SHH pathway and cerebellar development

Cerebellum

Volumn 8, Issue 3, 2009, Pages 291-301

  Vaillant, Catherine ^a   Monard, Denis ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Cerebellum; Development; Foliation; Proliferation; Sonic hedgehog

Indexed keywords

CHEMOKINE; GROWTH FACTOR; SONIC HEDGEHOG PROTEIN;

ATAXIA; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL POPULATION; CEREBELLUM CORTEX; DOWN SYNDROME; EXTRACELLULAR MATRIX; GLIA; GRANULAR CELL; HOMEOSTASIS; HUMAN; MEDULLOBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; REVIEW;

ANIMALS; ATAXIA; CEREBELLUM; DISEASE MODELS, ANIMAL; DOWN SYNDROME; HEDGEHOG PROTEINS; HUMANS; MEDULLOBLASTOMA; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 69549130773     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-009-0094-8     Document Type: Review

References (104)

1. AP McMahon PW Ingham CJ Tabin 2003 Developmental roles and clinical significance of hedgehog signaling Curr Top Dev Biol 53 1 114
2. M Varjosalo J Taipale 2008 Hedgehog: functions and mechanisms Genes Dev 22 2454 2472
3. DL DeCamp TM Thompson FJ de Sauvage MR Lerner 2000 Smoothened activates Galphai-mediated signaling in frog melanophores J Biol Chem 275 26322 26327
4. D Huangfu KV Anderson 2006 Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates Development 133 3 14
5. M Fuccillo AL Joyner G Fishell 2006 Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development Nat Rev Neurosci 7 772 783
6. RV Sillitoe AL Joyner 2007 Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum Annu Rev Cell Dev Biol 23 549 577
7. ME Hatten J Alder K Zimmerman N Heintz 1997 Genes involved in cerebellar cell specification and differentiation Curr Opin Neurobiol 7 40 47
8. M Repetto JC Maziere D Citadelle R Dupuis M Meier S Biade, et al. 1990 Teratogenic effect of the cholesterol synthesis inhibitor AY 9944 on rat embryos in vitro Teratology 42 611 618
9. L Lanoue DB Dehart ME Hinsdale N Maeda GS Tint KK Sulik 1997 Limb, genital, CNS, and facial malformations result from gene/environment-induced cholesterol deficiency: further evidence for a link to sonic hedgehog Am J Med Genet 73 24 31
10. DB Dehart L Lanoue GS Tint KK Sulik 1997 Pathogenesis of malformations in a rodent model for Smith-Lemli-Opitz syndrome Am J Med Genet 68 328 337
11. H Yu SB Patel 2005 Recent insights into the Smith-Lemli-Opitz syndrome Clin Genet 68 383 391
12. FD Porter 2003 Human malformation syndromes due to inborn errors of cholesterol synthesis Curr Opin Pediatr 15 607 613
13. N Dahmane A Ruiz i Altaba 1999 Sonic hedgehog regulates the growth and patterning of the cerebellum Development 126 3089 3100
14. VA Wallace 1999 Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum Curr Biol 9 445 448
15. RJ Wechsler-Reya MP Scott 1999 Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog Neuron 22 103 114
16. AM Kenney DH Rowitch 2000 Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors Mol Cell Biol 20 9055 9067
17. JD Corrales S Blaess EM Mahoney AL Joyner 2006 The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation Development 133 1811 1821
18. JD Corrales GL Rocco S Blaess Q Guo AL Joyner 2004 Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development Development 131 5581 5590
19. E Traiffort D Charytoniuk L Watroba H Faure N Sales M Ruat 1999 Discrete localizations of hedgehog signalling components in the developing and adult rat nervous system Eur J Neurosci 11 3199 31214
20. PM Lewis A Gritli-Linde R Smeyne A Kottmann AP McMahon 2004 Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum Dev Biol 270 393 410
21. E Diaz Y Ge YH Yang KC Loh TA Serafini Y Okazaki, et al. 2002 Molecular analysis of gene expression in the developing pontocerebellar projection system Neuron 36 417 434
22. TG Oliver LL Grasfeder AL Carroll C Kaiser CL Gillingham SM Lin, et al. 2003 Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors Proc Natl Acad Sci U S A 100 7331 7336
23. SK Sjostrom G Finn WC Hahn DH Rowitch AM Kenney 2005 The Cdk1 complex plays a prime role in regulating N-myc phosphorylation and turnover in neural precursors Dev Cell 9 327 338
24. Q Zhao A Kho AM Kenney DI Yuk Di I Kohane DH Rowitch 2002 Identification of genes expressed with temporal-spatial restriction to developing cerebellar neuron precursors by a functional genomic approach Proc Natl Acad Sci U S A 99 5704 5709
