cerebellar cortex. Brain Structure and Function 215: 115-122.
47. Dymecki SM, Tomasiewicz H, (1998) Using Flp-Recombinase to Characterize Expansion ofWnt1-Expressing Neural Progenitors in the Mouse. Developmental biology 201: 57-65.
48. Alder J, Lee K, Jessell T, Hatten M, (1999) Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nature Neuroscience 2: 535-540.
49. Inouye M, Murakami U, (1980) Temporal and spatial patterns of Purkinje cell formation in the mouse cerebellum. The Journal of comparative neurology 194: 499-503.
50. Northcott PA, Shih DJH, Remke M, Cho Y-J, Kool M, et al. (2011) Rapid, reliable, and reproducible molecular sub-grouping of clinical medulloblastoma samples. Acta neuropathologica.
51. Thompson M, Fuller C, Hogg T, Dalton J, Finkelstein D, et al. (2006) Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. Journal of Clinical Oncology 24: 1924.
52. Lang S-S, Beslow LA, Gabel B, Judkins AR, Fisher MJ, et al. (2011) Surgical Treatment of Brain Tumors in Infants Younger Than Six Months of Age and Review of the Literature. World Neurosurgery.
53. Due-T oslash nnessen BJ, Helseth E, (2007) Management of Hydrocephalus in Children with Posterior Fossa Tumors: Role of Tumor Surgery. Pediatric Neurosurgery 43: 92-96.
54. Dang L, Fan X, Chaudhry A, Wang M, Gaiano N, et al. (2006) Notch3 signaling initiates choroid plexus tumor formation. Oncogene 25: 487-491.
55. Fujimura M, Onuma T, Kameyama M, Motohashi O, Kon H, et al. (2004) Hydrocephalus due to cerebrospinal fluid overproduction by bilateral choroid plexus papillomas. Child's Nervous System 20.
56. Filippidis AS, Kalani MYS, Rekate HL, (2010) Hydrocephalus and aquaporins: lessons learned from the bench. Child's Nervous System 27: 27-33.
57. Banka S, Walsh R, Brundler M-A, (2006) First report of occurrence of choroid plexus papilloma and medulloblastoma in the same patient. Child's Nervous System 23: 587-589.
58. Lee KJ, Dietrich P, Jessell TM, (2000) Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403: 734-740.
59. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
60. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Developmental Biology 1: 4.
61. Litingtung Y, Chiang C, (2000) Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nature Neuroscience 3: 979-985.
62. Huang X, Ketova T, Litingtung Y, Chiang C, (2010) Isolation, Enrichment, and Maintenance of Medulloblastoma Stem Cells. Journal of Visualized Experiments.