Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression

Development

Volumn 135, Issue 2, 2008, Pages 237-247

  Alvarez Medina, Roberto ^a   Cayuso, Jordi ^a   Okubo, Tadashi ^b   Takada, Shinji ^b   Martí, Elisa ^a  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b NATIONAL INSTITUTES OF NATURAL SCIENCES   (Japan)

Author keywords

catenin; Chick; Gli transcription factors; Gli3 locus; Hedgehog signalling; Mouse; Neural development; Pattern formation; Spinal cord; Tcf Lef1 transcription factors; Wnt canonical signalling

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; LYMPHOID ENHANCER FACTOR 1; SONIC HEDGEHOG PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR NKX6.2; UNCLASSIFIED DRUG; WNT1 PROTEIN; WNT3A PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; HEDGEHOG; IN SITU HYBRIDIZATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SPINAL CORD; TRANSCRIPTION REGULATION; TRANSGENE;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; CHICK EMBRYO; CHICKENS; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HEPATOCYTE NUCLEAR FACTOR 1-ALPHA; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NERVE TISSUE PROTEINS; NEURAL TUBE; SIGNAL TRANSDUCTION; SPINAL CORD; WNT PROTEINS;

ERINACEIDAE; VERTEBRATA;

EID: 38949091712     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.012054     Document Type: Article

References (52)