25. J Pogoriler K Millen M Utset W Du 2006 Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation Development 133 3929 3937
26. JM Huard CC Forster ML Carter P Sicinski ME Ross 1999 Cerebellar histogenesis is disturbed in mice lacking cyclin D2 Development 126 1927 1935
27. MA Ciemerych AM Kenney E Sicinska I Kalaszczynska RT Bronson DH Rowitch, et al. 2002 Development of mice expressing a single D-type cyclin Genes Dev 16 3277 3289
28. U Schuller Q Zhao SA Godinho VM Heine RH Medema D Pellman, et al. 2007 Forkhead transcription factor FoxM1 regulates mitotic entry and prevents spindle defects in cerebellar granule neuron precursors Mol Cell Biol 27 8259 8270
29. PS Knoepfler PF Cheng RN Eisenman 2002 N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation Genes Dev 16 2699 2712
30. AM Kenney MD Cole DH Rowitch 2003 Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors Development 130 15 28
31. JS Yun JM Rust T Ishimaru E Diaz 2007 A novel role of the Mad family member Mad3 in cerebellar granule neuron precursor proliferation Mol Cell Biol 27 8178 8189
32. C Leung M Lingbeek O Shakhova J Liu E Tanger P Saremaslani, et al. 2004 Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas Nature 428 337 341
33. E Traiffort DA Charytoniuk H Faure M Ruat 1998 Regional distribution of Sonic Hedgehog, patched, and smoothened mRNA in the adult rat brain J Neurochem 70 1327 1330
34. RS Klein JB Rubin HD Gibson EN DeHaan X Alvarez-Hernandez RA Segal, et al. 2001 SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells Development 128 1971 1981
35. W Hartmann A Koch H Brune A Waha U Schuller I Dani, et al. 2005 Insulin-like growth factor II is involved in the proliferation control of medulloblastoma and its cerebellar precursor cells Am J Pathol 166 1153 1162
36. SR Parathath LA Mainwaring LA Fernandez DO Campbell AM Kenney 2008 Insulin receptor substrate 1 is an effector of sonic hedgehog mitogenic signaling in cerebellar neural precursors Development 135 19 3291 3300
37. OJ Shah T Hunter 2006 Turnover of the active fraction of IRS1 involves raptor-mTOR- and S6K1-dependent serine phosphorylation in cell culture models of tuberous sclerosis Mol Cell Biol 26 6425 6434
38. C Vaillant M Didier-Bazes A Hutter MF Belin N Thomasset 1999 Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum J Neurosci 19 4994 5004
39. C Vaillant C Meissirel M Mutin MF Belin LR Lund N Thomasset 2003 MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum Mol Cell Neurosci 24 395 408
40. S Blaess D Graus-Porta R Belvindrah R Radakovits S Pons A Littlewood-Evans, et al. 2004 Beta1-integrins are critical for cerebellar granule cell precursor proliferation J Neurosci 24 3402 3412
41. J Mills A Niewmierzycka A Oloumi B Rico R St-Arnaud IR Mackenzie, et al. 2006 Critical role of integrin-linked kinase in granule cell precursor proliferation and cerebellar development J Neurosci 26 830 840
42. JB Rubin Y Choi RA Segal 2002 Cerebellar proteoglycans regulate sonic hedgehog responses during development Development 129 2223 2232
43. S Pons JL Trejo JR Martinez-Morales E Marti 2001 Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation Development 128 1481 1492
44. C Vaillant O Michos S Orolicki F Brellier S Taieb E Moreno, et al. 2007 Protease nexin 1 and its receptor LRP modulate SHH signalling during cerebellar development Development 134 1745 1754
45. RA McCarthy WS Argraves 2003 Megalin and the neurodevelopmental biology of sonic hedgehog and retinol J Cell Sci 116 955 960
46. TE Willnow J Hilpert SA Armstrong A Rohlmann RE Hammer DK Burns, et al. 1996 Defective forebrain development in mice lacking gp330/megalin Proc Natl Acad Sci U S A 93 8460 8464
47. X Li J Herz D Monard 2006 Activation of ERK signaling upon alternative protease nexin-1 internalization mediated by syndecan-1 J Cell Biochem 99 936 951
48. A Nicot V Lelievre J Tam JA Waschek E DiCicco-Bloom 2002 Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation J Neurosci 22 9244 9254
49. MP Fogarty BA Emmenegger LL Grasfeder TG Oliver RJ Wechsler-Reya 2007 Fibroblast growth factor blocks Sonic hedgehog signaling in neuronal precursors and tumor cells Proc Natl Acad Sci U S A 104 2973 2978
