Differential requirement for Gli2 and Gli3 in ventral neural cell fate specification

Developmental Biology

Volumn 259, Issue 1, 2003, Pages 150-161

  Motoyama, Jun ^a   Milenkovic, Ljiljana ^c   Iwama, Mizuho ^a   Shikata, Yayoi ^a   Scott, Matthew P ^c   Hui, Chi Chung ^b  

^a RIKEN   (Japan)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gli2; Gli3; Mouse embryo; Mutant; Neural tube; Ptc1; Rostral caudal axis; Shh; Ventral cell fates

Indexed keywords

PROTEIN PATCHED 1; RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL FATE; CELL MATURATION; CELL TYPE; EMBRYO; FEMALE; GENE MUTATION; INTERNEURON; MALE; MOTONEURON; MOUSE; MUTANT; NERVE CELL; NEURAL TUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; TISSUE SPECIFICITY;

ERINACEIDAE;

EID: 0037706929     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(03)00159-3     Document Type: Article

References (48)

1. Aoto K., Nishimura T., Eto K., Motoyama J. Mouse GL13 regulates Fgf8 expression and apoptosis in the developing neural tube, face and limb bud. Dev. Biol. 251:2002;320-332.
2. Aza-Blanc P., Ramirez-Weber F., Laget M., Schwartz C., Kornberg T. Proteolysis that is inhibited by hedgehog targets cubitus interruptus protein to the nucleus and converts it to a repressor. Cell. 89:1997;1043-1053.
3. Aza-Blanc P., Lin H., Ruiz i Altaba A., Kornberg T. Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development. 127:2000;4293-4301.
4. Bai C.B., Auerbach W., Lee J.S., Stephan D., Joyner A.L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development. 129:2002;4753-4761.
5. Briscoe J., Chen Y., Jessell T.M., Struhl G. A Hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of Sonic hedgehog in the neural tube. Mol. Cell. 7:2001;1279-1291.
6. Buscher D., Grotewold L., Ruther U. The XtJ allele generates a Gli3 fusion transcript. Mamm. Genome. 9:1998;676-678.
7. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 383:1996;407-413.
8. Chen Y., Struhl G. Dual roles for patched in sequestering and transducing hedgehog. Cell. 87:1996;553-563.
9. Chuang C., McMahon A.P. Vertebrate Hedgehog signaling modulated by induction of a Hedgehog interacting protein. Nature. 397:1999;617-621.
10. Dai P., Akimaru H., Tanaka Y., Maekawa T., Nakafuku M., Ishii S. Sonic hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274:1999;8143-8152.
11. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C.-c. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development. 125:1998;2533-2543.
12. Echelard Y., Epstein D.J., St-Jacques B., Shen L., Mohler J., McMahon J.A., McMahon A.P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 75:1993;1417-1430.
13. Eggenschwiler J.T., Espinoza E., Anderson K.V. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature. 412:2001;194-198.
14. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., Briscoe J. Pax 6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell. 90:1997;169-180.
15. Goodrich L.V., Milenkovic L., Higgins K.M., Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science. 277:1997;1109-1113.
16. Gritli-Linde A., Lewis P., McMahon A.P., Linde A. The whereabouts of a morphogen direct evidence for short- and graded long-range activity of Hedgehog signaling peptides . Dev. Biol. 236:2001;364-386.
17. Hui C.-c., Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene . Nat. Genet. 3:1993;241-246.
18. Hui C.-c., Slusarski D., Platt K.A., Holmgren R., Joyner A.L. Expression of three mouse homologs of the Drosophila segment polarity genes cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm-and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 162:1994;402-413.
19. Hynes M., Stone D.M., Dowd M., Pitts-Meek S., Goddard A., Gurney A., Rosenthal A. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron. 19:1997;15-26.
20. Hynes M., Ye W., Wang K., Stone D., Murone M., Sauvage F., Rosenthal A. The seven-transmembrane receptor smoothened cell-autonomously induce multiple ventral cell types. Nat. Neurosci. 3:2000;41-46.
21. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development paradigms and principles . Genes Dev. 15:2001;3059-3087.
22. Ishibashi M., McMahon A.P. A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development. 129:2002;4807-4819.
23. Jessell T.M. Neuronal specification in the spinal cord inductive signals and transcriptional codes . Nat. Rev. Genet. 1:2000;20-29.
