Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning

Genes and Development

Volumn 26, Issue 24, 2012, Pages 2802-2816

  Peterson, Kevin A ^a,m   Nishi, Yuichi ^a,m   Ma, Wenxiu ^b   Vedenko, Anastasia ^c,d   Shokri, Leila ^c,d   Zhang, Xiaoxiao ^e   McFarlane, Matthew ^e   Baizabal, José Manuel ^a   Junker, Jan Philipp ^f   van Oudenaarden, Alexander ^f,g,h   Mikkelsen, Tarjei ^f,i   Bernstein, Bradley E ^j   Bailey, Timothy L ^k   Bulyk, Martha L ^c,d   Wong, Wing H ^l   McMahon, Andrew P ^a,e,i,m  

^a Harvard University   (United States)

^b Stanford University   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HARVARD UNIVERSITY   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^h UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

ⁱ HARVARD STEM CELL INSTITUTE   (United States)

^j MASSACHUSETTS GENERAL HOSPITAL   (United States)

^k UNIVERSITY OF QUEENSLAND   (Australia)

^l STANFORD UNIVERSITY   (United States)

^m UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

more..

Author keywords

Gli; Morphogen; Neural tube patterning; Shh

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR SOX2;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL FATE; CONTROLLED STUDY; DNA BINDING; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BODY PATTERNING; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, TRANSGENIC; NEURAL TUBE; PROTEIN BINDING; SOXB1 TRANSCRIPTION FACTORS;

ERINACEIDAE; MAMMALIA; MUS MUSCULUS; VERTEBRATA;

EID: 84871587536     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.207142.112     Document Type: Article

References (61)