50. A Lee JD Kessler TA Read C Kaiser D Corbeil WB Huttner, et al. 2005 Isolation of neural stem cells from the postnatal cerebellum Nat Neurosci 8 723 729
51. I Rios R Alvarez-Rodriguez E Marti S Pons 2004 Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling Development 131 3159 3168
52. R Alvarez-Rodriguez M Barzi J Berenguer S Pons 2007 Bone morphogenetic protein 2 opposes Shh-mediated proliferation in cerebellar granule cells through a TIEG-1-based regulation of Nmyc J Biol Chem 282 37170 37180
53. R Gallo F Zazzeroni E Alesse C Mincione U Borello P Buanne, et al. 2002 REN: a novel, developmentally regulated gene that promotes neural cell differentiation J Cell Biol 158 731 740
54. B Argenti R Gallo L Di Marcotullio E Ferretti M Napolitano S Canterini, et al. 2005 Hedgehog antagonist REN(KCTD11) regulates proliferation and apoptosis of developing granule cell progenitors J Neurosci 25 8338 8346
55. AL Klein O Zilian U Suter V Taylor 2004 Murine numb regulates granule cell maturation in the cerebellum Dev Biol 266 161 177
56. L Di Marcotullio E Ferretti A Greco E De Smaele A Po MA Sico, et al. 2006 Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination Nat Cell Biol 8 1415 1423
57. C Wetmore 2003 Sonic hedgehog in normal and neoplastic proliferation: insight gained from human tumors and animal models Curr Opin Genet Dev 13 34 42
58. MP Fogarty JD Kessler RJ Wechsler-Reya 2005 Morphing into cancer: the role of developmental signaling pathways in brain tumor formation J Neurobiol 64 458 475
59. CG Eberhart 2007 In search of the medulloblast: neural stem cells and embryonal brain tumors Neurosurg Clin N Am 18 59 69 viii-ix
60. HD Hemmati I Nakano JA Lazareff M Masterman-Smith DH Geschwind M Bronner-Fraser, et al. 2003 Cancerous stem cells can arise from pediatric brain tumors Proc Natl Acad Sci U S A 100 15178 15183
61. U Schuller VM Heine J Mao AT Kho AK Dillon YG Han, 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
62. ZJ Yang T Ellis SL Markant TA Read JD Kessler M Bourboulas, et al. 2008 Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells Cancer Cell 14 135 145
63. RJ Gorlin 1995 Nevoid basal cell carcinoma syndrome Dermatol Clin 13 113 125
64. T Pietsch A Koch OD Wiestler 1997 Molecular genetic studies in medulloblastomas: evidence for tumor suppressor genes at the chromosomal regions 1q31-32 and 17p13 Klin Padiatr 209 150 155
65. MD Taylor L Liu C Raffel CC Hui TG Mainprize X Zhang, et al. 2002 Mutations in SUFU predispose to medulloblastoma Nat Genet 31 306 310
66. J Reifenberger M Wolter RG Weber M Megahed T Ruzicka P Lichter, et al. 1998 Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system Cancer Res 58 1798 1803
67. HL Weiner R Bakst MS Hurlbert J Ruggiero E Ahn WS Lee, et al. 2002 Induction of medulloblastomas in mice by sonic hedgehog, independent of Gli1 Cancer Res 62 6385 6389
68. G Rao CA Pedone CM Coffin EC Holland DW Fults 2003 c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice Neoplasia 5 198 204
69. LV Goodrich L Milenkovic KM Higgins MP Scott 1997 Altered neural cell fates and medulloblastoma in mouse patched mutants Science 277 1109 1113
70. AR Hallahan JI Pritchard S Hansen M Benson J Stoeck BA Hatton, et al. 2004 The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas Cancer Res 64 7794 7800
71. J Mao KL Ligon EY Rakhlin SP Thayer RT Bronson D Rowitch, et al. 2006 A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway Cancer Res 66 10171 10178
72. H Kimura D Stephen A Joyner T Curran 2005 Gli1 is important for medulloblastoma formation in Ptc1+/- mice Oncogene 24 4026 4036
73. C Wetmore DE Eberhart T Curran 2001 Loss of p53 but not ARF accelerates medulloblastoma in mice heterozygous for patched Cancer Res 61 513 516
74. Y Lee R Kawagoe K Sasai Y Li HR Russell T Curran, et al. 2007 Loss of suppressor-of-fused function promotes tumorigenesis Oncogene 26 6442 6447
75. Y Lee HL Miller P Jensen R Hernan M Connelly C Wetmore, et al. 2003 A molecular fingerprint for medulloblastoma Cancer Res 63 5428 5437
76. SL Pomeroy P Tamayo M Gaasenbeek LM Sturla M Angelo ME McLaughlin, et al. 2002 Prediction of central nervous system embryonal tumour outcome based on gene expression Nature 415 436 442
77. H Hahn L Wojnowski K Specht R Kappler J Calzada-Wack D Potter, et al. 2000 Patched target Igf2 is indispensable for the formation of medulloblastoma and rhabdomyosarcoma J Biol Chem 275 28341 28344
