Medulloblastoma Can Be Initiated by Deletion of Patched in Lineage-Restricted Progenitors or Stem Cells

Cancer Cell

Volumn 14, Issue 2, 2008, Pages 135-145

  Yang, Zeng Jie ^a   Ellis, Tammy ^b   Markant, Shirley L ^a   Read, Tracy Ann ^a,c   Kessler, Jessica D ^a   Bourboulas, Melissa ^b   Schüller, Ulrich ^d   Machold, Robert ^e   Fishell, Gord ^e   Rowitch, David H ^f   Wainwright, Brandon J ^b   Wechsler Reya, Robert J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF BERGEN   (Norway)

^d UNIVERSITY OF MUNICH   (Germany)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLBIO; HUMDISEASE; STEMCELL

Indexed keywords

CRE RECOMBINASE; GREEN FLUORESCENT PROTEIN; PROTEIN PATCHED; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL EXPANSION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE MUTATION; HYPERPLASIA; KNOCKOUT MOUSE; MEDULLOBLASTOMA; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALIA; ERINACEIDAE;

EID: 48449101742     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2008.07.003     Document Type: Article

References (52)

1. Adolphe C., Hetherington R., Ellis T., and Wainwright B. Patched1 functions as a gatekeeper by promoting cell cycle progression. Cancer Res. 66 (2006) 2081-2088
2. Ahn S., and Joyner A.L. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437 (2005) 894-897
3. Balordi F., and Fishell G. Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J. Neurosci. 27 (2007) 5936-5947
4. Bar E.E., Chaudhry A., Lin A., Fan X., Schreck K., Matsui W., Piccirillo S., Vescovi A.L., DiMeco F., Olivi A., and Eberhart C.G. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 25 (2007) 2524-2533
5. Becher O.J., Hambardzumyan D., Fomchenko E.I., Momota H., Mainwaring L., Bleau A.M., Katz A.M., Edgar M., Kenney A.M., Cordon-Cardo C., et al. Gli activity correlates with tumor grade in platelet-derived growth factor-induced gliomas. Cancer Res. 68 (2008) 2241-2249
6. Buhren J., Christoph A.H., Buslei R., Albrecht S., Wiestler O.D., and Pietsch T. Expression of the neurotrophin receptor p75NTR in medulloblastomas is correlated with distinct histological and clinical features: evidence for a medulloblastoma subtype derived from the external granule cell layer. J. Neuropathol. Exp. Neurol. 59 (2000) 229-240
7. Casper K.B., and McCarthy K.D. GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol. Cell. Neurosci. 31 (2006) 676-684
8. Clement V., Sanchez P., de Tribolet N., Radovanovic I., and Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 17 (2007) 165-172
9. Cozzio A., Passegue E., Ayton P.M., Karsunky H., Cleary M.L., and Weissman I.L. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 17 (2003) 3029-3035
10. Eberhart C.G. In search of the medulloblast: neural stem cells and embryonal brain tumors. Neurosurg. Clin. N. Am. 18 (2007) 59-69
11. Ehtesham M., Sarangi A., Valadez J.G., Chanthaphaychith S., Becher M.W., Abel T.W., Thompson R.C., and Cooper M.K. Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells. Oncogene 26 (2007) 5752-5761
12. Ellis T., Smyth I., Riley E., Graham S., Elliot K., Narang M., Kay G.F., Wicking C., and Wainwright B. Patched 1 conditional null allele in mice. Genesis 36 (2003) 158-161
13. Ellison D. Classifying the medulloblastoma: insights from morphology and molecular genetics. Neuropathol. Appl. Neurobiol. 28 (2002) 257-282
14. Gilbertson R.J., and Ellison D.W. The origins of medulloblastoma subtypes. Annu. Rev. Pathol. 3 (2008) 341-365
15. 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
16. 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
17. Hahn H., Wicking C., Zaphiropoulous P.G., Gailani M.R., Shanley S., Chidambaram A., Vorechovsky I., Holmberg E., Unden A.B., Gillies S., et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85 (1996) 841-851
18. Hahn H., Wojnowski L., Specht K., Kappler R., Calzada-Wack J., Potter D., Zimmer A., Muller U., Samson E., and Quintanilla-Martinez L. Patched target Igf2 is indispensable for the formation of medulloblastoma and rhabdomyosarcoma. J. Biol. Chem. 275 (2000) 28341-28344
19. Hamre K.M., and Goldowitz D. meander tail acts intrinsic to granule cell precursors to disrupt cerebellar development: analysis of meander tail chimeric mice. Development 124 (1997) 4201-4212
20. Hashimoto M., and Mikoshiba K. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J. Neurosci. 23 (2003) 11342-11351
21. Heikens J., Michiels E.M., Behrendt H., Endert E., Bakker P.J., and Fliers E. Long-term neuro-endocrine sequelae after treatment for childhood medulloblastoma. Eur. J. Cancer 34 (1998) 1592-1597
22. Hemmati H.D., Nakano I., Lazareff J.A., Masterman-Smith M., Geschwind D.H., Bronner-Fraser M., and Kornblum H.I. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. USA 100 (2003) 15178-15183
23. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., Quinn A.G., Myers R.M., Cox D.R., Epstein Jr. E.H., and Scott M.P. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272 (1996) 1668-1671