24. Litingtung Y., Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3:2000;979-985.
25. Litingtung Y., Dahn R.D., Li Y., Fallon J.F., Chiang C. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature. 418:2002;979-983.
26. Martinez-Morales J.R., Barbas J.A., Marti E., Bovolenta P., Edgar D., Rodriguez-Tebar A. Vitronectin is expressed in the ventral region of the neural tube and promotes the differentiation of motor neurons. Development. 124:1997;5139-5147.
27. Matise M.P., Epstein D.J., Park H.L., Platt K.A., Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development. 125:1998;2759-2770.
28. Maynard T.M., Jain M.D., Balmer C.W., LaMantia A.S. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm. Genome. 13:2002;58-61.
29. Methot N., Basler K. An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development. 128:2001;733-742.
30. Mo R., Freer A.M., Zinyk D.L., Crackower M.A., Michaud J., Heng H.H., Chik K.W., Shi X.M., Tsui L.C., Cheng S.H., Joyner A.L., Hui C.-c. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development. 124:1997;113-123.
31. Motoyama J., Takabatake T., Takeshima K., Hui C.-c. Ptc2, a second mouse Patched gene is co-expressed with Sonic hedgehog. Nat. Genet. 18:1998;104-106.
32. Ohkubo Y., Chiang C., Rubenstein J.L.R. Coordinate regulation and synergistic actions of Bmp4, Shh and Fgf8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience. 111:2002;1-17.
33. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.-c., Nakashima M., Joyner A.L. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development. 127:2000;1593-1605.
34. Pierani A., Brenner-Morton S., Chiang C., Jessell T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell. 97:1999;903-915.
35. Pons S., Marti E. Sonic hedgehog synergies with the extracellular matrix protein vitronectin to induce spinal motor neuron differentiation. Development. 127:2000;333-342.
36. Quirk J., van den Heuvel M., Henrique D., Marigo V., Jones T.A., Tabin C., Ingham P.W. The smoothened gene and hedgehog signal transduction in Drosophila and vertebrate development. Cold Spring Harbor Symp. Quant. Biol. 62:1997;217-226.
37. Rallu M., Machold R., Gariano N., Corbin J.G., McMahon A.P., Fishell G. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and hedgehog signaling. Development. 129:2002;4774-4963.
38. Ruiz i Altaba A. Gli proteins and Hedgehog signaling development and cancer . Trends Genet. 15:1999;418-425.
39. Sasaki H., Hui C.-c., Nakafuku M., Kondoh H. A binding site for Gli proteins is essential for Hnf3β floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development. 124:1997;1313-1322.
40. Sasaki H., Nishizaki Y., Hui C.-c., Nakafuku M., Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain implication of Gli2 and Gli3 as primary mediators of Shh signaling . Development. 126:1999;3915-3924.
41. Shin S.H., Kogerman P., Lindstrom E., Toftgard R., Biesecker L.G. GLI3 mutations in human disorders mimic Drosophila cubitus interruptus protein functions and localization. Proc. Natl. Acad. Sci. USA. 96:1999;2880-2884.
42. Stone D.M., Hynes M., Armanini M., Swanson T.A., Gu Q., Johnson R.L., Scott M.P., Pennica D., Goddard A., Phillips H., Noll M., Hooper J.E., de Sauvage F., Rosenthal A. The tumor-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature. 384:1996;129-134.
43. Taipale J., Chen J.K., Cooper M.K., Wang B., Mann R.K., Milenkovic L., Scott M.P., Beachy P.A. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature. 406:2000;1005-1009.
44. te Welscher P., Zuniga A., Kuijper S., Drenth T., Goedemans H.J., Meijlink F., Zeller R. Progression of vertebrate limb development through SHH mediated counteraction of GLI3. Science. 298:2002;827-830.
45. Theil T., Alvarez-Bolado G., Walter A., Ruther U. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development. 126:1999;3561-3571.
46. Tole S., Ragsdale C.W., Grove E.A. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes (J). Dev. Biol. 217:2000;254-265.
47. von Mering C., Basler K. Distinct and regulated activities of human Gli proteins in Drosophila. Curr. Biol. 9:1999;1319-1322.
48. Zhang X.M., Ramalho-Santos M., McMahon A.P. Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R asymmetry by the mouse node. Cell. 106:2001;781-792.