78. G Rao CA Pedone L Del Valle K Reiss EC Holland DW Fults 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
79. AM Kenney HR Widlund DH Rowitch 2004 Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors Development 131 217 228
80. SR Browd AM Kenney ON Gottfried JW Yoon D Walterhouse CA Pedone, et al. 2006 N-myc can substitute for insulin-like growth factor signaling in a mouse model of sonic hedgehog-induced medulloblastoma Cancer Res 66 2666 2672
81. E Ferretti E De Smaele E Miele P Laneve A Po M Pelloni, et al. 2008 Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells EMBO J 27 2616 2627
82. L Di Marcotullio E Ferretti E De Smaele B Argenti C Mincione F Zazzeroni, et al. 2004 REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma Proc Natl Acad Sci U S A 101 10833 10838
83. E Ferretti E De Smaele L Di Marcotullio I Screpanti A Gulino 2005 Hedgehog checkpoints in medulloblastoma: the chromosome 17p deletion paradigm Trends Mol Med 11 537 545
84. KJ Briggs IM Corcoran-Schwartz W Zhang T Harcke WL Devereux SB Baylin, et al. 2008 Cooperation between the Hic1 and Ptch1 tumor suppressors in medulloblastoma Genes Dev 22 770 785
85. DM Berman SS Karhadkar AR Hallahan JI Pritchard CG Eberhart DN Watkins, et al. 2002 Medulloblastoma growth inhibition by hedgehog pathway blockade Science 297 1559 1561
86. JT Romer H Kimura S Magdaleno K Sasai C Fuller H Baines, et al. 2004 Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice Cancer Cell 6 229 240
87. JB Rubin AL Kung RS Klein JA Chan Y Sun K Schmidt, et al. 2003 A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors Proc Natl Acad Sci U S A 100 13513 13518
88. RB Corcoran T Bachar Raveh MT Barakat EY Lee MP Scott 2008 Insulin-like growth factor 2 is required for progression to advanced medulloblastoma in patched1 heterozygous mice Cancer Res 68 8788 8795
89. RB Corcoran MP Scott 2006 Oxysterols stimulate Sonic hedgehog signal transduction and proliferation of medulloblastoma cells Proc Natl Acad Sci U S A 103 8408 8413
90. MR Grimmer WA Weiss 2008 BMPs oppose Math1 in cerebellar development and in medulloblastoma Genes Dev 22 693 699
91. SM Duplan Y Theoret RL Kenigsberg 2002 Antitumor activity of fibroblast growth factors (FGFs) for medulloblastoma may correlate with FGF receptor expression and tumor variant Clin Cancer Res 8 246 257
92. P Vachon C Girard Y Theoret 2004 Effects of basic fibroblastic growth factor on the growth of human medulloblastoma xenografts J Neurooncol 67 139 146
93. R Rohatgi L Milenkovic MP Scott 2007 Patched1 regulates hedgehog signaling at the primary cilium Science 317 372 376
94. VV Chizhikov J Davenport Q Zhang EK Shih OA Cabello JL Fuchs, et al. 2007 Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool J Neurosci 27 9780 9789
95. N Spassky YG Han A Aguilar L Strehl L Besse C Laclef, et al. 2008 Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool Dev Biol 317 246 259
96. KJ Millen JG Gleeson 2008 Cerebellar development and disease Curr Opin Neurobiol 18 12 19
97. CM Louie JG Gleeson 2005 Genetic basis of Joubert syndrome and related disorders of cerebellar development Hum Mol Genet 14 Spec No. 2 R235 R242
98. J Aruga 2004 The role of Zic genes in neural development Mol Cell Neurosci 26 205 221
99. ML Latash DM Corcos 1991 Kinematic and electromyographic characteristics of single-joint movements of individuals with Down syndrome Am J Ment Retard 96 189 201
100. RX Moldrich L Dauphinot J Laffaire J Rossier MC Potier 2007 Down syndrome gene dosage imbalance on cerebellum development Prog Neurobiol 82 87 94
101. RJ Roper LL Baxter NG Saran DK Klinedinst PA Beachy RH Reeves 2006 Defective cerebellar response to mitogenic Hedgehog signaling in Down [corrected] syndrome mice Proc Natl Acad Sci U S A 103 1452 1456
102. GD Dakubo ST Beug CJ Mazerolle S Thurig Y Wang VA Wallace 2008 Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells Brain Res 1228 27 42
103. F Charron E Stein J Jeong AP McMahon M Tessier-Lavigne 2003 The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance Cell 113 11 23
104. PL So PK Yip S Bunting LF Wong ND Mazarakis S Hall, et al. 2006 Interactions between retinoic acid, nerve growth factor and sonic hedgehog signalling pathways in neurite outgrowth Dev Biol 298 167 175