Suppressors of Hedgehog signaling: Linking aberrant development of neural progenitors and tumorigenesis

Molecular Neurobiology

Volumn 34, Issue 3, 2006, Pages 193-204

  Di Marcotullio, Lucia ^a   Ferretti, Elisabetta ^a   De Smaele, Enrico ^a   Screpanti, Isabella ^a,b   Gulino, Alberto ^a,b,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Pasteur Institute   (Italy)

^c IRCCS NEUROMED   (Italy)

Author keywords

Cerebellum; ErbB4; Gli; Granule cell progenitors; Hedgehog; Medulloblastoma; Neural stem cells; RENKCTD11

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYT 2 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BRAIN DEVELOPMENT; CARCINOGENESIS; CHROMOSOME 17P; CHROMOSOME DELETION; DOWN REGULATION; GENE; GROWTH DISORDER; HUMAN; MEDULLOBLASTOMA; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REN KCTD11 GENE; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 33847084412     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1385/MN:34:3:193     Document Type: Article

References (65)

1. Nusslein-Volhard C. and Wieschaus E. (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
2. Ruiz i Altaba A., Palma V., and Dahmane N. (2002) Hedgehog-Gli signaling and the growth of the brain. Nat. Rev. Neurosci. 3, 24-33.
3. Pasca di Magliano M. and Hebrok M. (2003) Hedgehog signaling in cancer formation and maintenance. Nat. Rev. Cancer. 3, 903-911.
4. Beachy P. A., Karhadkar S. S., and Berman D. M. (2004) Tissue repair and stem cell renewal in carcinogenesis. Nature 432, 324-331.
5. Dellovade T., Romer J. T., Curran T., and Rubin L. L. (2006) The Hedgehog Pathway and Neurological Disorders. Annu. Rev. Neurosci. 29, 539-563.
6. Hooper J. E., and Scott M. P. (2005) Communicating with Hedgehogs. Nat. Rev. Mol. Cell Biol. 6, 306-317.
7. Yao S., Lum L., and Beachy P. (2006) The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell 125, 343-357.
8. Tenzen T., Allen B. L., Cole F., Kang J. S., Krauss R. S., and McMahon A. P. (2006) The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell 10, 647-656.
9. Zhang W., Kang J. S., Cole F., Yi M. J., and Krauss R. S. (2006) Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev. Cell 10, 657-665.
10. Corcoran R. B., and Scott M. P. (2006) Oxysterols stimulate Sonic hedgehog signal transduction and proliferation of medulloblastoma cells. Proc. Natl. Acad. Sci. USA. 103, 8408-8413.
11. Incardona J. P., Gruenberg J., and Roelink H. (2002) Sonic hedgehog induces the segregation of patched and smoothened in endosomes. Curr Biol. 12, 983-995.
12. Chen W., Ren X. R., Nelson C. D., et al. (2004) Activity-dependent internalization of smoothened mediated by beta-arrestin 2 and GRK2. Science 306, 2257-2260.
13. Wilbanks A. M., Fralish G. B., Kirby M. L., Barak L. S., Li Y. X., and Caron M. G. (2004) Betaarrestin 2 regulates zebrafish development through the hedgehog signaling pathway. Science 306, 2264-2267.
14. Huangfu D. and Anderson K. V. (2005) Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA. 102, 11,325-11,330.
15. Corbit K. C., Aanstad P., Singla V., Norman A. R., Stainier D. Y., and Reiter J. F. (2005) Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018-1021.
16. Haycraft C. J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E. J., and Yoder B. K. (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS. Genet. 1, e53.
17. Tay S. Y., Ingham P. W., and Roy S. (2005) A homologue of the Drosophila kinesin-like protein Costal2 regulates Hedgehog signal transduction in the vertebrate embryo. Development 132, 625-634.
18. Varjosalo M., Li S. P., and Taipale J. (2006) Divergence of hedgehog signal transduction mechanism between Drosophila and mammals. Dev. Cell. 10, 177-186.
19. Huangfu D., Liu A., Rakeman A. S., Murcia N. S., Niswander L., and Anderson K. V. (2003) Hedgehog signaling in the mouse requires intraflagellar transport proteins. Nature 426, 83-87.
20. Liu A., Wang B., and Niswander L. A. (2005) Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132, 3103-3111.
21. Park T. J., Haigo S. L., and Wallingford J. B. (2006) Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 38, 303-311.
22. Dai P., Akimaru H., Tanaka Y., Maekawa T., Nakafuku M,. Ishii S. (1999) Sonic Hedgehoginduced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152.
23. Eggenschwiler J. T., Bulgakov O. V., Qin J., Li T., and Anderson K. V. (2006) Mouse Rab23 regulates hedgehog signaling from smoothened to Gli proteins. Dev. Biol. 290, 1-12.
24. Jiang J. and Struhl G. (1998) Regulation of the Hedgehog and Wingless signaling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493-496
25. Huntzicker E. G., Estay I. S., Zhen H., Lokteva L. A., Jackson P. K., and Oro A. E. (2006) Dual degradation signals control Gli protein stability and tumor formation. Gen. Dev. 20, 276-281.
26. Wang B. and Li Y. (2006) Evidence for the direct involvement of βTrCP in Gli3 protein processing. Proc. Natl. Acad. Sci. USA. 103, 33-38
27. Pan Y., Bai C. B., Joyner A. L., and Wang B. (2006) Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell Biol. 26, 3365-3377.
28. Sheng T., Chi S., Zhang X., and Xie J. (2006) Regulation of Gli1 localization by the cAMP/ protein kinase A signaling axis through a site near the nuclear localization signal. J. Biol. Chem. 281, 9-12.
29. Kogerman P., Grimm T., Kogerman L., et al. (1999) Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat. Cell Biol. 1, 312-319.
