Wnt Signaling Inhibitors Regulate the Transcriptional Response to Morphogenetic Shh-Gli Signaling in the Neural Tube

Developmental Cell

Volumn 11, Issue 3, 2006, Pages 325-337

  Lei, Qiubo ^a   Jeong, Yongsu ^b   Misra, Kamana ^a   Li, Shike ^a   Zelman, Alice K ^a   Epstein, Douglas J ^b   Matise, Michael P ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

DEVBIO

Indexed keywords

REPRESSOR PROTEIN; SONIC HEDGEHOG PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; GENETIC DIFFERENCE; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SPINAL CORD VENTRAL HORN; STEM CELL; TRANSCRIPTION REGULATION;

ANIMALS; BIOLOGICAL MARKERS; CENTRAL NERVOUS SYSTEM; CHICKENS; CONSERVED SEQUENCE; ENHANCER ELEMENTS (GENETICS); EYE PROTEINS; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; INTEGRIN ALPHA3; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; WNT PROTEINS;

EID: 33747833061     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.06.013     Document Type: Article

References (46)

1. Ahn S., and Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118 (2004) 505-516
2. Bai C.B., Stephen D., and Joyner A.L. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 6 (2004) 103-115
3. Brantjes H., Roose J., van De Wetering M., and Clevers H. All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 29 (2001) 1410-1419
4. Brantjes H., Barker N., van Es J., and Clevers H. TCF: Lady Justice casting the final verdict on the outcome of Wnt signalling. Biol. Chem. 383 (2002) 255-261
5. Briscoe J., and Ericson J. Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11 (2001) 43-49
6. Briscoe J., Sussel L., Serup P., Hartigan-O'Connor D., Jessell T.M., Rubenstein J.L., and Ericson J. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398 (1999) 622-627
7. Briscoe J., Pierani A., Jessell T.M., and Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000) 435-445
8. Burrill J.D., Moran L., Goulding M.D., and Sauressig H. PAX2 is expressed in multiple spinal cord interneurons including a population of EN1+ interneurons that require PAX6 for their development. Development 124 (1997) 4493-4503
9. Cho E.A., and Dressler G.R. TCF-4 binds β-catenin and is expressed in distinct regions of the embryonic brain and limbs. Mech. Dev. 77 (1998) 9-18
10. Ericson J., Morton S., Kawakami A., Roelink H., and Jessell T.M. Two critical periods of sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87 (1996) 661-673
11. Ericson J., Briscoe J., Rashbass P., van Heyningen V., and Jessell T.M. Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 62 (1997) 451-466
12. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heynigen V., Jessell T.M., and Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90 (1997) 169-180
13. Galli L.M., Barnes T., Cheng T., Acosta L., Anglade A., Willert K., Nusse R., and Burrus L.W. Differential inhibition of Wnt-3a by Sfrp-1, Sfrp-2, and Sfrp-3. Dev. Dyn. 235 (2006) 681-690
14. Gritli-Linde A., Lewis P., McMahon A.P., and 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
15. Gustafsson M.K., Pan H., Pinney D.F., Liu Y., Lewandowski A., Epstein D.J., and Emerson Jr. C.P. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 16 (2002) 114-126
16. Hallikas O., Palin K., Sinjushina N., Rautiainen R., Partanen J., Ukkonen E., and Taipale J. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124 (2006) 47-59
17. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., and Tabin C.J. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118 (2004) 517-528
18. Hurlstone A., and Clevers H. T-cell factors: turn-ons and turn-offs. EMBO J. 21 (2002) 2303-2311
19. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15 (2001) 3059-3087
20. Jeong J., and McMahon A.P. Growth and pattern of the mammalian neural tube are governed by partially overlapping feedback activities of the hedgehog antagonists patched 1 and Hhip1. Development 132 (2005) 143-154
21. Jeong Y., and Epstein D.J. Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130 (2003) 3891-3902
22. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
23. Kawano Y., and Kypta R. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116 (2003) 2627-2634
24. Kim A.S., Anderson S.A., Rubenstein J.L., Lowenstein D.H., and Pleasure S.J. Pax-6 regulates expression of SFRP-2 and Wnt-7b in the developing CNS. J. Neurosci. 21 (2001) RC132
25. Kinzler K.W., and Vogelstein B. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol. 10 (1990) 634-642
26. Lee C.S., Buttitta L.A., May N.R., Kispert A., and Fan C.M. SHH-N upregulates Sfrp2 to mediate its competitive interaction with WNT1 and WNT4 in the somitic mesoderm. Development 127 (2000) 109-118
27. Lee S.-K., and Pfaff S.L. Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 4 (2001) 1183-1191
28. Lei Q., Zelman A.K., Kuang E., Li S., and Matise M.P. Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 131 (2004) 3593-3604
29. Leimeister C., Bach A., and Gessler M. Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech. Dev. 75 (1998) 29-42
30. Matise M.P., Epstein D.J., Park H.L., Platt K.A., and 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
31. McMahon A.P., Ingham P.W., and Tabin C.J. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53 (2003) 1-114
32. Megason S.G., and McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129 (2002) 2087-2098
33. Muhr J., Andersson E., Persson M., Jessell T.M., and Ericson J. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104 (2001) 861-873
34. Novitch B.G., Chen A.I., and Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31 (2001) 773-789
35. Novitch B.G., Wichterle H., Jessell T.M., and Sockanathan S. A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40 (2003) 81-95
36. Nusse R. WNT targets. Repression and activation. Trends Genet. 15 (1999) 1-3
37. Roelink H., Augsburger A., Heemskerk J., Korzh V., Norlin S., Ruiz i Altaba A., Tanabe Y., Placzek M., Edlund T., Jessell T.M., and Dodd J. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76 (1994) 761-775
38. Ruiz i Altaba A. Gli proteins and Hedgehog signaling: development and cancer. Trends Genet. 15 (1999) 418-425
39. Sasaki H., Nishizaki Y., Hui C.-c., Nakafuku M., and Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signalling. Development 126 (1999) 3915-3924
40. Stamataki D., Ulloa F., Tsoni S.V., Mynett A., and Briscoe J. A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev. 19 (2005) 626-641
41. Takahashi M., and Osumi N. Pax6 regulates specification of ventral neurone subtypes in the hindbrain by establishing progenitor domains. Development 129 (2002) 1327-1338
42. Terry K., Magan H., Baranski M., and Burrus L.W. Sfrp-1 and sfrp-2 are expressed in overlapping and distinct domains during chick development. Mech. Dev. 97 (2000) 177-182
43. Tetsu O., and McCormick F. β-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (1999) 422-426
44. van de Wetering M., Oosterwegel M., Dooijes D., and Clevers H. Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J. 10 (1991) 123-132
45. Yee S.P., and Rigby P.W. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7 (1993) 1277-1289
46. Zhu A.J., and Scott M.P. Incredible journey: how do developmental signals travel through tissue?. Genes Dev. 18 (2004) 2985-2997