1. Allen BL, Tenzen T, McMahon AP. 2007. The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev 21: 1244-1257.
2. Allen BL, Song JY, Izzi L, Althaus IW, Kang J-S, Charron F, Krauss RS, McMahon AP. 2011. Overlapping roles and collective requirement for the coreceptors GAS1, CDO, and BOC in SHH pathway function. Dev Cell 20: 775-787.
3. Bai CB, Stephen D, Joyner AL. 2004. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 6: 103-115.
4. Balaskas N, Ribeiro A, Panovska J, Dessaud E, Sasai N, Page KM, Briscoe J, Ribes V. 2012. Gene regulatory logic for reading the sonic hedgehog signaling gradient in the vertebrate neural tube. Cell 148: 273-284.
5. Berger MF, Bulyk ML. 2009. Universal protein-binding microarrays for the comprehensive characterization of the DNAbinding specificities of transcription factors. Nat Protoc 4: 393-411.
6. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW III, Bulyk ML. 2006. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol 24: 1429-1435.
7. Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J. 2011. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 25: 2453-2464.
8. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
9. Briscoe J, Pierani A, Jessell TM, Ericson J. 2000. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101: 435-445.
10. Bylund M, Andersson E, Novitch BG, Muhr J. 2003. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6: 1162-1168.
11. Chamberlain CE, Jeong J, Guo C, Allen BL, McMahon AP. 2008. Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning. Development 135: 1097-1106.
12. Chen JK, Taipale J, Young KE, Maiti T, Beachy PA. 2002. Small molecule modulation of Smoothened activity. Proc Natl Acad Sci 99: 14071-14076.
13. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
14. Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, Mynett A, Novitch BG, Briscoe J. 2007. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450: 717-720.
15. Dessaud E, McMahon AP, Briscoe J. 2008. Pattern formation in the vertebrate neural tube: A sonic hedgehog morphogen-regulated transcriptional network. Development 135: 2489-2503.
16. Dessaud E, Ribes V, Balaskas N, Yang LL, Pierani A, Kicheva A, Novitch BG, Briscoe J, Sasai N. 2010. Dynamic assignment and maintenance of positional identity in the ventral neural tube by the morphogen Sonic Hedgehog. PLoS Biol 8: e1000382. doi: 10.1371/journal.pbio.1000382.
17. Ding Q, Motoyama J, Gasca S, Mo R, Sasaki H, Rossant J, Hui CC. 1998. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125: 2533-2543.
18. Epstein DJ, McMahon AP, Joyner AL. 1999. Regionalization of Sonic hedgehog transcription along the anteroposterior axis of the mouse central nervous system is regulated by Hnf3-dependent and-independent mechanisms. Development 126: 281-292.
19. Gaudet J, Mango SE. 2002. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295: 821-825.
20. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP. 1996. Conservation of the hedgehog/patched signaling pathway from flies to mice: Induction of a mouse patched gene by Hedgehog. Genes Dev 10: 301-312.
21. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
22. Gritli-Linde A, Lewis P, McMahon AP, Linde A. 2001. The whereabouts of a morphogen: Direct evidence for short-and graded long-range activity of hedgehog signaling peptides. Dev Biol 236: 364-386.
23. Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E, Taipale J. 2006. Genome-wide prediction of mammalian enhancers based on analysis of transcriptionfactor binding affinity. Cell 124: 47-59.
24. Jeong J, McMahon AP. 2005. 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: 143-154.
25. Jessell TM. 2000. Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
26. Jiang J, Levine M. 1993. Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72: 741-752.
27. Kinzler KW, Vogelstein B. 1990. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol Cell Biol 10: 634-642.
28. Lei Q, Jeong Y, Misra K, Li S, Zelman AK, Epstein DJ, Matise MP. 2006. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev Cell 11: 325-337.
29. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, Oostra BA, Goode D, Elgar G, Hill RE, de Graaff E. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12: 1725-1735.
30. Ma W, Wong WH. 2011. The analysis of ChIP-seq data. Methods Enzymol 497: 51-73.
31. Marti E, Bumcrot DA, Takada R, McMahon AP. 1995. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375: 322-325.
32. Martinelli DC, Fan CM. 2007. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev 21: 1231-1243.
33. Matise MP, Epstein DJ, Park HL, Platt KA, Joyner AL. 1998. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125: 2759-2770.
34. Mavromatakis YE, Lin W, Metzakopian E, Ferri AL, Yan CH, Sasaki H, Whisett J, Ang SL. 2011. Foxa1 and Foxa2 positively and negatively regulate Shh signalling to specify ventral midbrain progenitor identity. Mech Dev 128: 90-103.
35. Metzakopian E, Lin W, Salmon-Divon M, Dvinge H, Andersson E, Ericson J, Perlmann T, Whitsett JA, Bertone P, Ang SL. 2012. Genome-wide characterization of Foxa2 targets reveals upregulation of floor plate genes and repression of ventrolateral genes in midbrain dopaminergic progenitors. Development 139: 2625-2634.
36. Novitch BG, Chen AI, Jessell TM. 2001. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31: 773-789.
37. Novitch BG, Wichterle H, Jessell TM, Sockanathan S. 2003. A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40: 81-95.
38. Oosterveen T, Kurdija S, Alekseenko Z, Uhde CW, Bergsland M, Sandberg M, Andersson E, Dias JM, Muhr J, Ericson J. 2012. Mechanistic differences in the transcriptional interpretation of local and long-range shh morphogen signaling. Dev Cell 23: 1006-1019.
39. Pan Y, Bai CB, Joyner AL, Wang B. 2006. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol Cell Biol 26: 3365-3377.
40. Papatsenko D, Levine M. 2005. Quantitative analysis of binding motifs mediating diverse spatial readouts of the Dorsal gradient in the Drosophila embryo. Proc Natl Acad Sci 102: 4966-4971.
41. Parker DS, White MA, Ramos AI, Cohen BA, Barolo S. 2011. The cis-regulatory logic of Hedgehog gradient responses: Key roles for gli binding affinity, competition, and cooperativity. Sci Signal 4: ra38. doi: 10.1126/scisignal.2002077.
42. Persson M, Stamataki D, te Welscher P, Andersson E, Bose J, Ruther U, Ericson J, Briscoe J. 2002. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev 16: 2865-2878.
43. Pevny L, Placzek M. 2005. SOX genes and neural progenitor identity. Curr Opin Neurobiol 15: 7-13.
44. Placzek M, Briscoe J. 2005. The floor plate: Multiple cells, multiple signals. Nat Rev Neurosci 6: 230-240.
45. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
46. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877-879.
47. Ribes V, Balaskas N, Sasai N, Cruz C, Dessaud E, Cayuso J, Tozer S, Yang LL, Novitch B, Marti E, et al. 2010. Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev 24: 1186-1200.
48. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM. 1995. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81: 445-455.
49. Rowan S, Siggers T, Lachke SA, Yue Y, Bulyk ML, Maas RL. 2010. Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity. Genes Dev 24: 980-985.
50. Santagati F, Abe K, Schmidt V, Schmitt-John T, Suzuki M, Yamamura K, Imai K. 2003. Identification of cis-regulatory elements in the mouse Pax9/Nkx2-9 genomic region: Implication for evolutionary conserved synteny. Genetics 165: 235-242.
51. Sasaki H, Hui C, Nakafuku M, Kondoh H. 1997. A binding site for Gli proteins is essential for HNF-3b floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124: 1313-1322.
52. Tenzen T, Allen BL, Cole F, Kang JS, Krauss RS, McMahon AP. 2006. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev Cell 10: 647-656.
53. Thomson M, Liu SJ, Zou LN, Smith Z, Meissner A, Ramanathan S. 2011. Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145: 875-889.
54. Tsanov KM, Nishi Y, Peterson KA, Liu J, Baetscher M, McMahon AP. 2012. An embryonic stem cell-based system for rapid analysis of transcriptional enhancers. Genesis 50: 443-450.
55. Vokes SA, Ji H, McCuine S, Tenzen T, Giles S, Zhong S, Longabaugh WJ, Davidson EH, Wong WH, McMahon AP. 2007. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134: 1977-1989.
56. Vokes SA, Ji H, Wong WH, McMahon AP. 2008. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev 22: 2651-2663.
57. Wang B, Li Y. 2006. Evidence for the direct involvement of bTrCP in Gli3 protein processing. Proc Natl Acad Sci 103: 33-38.
58. Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100: 423-434.
59. Wang H, Lei Q, Oosterveen T, Ericson J, Matise MP. 2011. Tcf/Lef repressors differentially regulate Shh-Gli target gene activation thresholds to generate progenitor patterning in the developing CNS. Development 138: 3711-3721.
60. Wichterle H, Lieberam I, Porter JA, Jessell TM. 2002. Directed differentiation of embryonic stem cells into motor neurons. Cell 110: 385-397.
61. Wijgerde M, McMahon JA, Rule M, McMahon AP. 2002. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev 16: 2849-2864.