30. Cheng S. Y. and Bishop J. M. (2002) Suppressor of Fused represses Gli-mediated transcription by recruiting the SAP18-mSin3 corepressor complex. Proc. Natl. Acad. Sci. USA. 16, 5442-5447
31. Stone D. M., Murone M., Luoh S., et al. (1999) Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli. J. Cell Sci. 112, 4437-4448.
32. Ding Q., Fukami S., Meng X., et al. (1999) Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1. Curr. Biol. 9, 1119-1122
33. Di Marcotullio L., Ferretti E., De Smaele E., et al. (2004) A. REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc. Natl. Acad. Sci. USA. 101, 10,833-10,838.
34. Huangfu D. and Anderson K. V. (2006) Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133, 3-14.
35. Ferretti E., De Smaele E., Di Marcotullio L., Screpanti I., and Gulino A. (2005) Hedgehog checkpoints in medulloblastoma: the chromosome 17p deletion paradigm. Trends Mol. Med. 11, 537-545
36. Osterlund T. and Kogerman P. (2006) Hedgehog signaling: how to get from Smo to Ci and Gli. Trends Cell Biol. 16, 176-180.
37. Ruiz i Altaba A., Sanchez P., and Dahmane N. (2002) Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer. 2, 361-372.
38. Lai K., Kaspar B. K., Gage F. H., and Schaffer D. V. (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6, 21-27
39. Machold R., Hayashi S., Rutlin M., et al. (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39, 937-950
40. Palma V. and Ruiz i Altaba A. (2004) Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131, 337-345
41. Palma V., Lim D. A., Dahmane N., et al. (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132, 335-344
42. Ahn S. and Joyner A. L. (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437, 894-897
43. Singh S. K., Hawkins C., Clarke I. D., et al. (2004) Identification of human brain tumour initiating cells. Nature 432, 396-401
44. Wechsler-Reya R. J. and Scott M. P. (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
45. Dahmane N, Ruiz i Altaba A. (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100.
46. Wallace V. A. (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448.
47. Lee A., Kessler J. D., Read T. A., et al. (2005) Isolation of neural stem cells from the postnatal cerebellum. Nat. Neurosci. 8, 723-729.
48. Dahmane N., Sanchez P., Gitton Y., et al. (2001) The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128, 5201-5212.
49. Berman D. M., Karhadkar S. S., Hallahan A. R., et al. (2002) Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 297, 1559-1561.
50. Romer J. T., Kimura H., Magdaleno S., et al. (2004) Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-)mice. Cancer Cell 6, 229-240.
51. Sanchez P. and Ruiz i Altaba A. (2005) In vivo inhibition of endogenous brain tumors through systemic interference of Hedgehog signaling in mice. Mech. Dev. 122, 223-230.
52. Thompson M. C., Fuller C., Hogg T. L.,et al. (2006) Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J. Clin. Oncol. 24, 1924-1931.
53. Svard J., Heby-Henricson K., Persson-Lek M., et al. (2006) Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev. Cell. 10, 187-197.
54. Goodrich L. V., Milenkovic L., Higgins K. M., and Scott M. P. (1997) Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
55. Hahn H., Wojnowski L., Zimmer A. M., Hall J., Miller G., and Zimmer A. (1998) Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nat. Med. 4, 619-622.
56. Oliver T. G., Read T. A., Kessler J. D., et al. (2005) Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 132, 2425-2439
57. Pazzaglia S., Tanori M., Mancuso M., et al. (2006) Two-hit model for progression of medulloblastoma preneoplasia in Patched heterozygous mice. Oncogene 25, 5575-5580.
58. Gallo R., Zazzeroni F., Alesse E., et al. (2002) REN: a novel, developmentally regulated gene that promotes neural cell differentiation. J. Cell Biol. 158, 731-740.
59. Argenti B., Gallo R., Di Marcotullio L., et al. (2005) Hedgehog antagonist REN(KCTD11) regulates proliferation and apoptosis of developing granule cell progenitors. J. Neurosci. 25, 8338-8346.
60. Ferretti E., Di Marcotullio L., Gessi M., et al. (2006) Alternative splicing of the ErbB-4 cytoplasmic domain and its regulation by Hedgehog signaling identify distinct medulloblastoma subsets. Oncogene, July 31 (epub ahead of print)
61. Tidcombe H., Jackson-Fisher A., Mathers K., Stern D. F., Gassmann M., and Golding J. P. (2003) Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc. Natl. Acad. Sci. USA. 100, 8281-8286.
62. Rieff H. I., Raetzman L. T., Sapp D. W., Yeh H. H., Siegel R. E., Corfas G. (1999) Neuregulin induces GABA(A) receptor subunit expression and neurite outgrowth in cerebellar granule cells. J. Neurosci. 19, 10,757-10,766.
63. Gilbertson R. .J., Clifford S. C., MacMeekin W., et al. (1998) Expression of the ErbB-neuregulin signaling network during human cerebellar development: implications for the biology of medulloblastoma. Cancer Res. 58, 3932-3941.
64. Kainulainen V., Sundvall M, Maatta J. A., Santiestevan E., Klagsbrun M., and Elenius K. (2000) A natural ErbB4 isoform that does not activate phosphoinositide 3-kinase mediates proliferation but not survival or chemotaxis. J. Biol. Chem. 275, 8641-8649.
65. Elenius K., Choi C. J., Paul S., Santiestevan E., Nishi E., and Klagsbrun M. (1999) Characterization of a naturally occurring ErbB4 isoform that does not bind or activate phosphatidyl inositol 3-kinase. Oncogene. 18, 2607-2615.