1. Abbasi, A. A., Paparidis, Z., Malik, S., Goode, D. K., Callaway, H., Elgar, G. and Grzeschick, K. H. (2007), Human Gli3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS ONE 4, 1-12.
2. Backman, M., Machon, O., Mygland, L., van den Bout, C. J., Zhong, W., Taketo, M. M. and Krauss, S. (2005). Effects of canonical Wnt signalling on dorso-ventral specification of the mouse telencephalon. Dev. Biol. 297, 155-168.
3. Bai, C. B. and Joyner, A. (2001). Gli1 can rescue the in vivo function of Gli2 Development 12, 5161-5172.
4. Bai, C. B., Stephen, D. and Joyner, A. (2004). All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 16, 103-115.
5. Borello, U., Berarducci, B., Murphy, P., Bajard, L., Buffa, V.. Piccollo, S., Buckinham, M. and Cossu, G. (2006). The Wnt/ β-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 133, 3723-3732.
6. Borycki, A., Brown, A. M. and Emerson, C. P. (2000). Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites. Development 127, 2075-2087.
7. Briscoe, J. and Ericson, J. (2001). Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49.
8. Brudno, M., Malde, S., Poliakov, A., Do, C. B., Couronne, O., Dubchak, I. and Batzoglou, S. (2003). Global alignment: finding rearrangements during alignment. Bioinformatics 19 Suppl. 1, i54-i62.
9. Burstyn-Cohen, T., Stanleigh, J., Sela-Donefeld, D. and Kalcheim, C. (2004). Canonical Wnt activity regulates trunk neural crest delamination linking BMP/Noggin signalling to G1/S transition. Development 131, 5327-5339.
10. Cayuso, J. and Martí, E. (2005). Morphogens in motion: growth control of the neural tube. J. Neurobiol. 64, 376-387.
11. Cayuso, J., Ulloa, F., Cox, B., Briscoe, J. and Martí, E. (2006). The Sonic hedgehog pathway independently controls the patterning proliferation and survival of neuroepithelial cells by regulating Gli activity. Development 133, 517-528.
12. Chesnutt, C., Burrus, L. W., Brown, A. M. and Niswander, L. (2004). Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev. Biol. 274, 334-347.
13. Dickinson, M. E., Krumlauf, R. and McMahon, A. P. (1994). Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development 120, 1453-1471.
14. Epstein, D. J., Martí, E., Scott, M. P. and McMahon, A. (1996). Antagonizing cAMP-dependent protein kinase A in the dorsal CNS activates a conserved Sonic hedgehog signaling pathway. Development 122, 2885-2894.
15. García-Campmany, L. and Marti, E. (2007). The TGFβ-intracellular effector Smad3 regulates neuronal differentiation and cell fate decisions in the developing spinal cord. Development 134, 65-75.
16. Gunhaga, L., Marklund, M., Sjodal, M., Hsieh, J., Jessell, T. M. and Edlund, T. (2003). Specification of dorsal telencephalic character by sequential Wnt and FGF signalling. Nat. Neurosci. 6, 701-707.
17. Hallikas, O., Palin, K., Sinjushina, N., Rauriainen, R., Partanen, R., Ukkonen, E. and Taipale, J. (2006). Genome-wide prediction of mammalian enhancers based on analisis of transcription factor binding affinity. Cell 124, 47-59.
18. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of chick embryo. J. Morphol. 88, 49-92.
19. Helms, A. W. and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 1, 42-49.
20. Hollyday, M., McMahon, J. A. and McMahon, A. P. (1995). Wnt expression patterns in chick embryo nervous system. Mech. Dev. 1, 9-25.
21. Ille, F., Atanasoski, S., Falk, S., Ittner, L. M., Märid, D., Büchmann-Møller, S., Wurdak, H., Suter, U., Taketo, M. M. and Sommer. L. (2007). Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev. Biol. 304, 394-408.
22. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
23. Jacob, J. and Briscoe, J. (2003). Gli proteins and the control of spinal-cord patterning. EMBO Rep. 4, 761-765.
24. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
25. Kim, C. H., Oda, T., Itoh, M., Jiang, D., Artinger, K. B., Chandrasekharappa, S. C., Driever, W. and Chitnis, A. B. (2000). Repressor activity of Headless(Tcf3 is essential for vertebrate head formation. Nature 407, 913-916.
26. Korinek, V., Barker, N., Willert, K., Molenaar, M, Roose, J., Wagenaar, G., Markman, M., Lamers, W., Destree, O. and Clevers, H. (1998). Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol. Cell. Biol. 18, 1248-1256.
27. Lei, Q., Jeong, Y., Misra, K., Li, S., Zelman, A. K., Epstein, D. J. and Matise, M. P. (2006). Wnt signalling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signalling in the neural tube. Dev. Cell 11, 325-337.
28. Litingtung, Y. and Chiang, C. (2000). Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3, 979-985.
29. Liu, A. and Niswander, L. (2005). Bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev. Neurosci. 6, 945-954.
30. Liu, F., van den Broek, O., Destrée, O. and Hoppler, S. (2005). Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/{beta}-catenin signalling in mesoderm development. Development 132, 5375-5385.
31. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
32. Lum, L. and Beachy, P. A. (2004). The Hedgehog response network: sensors, switches, and routers. Science 304, 1755-1759.
33. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/beta-catenin signalling during mouse development and colorectal tumors. Proc. Natl. Acad. Sci USA 100, 3299-3304.
34. Marti, E., Garcia-Campmany, L. and Bovolenta, P. (2005). Dorso-ventral patterning of the vertebrate nervous system. In Cell Signalling and Growth Factors in Development (ed. K. Unsicke and K. Kligestein), pp. 361-394. Weinheim: Wiley-VCH.
35. Matise, M. P. and Joyner, A. L. (1999). Gli genes in development and cancer. Oncogene 18, 7852-7859.
36. Mayor, C., Brudno, M., Schwartz, J. R., Poliakov, A., Rubin, E. M., Frazer, K. A., Pachter, L. S. and Dubchak, I. (2000). VISTA: visualization global DNA sequence alignments of arbitrary length. Bioinformatics 16, 1046-1047.
37. Megason, S. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
38. Muroyama, Y., Fujihara, M., Ikeya, M., Kondoh, H. and Takada, S. (2002). Wnt signalling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16, 548-553.
39. Parr, B. A., Shea, M. J., Vassileva, G. and McMahon, A. P. (1993). Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247-261.
40. Persson, M., Stamataki, D., Weischer, P., Anderson, E., Bose, J., Ruther U., Ericson, J. and Briscoe, J. (2002). Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16, 2865-2878.
41. Ramón, Y and Cajal, S. (1911). Histologia du system nerveux de l'home et des vertebrats. Vols 1/2, Paris. [Reprinted Cajal, Madrid: Consejo Superior de Investigaciones Cientificas, Inst. 1955.]
42. Riccomagno, M. M., Takada, S. and Epstein, D. J. (2005). Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev. 19, 1612-1623.
43. Robertson, C. P., Braun, M. M. and Roelink, H. (2004). Sonic hedgehog patterning in chick neural plate is antagonized by a Wnt3-like signal. Dev. Dyn. 229, 10-519.
44. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322.
45. Schmidt, M., Patterson, M., Farrell, E. and Munsterberg, A. (2004). Dynamic expression of Lef/Tcf family members and beta-catenin during chick gastrulation, neurulation, and early limb development. Dev. Dyn. 229, 703-707.
46. Stamataki, D., Ulloa, F., Tsoni, S. V., Mynnet, A. and Briscoe, J. (2005). A gradient of Gli activity mediates graded Sonic hedgehog signalling in the neural tube. Genes Dev. 19, 626-641.
47. Sun, T., Echelard, Y., Lu, R., Yuk, D. I., Kaing, S., Stiles, C. D. and Rowitch, D. H. (2001). Olig bHLH proteins interact with homeodomain proteins to regulate cell fate acquisition in progenitors of the ventral neural tube. Curr. Biol. 11, 1413-1420.
48. Tetsu, O. and McCormick, F. (1999). Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
49. Uchikawa, M., Ishida, Y., Takemoto, T., Kamachi, Y. and Kondoh, H. (2003). Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammlas. Dev. Cell 4, 509-519.
50. Ulloa, F., Itasaki, N. and Briscoe, J. (2007). Inhibitory Gli3 activity negatively regulates Wnt/b-Catenin signalling. Curr. Biol. 17, 545-550.
51. Van de Wetering, M., Oosterwegel, M., Dooijes, D. and Clevers, H. (1991). Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing sequence-specific HMG box. EMBO J. 10, 123-132.
52. Zechner, D., Fujita, Y., Hulsken, J., Muller, T., Walter, I., Taketo, M. M., Crenshaw, E. B., Birchmeier, W. and Birchmeier, C. (2003). β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258, 406-418.