Mechanistic Differences in the Transcriptional Interpretation of Local and Long-Range Shh Morphogen Signaling

Developmental Cell

Volumn 23, Issue 5, 2012, Pages 1006-1019

  Oosterveen, Tony ^a   Kurdija, Sanja ^a   Alekseenko, Zhanna ^a   Uhde, Christopher W ^a   Bergsland, Maria ^b   Sandberg, Magnus ^a,b   Andersson, Elisabet ^a   Dias, José M ^a   Muhr, Jonas ^a,b   Ericson, Johan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; MORPHOGEN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NEUROGENESIS; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 84869032400     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.09.015     Document Type: Article

References (42)

1. Agren M., Kogerman P., Kleman M.I., Wessling M., Toftgård R. Expression of the PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 2004, 330:101-114.
2. Alexandre C., Jacinto A., Ingham P.W. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 1996, 10:2003-2013.
3. Bai C.B., Stephen D., Joyner A.L. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 2004, 6:103-115.
4. Bailey P.J., Klos J.M., Andersson E., Karlén M., Källström M., Ponjavic J., Muhr J., Lenhard B., Sandelin A., Ericson J. A global genomic transcriptional code associated with CNS-expressed genes. Exp. Cell Res. 2006, 312:3108-3119.
5. Balaskas N., Ribeiro A., Panovska J., Dessaud E., Sasai N., Page K.M., Briscoe J., Ribes V. Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 2012, 148:273-284.
6. Bergsland M., Ramsköld D., Zaouter C., Klum S., Sandberg R., Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev. 2011, 25:2453-2464.
7. Briscoe J., Pierani A., Jessell T.M., Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 2000, 101:435-445.
8. 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 2001, 7:1279-1291.
9. Brody T., Rasband W., Baler K., Kuzin A., Kundu M., Odenwald W.F. cis-Decoder discovers constellations of conserved DNA sequences shared among tissue-specific enhancers. Genome Biol. 2007, 8:R75.
10. Davidson E.H. Emerging properties of animal gene regulatory networks. Nature 2010, 468:911-920.
11. Dessaud E., Yang L.L., Hill K., Cox B., Ulloa F., Ribeiro A., Mynett A., Novitch B.G., Briscoe J. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 2007, 450:717-720.
12. Dessaud E., McMahon A.P., Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 2008, 135:2489-2503.
13. Gustafsson M.K., Pan H., Pinney D.F., Liu Y., Lewandowski A., Epstein D.J., Emerson C.P. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 2002, 16:114-126.
14. Hallikas O., Palin K., Sinjushina N., Rautiainen R., Partanen J., Ukkonen E., Taipale J. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 2006, 124:47-59.
15. Hepker J., Wang Q.T., Motzny C.K., Holmgren R., Orenic T.V. Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development 1997, 124:549-558.
16. Ingham P.W., Placzek M. Orchestrating ontogenesis: variations on a theme by sonic hedgehog. Nat. Rev. Genet. 2006, 7:841-850.
17. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
18. Kamachi Y., Uchikawa M., Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 2000, 16:182-187.
19. Lander A.D. Morpheus unbound: reimagining the morphogen gradient. Cell 2007, 26:245-256.
20. Lei Q., Zelman A.K., Kuang E., Li S., Matise M.P. Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 2004, 131:3593-3604.
21. Lei Q., Jeong Y., Misra K., Li S., Zelman A.K., Epstein D.J., Matise M.P. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev. Cell 2006, 11:325-337.
22. Lek M., Dias J.M., Marklund U., Uhde C.W., Kurdija S., Lei Q., Sussel L., Rubenstein J.L., Matise M.P., Arnold H.H., et al. A homeodomain feedback circuit underlies step-function interpretation of a Shh morphogen gradient during ventral neural patterning. Development 2010, 137:4051-4060.
23. Liu Y., Helms A.W., Johnson J.E. Distinct activities of Msx1 and Msx3 in dorsal neural tube development. Development 2004, 131:1017-1028.
24. Marigo V., Tabin C.J. Regulation of patched by sonic hedgehog in the developing neural tube. Proc. Natl. Acad. Sci. USA 1996, 93:9346-9351.
25. Muhr J., Andersson E., Persson M., Jessell T.M., Ericson J. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 2001, 104:861-873.
26. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 2001, 31:773-789.
27. Ochoa-Espinosa A., Yucel G., Kaplan L., Pare A., Pura N., Oberstein A., Papatsenko D., Small S. The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc. Natl. Acad. Sci. USA 2005, 102:4960-4965.
28. Ovcharenko I., Nobrega M.A., Loots G.G., Stubbs L. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 2004, 32(Web Server issue):W280-W286.
29. Pan Y., Bai C.B., Joyner A.L., Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol. 2006, 26:3365-3377.
30. Parker D.S., White M.A., Ramos A.I., Cohen B.A., Barolo S. The cis-regulatory logic of Hedgehog gradient responses: key roles for gli binding affinity, competition, and cooperativity. Sci. Signal. 2011, 4:ra38.
31. Pavletich N.P., Pabo C.O. Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 1993, 261:1701-1707.
32. Persson M., Stamataki D., te Welscher P., Andersson E., Böse J., Rüther U., Ericson J., Briscoe J. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 2002, 16:2865-2878.
33. Saitsu H., Komada M., Suzuki M., Nakayama R., Motoyama J., Shiota K., Ishibashi M. Expression of the mouse Fgf15 gene is directly initiated by Sonic hedgehog signaling in the diencephalon and midbrain. Dev. Dyn. 2005, 232:282-292.
34. Sasaki H., Hui C., Nakafuku M., Kondoh H. 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 1997, 124:1313-1322.
35. Schaeren-Wiemers N., Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 1993, 100:431-440.
36. Stamataki D., Ulloa F., Tsoni S.V., Mynett A., Briscoe J. A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev. 2005, 19:626-641.
37. Stathopoulos A., Levine M. Genomic regulatory networks and animal development. Dev. Cell 2005, 9:449-462.
38. Vallstedt A., Muhr J., Pattyn A., Pierani A., Mendelsohn M., Sander M., Jessell T.M., Ericson J. Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 2001, 31:743-755.
39. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J., Davidson E.H., Wong W.H., McMahon A.P. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 2007, 134:1977-1989.
40. Vokes S.A., Ji H., Wong W.H., McMahon A.P. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 2008, 22:2651-2663.
41. Wijgerde M., McMahon J.A., Rule M., McMahon A.P. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 2002, 16:2849-2864.
42. Xie J., Murone M., Luoh S.M., Ryan A., Gu Q., Zhang C., Bonifas J.M., Lam C.W., Hynes M., Goddard A., et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998, 391:90-92.