Attenuation of Notch and hedgehog signaling is required for fate specification in the spinal cord

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Huang, Peng ^a   Xiong, Fengzhu ^b   Megason, Sean G ^b   Schier, Alexander F ^a  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; CELL SURFACE RECEPTOR; PATCHED RECEPTORS;

ANALYTIC METHOD; ARTICLE; ATTENUATION; CELL ACTIVATION; CELL DIVISION; CELL FATE; CELL SPECIFICITY; CELL TRACKING; CONTROLLED STUDY; EMBRYO; IN VIVO STUDY; INTERNEURON; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHOTOCONVERTIBLE REPORTER OF SIGNALING HISTORY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINAL CORD; ZEBRA FISH; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; STEM CELL; TRANSGENIC ANIMAL;

DANIO RERIO; ERINACEIDAE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; INTERNEURONS; RECEPTORS, CELL SURFACE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELLS; ZEBRAFISH;

EID: 84864049056     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002762     Document Type: Article

References (49)

1. 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.
2. Ulloa F, Briscoe J, (2007) Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6: 2640-2649.
3. Briscoe J, Novitch BG, (2008) Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos Trans R Soc Lond B Biol Sci 363: 57-70.
4. Zhang Y, Narayan S, Geiman E, Lanuza GM, Velasquez T, et al. (2008) V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60: 84-96.
5. Yang L, Rastegar S, Strahle U, (2010) Regulatory interactions specifying Kolmer-Agduhr interneurons. Development 137: 2713-2722.
6. Schafer M, Kinzel D, Winkler C, (2007) Discontinuous organization and specification of the lateral floor plate in zebrafish. Dev Biol 301: 117-129.
7. Odenthal J, van Eeden FJ, Haffter P, Ingham PW, Nusslein-Volhard C, (2000) Two distinct cell populations in the floor plate of the zebrafish are induced by different pathways. Dev Biol 219: 350-363.
8. Schafer M, Kinzel D, Neuner C, Schartl M, Volff JN, et al. (2005) Hedgehog and retinoid signalling confines nkx2.2b expression to the lateral floor plate of the zebrafish trunk. Mech Dev 122: 43-56.
9. Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, et al. (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450: 717-720.
10. Dessaud E, Ribes V, Balaskas N, Yang LL, Pierani A, et al. (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.
11. Louvi A, Artavanis-Tsakonas S, (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7: 93-102.
12. Pierfelice T, Alberi L, Gaiano N, (2011) Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69: 840-855.
13. Kopan R, Ilagan MX, (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233.
14. Rocha SF, Lopes SS, Gossler A, Henrique D, (2009) Dll1 and Dll4 function sequentially in the retina and pV2 domain of the spinal cord to regulate neurogenesis and create cell diversity. Dev Biol 328: 54-65.
15. Marklund U, Hansson EM, Sundstrom E, de Angelis MH, Przemeck GK, et al. (2010) Domain-specific control of neurogenesis achieved through patterned regulation of Notch ligand expression. Development 137: 437-445.
16. Ramos C, Rocha S, Gaspar C, Henrique D, (2010) Two Notch ligands, Dll1 and Jag1, are differently restricted in their range of action to control neurogenesis in the mammalian spinal cord. PLoS ONE 5: e15515 doi:10.1371/journal.pone.0015515.
17. Appel B, Givan LA, Eisen JS, (2001) Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev Biol 1: 13.
18. Yeo SY, Chitnis AB, (2007) Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord. Proc Natl Acad Sci U S A 104: 5913-5918.
19. Myat A, Henrique D, Ish-Horowicz D, Lewis J, (1996) A chick homologue of Serrate and its relationship with Notch and Delta homologues during central neurogenesis. Dev Biol 174: 233-247.
20. Lindsell CE, Boulter J, diSibio G, Gossler A, Weinmaster G, (1996) Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci 8: 14-27.
21. Rabadan MA, Cayuso J, Le Dreau G, Cruz C, Barzi M, et al. (2011) Jagged2 controls the generation of motor neuron and oligodendrocyte progenitors in the ventral spinal cord. Cell Death Differ 19: 209-219.