24. Kalifa C., and Grill J. The therapy of infantile malignant brain tumors: current status?. J. Neurooncol. 75 (2005) 279-285
25. 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
26. Krivtsov A.V., Twomey D., Feng Z., Stubbs M.C., Wang Y., Faber J., Levine J.E., Wang J., Hahn W.C., Gilliland D.G., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 (2006) 818-822
27. Machold R., and Fishell G. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48 (2005) 17-24
28. Mao X., Fujiwara Y., Chapdelaine A., Yang H., and Orkin S.H. Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 97 (2001) 324-326
29. Mulhern R.K., Palmer S.L., Merchant T.E., Wallace D., Kocak M., Brouwers P., Krull K., Chintagumpala M., Stargatt R., Ashley D.M., et al. Neurocognitive consequences of risk-adapted therapy for childhood medulloblastoma. J. Clin. Oncol. 23 (2005) 5511-5519
30. Oliver T.G., Grasfeder L.L., Carroll A.L., Kaiser C., Gillingham C.L., Lin S.M., Wickramasinghe R., Scott M.P., and Wechsler-Reya R.J. 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
31. Oliver T.G., Read T.A., Kessler J.D., Mehmeti A., Wells J.F., Huynh T.T., Lin S.M., and Wechsler-Reya R.J. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 132 (2005) 2425-2439
32. Packer R.J., Cogen P., Vezina G., and Rorke L.B. Medulloblastoma: clinical and biologic aspects. Neuro-oncol. 1 (1999) 232-250
33. Pevny L., and Placzek M. SOX genes and neural progenitor identity. Curr. Opin. Neurobiol. 15 (2005) 7-13
34. Pomeroy S.L., Sutton M.E., Goumnerova L.C., and Segal R.A. Neurotrophins in cerebellar granule cell development and medulloblastoma. J. Neurooncol. 35 (1997) 347-352
35. Raffel C., Jenkins R.B., Frederick L., Hebrink D., Alderete B., Fults D.W., and James C.D. Sporadic medulloblastomas contain PTCH mutations. Cancer Res. 57 (1997) 842-845
36. Read T.A., Hegedus B., Wechsler-Reya R., and Gutmann D.H. The neurobiology of neurooncology. Ann. Neurol. 60 (2006) 3-11
37. Romer J.T., Kimura H., Magdaleno S., Sasai K., Fuller C., Baines H., Connelly M., Stewart C.F., Gould S., Rubin L.L., and Curran T. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice. Cancer Cell 6 (2004) 229-240
38. Salsano E., Pollo B., Eoli M., Giordana M.T., and Finocchiaro G. Expression of MATH1, a marker of cerebellar granule cell progenitors, identifies different medulloblastoma sub-types. Neurosci. Lett. 370 (2004) 180-185
39. Sanchez P., and Ruiz i Altaba A. In vivo inhibition of endogenous brain tumors through systemic interference of Hedgehog signaling in mice. Mech. Dev. 122 (2005) 223-230
40. Schüller U., Zhao Q., Godinho S.A., Heine V.M., Medema R.H., Pellman D., and Rowitch D.H. Forkhead transcription factor FoxM1 regulates mitotic entry and prevents spindle defects in cerebellar granule neuron precursors. Mol. Cell. Biol. 27 (2007) 8259-8270
41. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., and Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63 (2003) 5821-5828
42. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., and Dirks P.B. Identification of human brain tumour initiating cells. Nature 432 (2004) 396-401
43. Spassky N., Han Y.G., Aguilar A., Strehl L., Besse L., Laclef C., Romaguera Ros M., Garcia-Verdugo J.M., and Alvarez-Buylla A. Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev. Biol. 317 (2008) 246-259
44. Surmeier D.J., Mermelstein P.G., and Goldowitz D. The weaver mutation of GIRK2 results in a loss of inwardly rectifying K+ current in cerebellar granule cells. Proc. Natl. Acad. Sci. USA 93 (1996) 11191-11195
45. Tanaka S., Kamachi Y., Tanouchi A., Hamada H., Jing N., and Kondoh H. Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol. Cell. Biol. 24 (2004) 8834-8846
46. Wang V.Y., Rose M.F., and Zoghbi H.Y. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48 (2005) 31-43
47. Wechsler-Reya R.J., and Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22 (1999) 103-114
48. Wetmore C., Eberhart D.E., and Curran T. Loss of p53 but not ARF accelerates medulloblastoma in mice heterozygous for patched. Cancer Res. 61 (2001) 513-516
49. Yokota N., Aruga J., Takai S., Yamada K., Hamazaki M., Iwase T., Sugimura H., and Mikoshiba K. Predominant expression of human zic in cerebellar granule cell lineage and medulloblastoma. Cancer Res. 56 (1996) 377-383
50. Zhuo L., Sun B., Zhang C.L., Fine A., Chiu S.Y., and Messing A. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev. Biol. 187 (1997) 36-42
51. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Willecke K., and Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31 (2001) 85-94
52. Zindy F., Uziel T., Ayrault O., Calabrese C., Valentine M., Rehg J.E., Gilbertson R.J., Sherr C.J., and Roussel M.F. Genetic alterations in mouse medulloblastomas and generation of tumors de novo from primary cerebellar granule neuron precursors. Cancer Res. 67 (2007) 2676-2684