A predictive model of bifunctional transcription factor signaling during embryonic tissue patterning

Developmental Cell

Volumn 31, Issue 4, 2014, Pages 448-460

  Junker, JanPhilipp ^a,b   Peterson, Kevin A ^c   Nishi, Yuichi ^c   Mao, Junhao ^d   McMahon, Andrew P ^c   van Oudenaarden, Alexander ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; CELL SURFACE RECEPTOR; GLI PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; PATCHED RECEPTORS;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONAL TISSUE; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; TISSUE CHARACTERIZATION; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VALIDATION STUDY; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

ERINACEIDAE; MAMMALIA; VERTEBRATA;

ANIMALS; BODY PATTERNING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NERVE TISSUE PROTEINS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84921276165     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.017     Document Type: Article

References (45)

1. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
2. Bai C.B., Auerbach W., Lee J.S., Stephen D., Joyner A.L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002, 129:4753-4761.
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. 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.
5. Barolo S., Posakony J.W. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev. 2002, 16:1167-1181.
6. Bénazet J.-D., Zeller R. Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb. Perspect. Biol. 2009, 1:a001339.
7. Bintu L., Buchler N.E., Garcia H.G., Gerland U., Hwa T., Kondev J., Phillips R. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 2005, 15:116-124.
8. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 2012, 28:276-284.
9. Cadigan K.M., Waterman M.L. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb. Perspect. Biol. 2012, 4. a007906-a007906.
10. Chen J.K., Taipale J., Young K.E., Maiti T., Beachy P.A. Small molecule modulation of Smoothened activity. Proc. Natl. Acad. Sci. USA 2002, 99:14071-14076.
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. 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.
14. Haskel-Ittah M., Ben-Zvi D., Branski-Arieli M., Schejter E.D., Shilo B.-Z., Barkai N. Self-organized shuttling: generating sharp dorsoventral polarity in the early Drosophila embryo. Cell 2012, 150:1016-1028.
15. Hui C.-C., Angers S. Gli proteins in development and disease. Annu. Rev. Cell Dev. Biol. 2011, 27:513-537.
16. Itzkovitz S., Lyubimova A., Blat I.C., Maynard M., van Es J., Lees J., Jacks T., Clevers H., van Oudenaarden A. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat. Cell Biol. 2012, 14:106-114.
17. Jeong J., 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 2005, 132:143-154.
18. Kaplan S., Bren A., Zaslaver A., Dekel E., Alon U. Diverse two-dimensional input functions control bacterial sugar genes. Mol. Cell 2008, 29:786-792.
19. Kim H.D., O'Shea E.K. A quantitative model of transcription factor-activated gene expression. Nat. Struct. Mol. Biol. 2008, 15:1192-1198.
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. Levine M. Transcriptional enhancers in animal development and evolution. Curr. Biol. 2010, 20:R754-R763.
22. Mao J., Barrow J., McMahon J., Vaughan J., McMahon A.P. An ES cell system for rapid, spatial and temporal analysis of gene function invitro and invivo. Nucleic Acids Res. 2005, 33:e155.
23. 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 2002, 13:58-61.
24. Merrill B.J., Pasolli H.A., Polak L., Rendl M., García-García M.J., Anderson K.V., Fuchs E. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 2004, 131:263-274.
25. 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., et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 1997, 124:113-123.
26. Motoyama J., Heng H., Crackower M.A., Takabatake T., Takeshima K., Tsui L.-C., Hui C. Overlapping and non-overlapping Ptch2 expression with Shh during mouse embryogenesis. Mech. Dev. 1998, 78:81-84.
27. Müller B., Basler K. The repressor and activator forms of Cubitus interruptus control Hedgehog target genes through common generic gli-binding sites. Development 2000, 127:2999-3007.
28. Oosterveen T., Kurdija S., Alekseenko Z., Uhde C.W., Bergsland M., Sandberg M., Andersson E., Dias J.M., Muhr J., Ericson J. Mechanistic differences in the transcriptional interpretation of local and long-range Shh morphogen signaling. Dev. Cell 2012, 23:1006-1019.
29. Oosterveen T., Kurdija S., Ensterö M., Uhde C.W., Bergsland M., Sandberg M., Sandberg R., Muhr J., Ericson J. SoxB1-driven transcriptional network underlies neural-specific interpretation of morphogen signals. Proc. Natl. Acad. Sci. USA 2013, 110:7330-7335.
30. 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.
31. Parker D.S., White M.A., Ramos A.I., Cohen B.A., Barolo S. Thecis-regulatory logic of Hedgehog gradient responses: key roles for gli binding affinity, competition, and cooperativity. Sci. Signal. 2011, 4:ra38.
32. Peterson K.A., Nishi Y., Ma W., Vedenko A., Shokri L., Zhang X., McFarlane M., Baizabal J.M., Junker J.P., van Oudenaarden A., et al. Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning. Genes Dev. 2012, 26:2802-2816.
33. Raj A., van den Bogaard P., Rifkin S.A., van Oudenaarden A., Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 2008, 5:877-879.
34. Ribes V., Balaskas N., Sasai N., Cruz C., Dessaud E., Cayuso J., Tozer S., Yang L.L., Novitch B., Martí E., Briscoe J. Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev. 2010, 24:1186-1200.
35. 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 invitro. Development 1997, 124:1313-1322.
36. Segal E., Raveh-Sadka T., Schroeder M., Unnerstall U., Gaul U. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 2008, 451:535-540.
37. Setty Y., Mayo A.E., Surette M.G., Alon U. Detailed map of acis-regulatory input function. Proc. Natl. Acad. Sci. USA 2003, 100:7702-7707.
38. Sherman M.S., Cohen B.A. Thermodynamic state ensemble models ofcis-regulation. PLoS Comput. Biol. 2012, 8:e1002407.
39. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
40. 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.
41. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J.R., 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.
42. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
43. Zhang X.M., Ramalho-Santos M., McMahon A.P. Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node. Cell 2001, 106:781-792.
44. Zinzen R.P., Senger K., Levine M., Papatsenko D. Computational models for neurogenic gene expression in the Drosophila embryo. Curr. Biol. 2006, 16:1358-1365.
45. Zinzen R.P., Girardot C., Gagneur J., Braun M., Furlong E.E.M. Combinatorial binding predicts spatio-temporalcis-regulatory activity. Nature 2009, 462:65-70.