22. Yang X, Tomita T, Wines-Samuelson M, Beglopoulos V, Tansey MG, et al. (2006) Notch1 signaling influences v2 interneuron and motor neuron development in the spinal cord. Dev Neurosci 28: 102-117.
23. Park HC, Appel B, (2003) Delta-Notch signaling regulates oligodendrocyte specification. Development 130: 3747-3755.
24. Dave RK, Ellis T, Toumpas MC, Robson JP, Julian E, et al. (2011) Sonic hedgehog and notch signaling can cooperate to regulate neurogenic divisions of neocortical progenitors. PLoS ONE 6: e14680 doi:10.1371/journal.pone.0014680.
25. Crawford TQ, Roelink H, (2007) The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling. Dev Dyn 236: 886-892.
26. Guner B, Karlstrom RO, (2007) Cloning of zebrafish nkx6.2 and a comprehensive analysis of the conserved transcriptional response to Hedgehog/Gli signaling in the zebrafish neural tube. Gene Expr Patterns 7: 596-605.
27. Jessen JR, Meng A, McFarlane RJ, Paw BH, Zon LI, et al. (1998) Modification of bacterial artificial chromosomes through chi-stimulated homologous recombination and its application in zebrafish transgenesis. Proc Natl Acad Sci U S A 95: 5121-5126.
28. Lewis KE, Eisen JS, (2003) From cells to circuits: development of the zebrafish spinal cord. Prog Neurobiol 69: 419-449.
29. Concordet JP, Lewis KE, Moore JW, Goodrich LV, Johnson RL, et al. (1996) Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122: 2835-2846.
30. Chen JK, Taipale J, Cooper MK, Beachy PA, (2002) Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 16: 2743-2748.
31. Huang P, Schier AF, (2009) Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 136: 3089-3098.
32. Bae YK, Shimizu T, Hibi M, (2005) Patterning of proneuronal and inter-proneuronal domains by hairy- and enhancer of split-related genes in zebrafish neuroectoderm. Development 132: 1375-1385.
33. Scheer N, Campos-Ortega JA, (1999) Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80: 153-158.
34. Yang T, Arslanova D, Gu Y, Augelli-Szafran C, Xia W, (2008) Quantification of gamma-secretase modulation differentiates inhibitor compound selectivity between two substrates Notch and amyloid precursor protein. Mol Brain 1: 15.
35. Park HC, Shin J, Appel B, (2004) Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling. Development 131: 5959-5969.
36. Ribes V, Balaskas N, Sasai N, Cruz C, Dessaud 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.
37. Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM, (1996) Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661-673.
38. Sanchez-Camacho C, Bovolenta P, (2009) Emerging mechanisms in morphogen-mediated axon guidance. Bioessays 31: 1013-1025.
39. Ng AN, de Jong-Curtain TA, Mawdsley DJ, White SJ, Shin J, et al. (2005) Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev Biol 286: 114-135.
40. Zhang Y, Buchholz F, Muyrers JP, Stewart AF, (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20: 123-128.
41. Wan Y, Otsuna H, Chien CB, Hansen C, (2009) An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans Vis Comput Graph 15: 1489-1496.
42. Wolff C, Roy S, Ingham PW, (2003) Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr Biol 13: 1169-1181.
43. Karlstrom RO, Talbot WS, Schier AF, (1999) Comparative synteny cloning of zebrafish you-too: mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev 13: 388-393.
44. Karlstrom RO, Tyurina OV, Kawakami A, Nishioka N, Talbot WS, et al. (2003) Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 130: 1549-1564.
45. Ke Z, Kondrichin I, Gong Z, Korzh V, (2008) Combined activity of the two Gli2 genes of zebrafish play a major role in Hedgehog signaling during zebrafish neurodevelopment. Mol Cell Neurosci 37: 388-401.
46. Tyurina OV, Guner B, Popova E, Feng J, Schier AF, et al. (2005) Zebrafish Gli3 functions as both an activator and a repressor in Hedgehog signaling. Dev Biol 277: 537-556.
47. Bernhardt RR, Patel CK, Wilson SW, Kuwada JY, (1992) Axonal trajectories and distribution of GABAergic spinal neurons in wildtype and mutant zebrafish lacking floor plate cells. J Comp Neurol 326: 263-272.
48. Wyart C, Del Bene F, Warp E, Scott EK, Trauner D, et al. (2009) Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461: 407-410.
49. Shimojo H, Ohtsuka T, Kageyama R, (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58: 52-64.