Specified neural progenitors sort to form sharp domains after noisy Shh signaling

Cell

Volumn 153, Issue 3, 2013, Pages 550-561

  Xiong, Fengzhu ^a   Tentner, Andrea R ^a   Huang, Peng ^b   Gelas, Arnaud ^a   Mosaliganti, Kishore R ^a   Souhait, Lydie ^a   Rannou, Nicolas ^a   Swinburne, Ian A ^a   Obholzer, Nikolaus D ^a   Cowgill, Paul D ^a   Schier, Alexander F ^b   Megason, Sean G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHOGEN; SONIC HEDGEHOG PROTEIN;

ARTICLE; CELL FATE; CELL MATURATION; CELL MOTION; CELL SELECTION; CELL STRUCTURE; NEURAL STEM CELL; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH;

DANIO RERIO; ERINACEIDAE;

EID: 84876939667     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.03.023     Document Type: Article

References (69)

1. S. Ahn, and A.L. Joyner Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning Cell 118 2004 505 516
2. N. Balaskas, A. Ribeiro, J. Panovska, E. Dessaud, N. Sasai, K.M. Page, J. Briscoe, and V. Ribes Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube Cell 148 2012 273 284
3. M. Catala, M.A. Teillet, E.M. De Robertis, and M.L. Le Douarin A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls Development 122 1996 2599 2610
4. C.E. Chamberlain, J. Jeong, C. Guo, B.L. Allen, and A.P. McMahon 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 2008 1097 1106
5. B. Ciruna, A. Jenny, D. Lee, M. Mlodzik, and A.F. Schier Planar cell polarity signalling couples cell division and morphogenesis during neurulation Nature 439 2006 220 224
6. J. Clarke Role of polarized cell divisions in zebrafish neural tube formation Curr. Opin. Neurobiol. 19 2009 134 138
7. R.M. Das, and K.G. Storey Mitotic spindle orientation can direct cell fate and bias Notch activity in chick neural tube EMBO Rep. 13 2012 1030
8. E. Dessaud, L.L. Yang, K. Hill, B. Cox, F. Ulloa, A. Ribeiro, A. Mynett, B.G. Novitch, and J. Briscoe Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism Nature 450 2007 717 720
9. E. Dessaud, V. Ribes, N. Balaskas, L.L. Yang, A. Pierani, A. Kicheva, B.G. Novitch, J. Briscoe, and N. Sasai Dynamic assignment and maintenance of positional identity in the ventral neural tube by the morphogen sonic hedgehog PLoS Biol. 8 2010 e1000382
10. Y. Echelard, D.J. Epstein, B. St-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity Cell 75 1993 1417 1430
11. J. Ericson, J. Briscoe, P. Rashbass, V. van Heyningen, and T.M. Jessell 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. L. Erskine, K. Patel, and J.D. Clarke Progenitor dispersal and the origin of early neuronal phenotypes in the chick embryo spinal cord Dev. Biol. 199 1998 26 41
13. H. Flanagan-Steet, M.A. Fox, D. Meyer, and J.R. Sanes Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations Development 132 2005 4471 4481
14. B.D. Harfe, P.J. Scherz, S. Nissim, H. Tian, A.P. McMahon, and C.J. Tabin Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities Cell 118 2004 517 528
15. P. Huang, F. Xiong, S.G. Megason, and A.F. Schier Attenuation of Notch and Hedgehog signaling is required for fate specification in the spinal cord PLoS Genet. 8 2012 e1002762
16. T. Inoue, S. Nakamura, and N. Osumi Fate mapping of the mouse prosencephalic neural plate Dev. Biol. 219 2000 373 383
17. J. Jeong, and A.P. McMahon 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
18. T.M. Jessell Neuronal specification in the spinal cord: inductive signals and transcriptional codes Nat. Rev. Genet. 1 2000 20 29
19. J.R. Jessen, A. Meng, R.J. McFarlane, B.H. Paw, L.I. Zon, G.R. Smith, and S. Lin Modification of bacterial artificial chromosomes through chi-stimulated homologous recombination and its application in zebrafish transgenesis Proc. Natl. Acad. Sci. USA 95 1998 5121 5126
20. R.R. Kay, and C.R. Thompson Forming patterns in development without morphogen gradients: scattered differentiation and sorting out Cold Spring Harb. Perspect. Biol. 1 2009 a001503
21. C.B. Kimmel, R.M. Warga, and D.A. Kane Cell cycles and clonal strings during formation of the zebrafish central nervous system Development 120 1994 265 276
22. V. Korzh, T. Edlund, and S. Thor Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation Development 118 1993 417 425
23. S. Krauss, J.P. Concordet, and P.W. Ingham A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos Cell 75 1993 1431 1444
24. A.D. Lander, W.C. Lo, Q. Nie, and F.Y. Wan The measure of success: constraints, objectives, and tradeoffs in morphogen-mediated patterning Cold Spring Harb. Perspect. Biol. 1 2009 a002022
25. P.A. Lawrence, J. Casal, and G. Struhl The hedgehog morphogen and gradients of cell affinity in the abdomen of Drosophila Development 126 1999 2441 2449
26. S.M. Leber, and J.R. Sanes Migratory paths of neurons and glia in the embryonic chick spinal cord J. Neurosci. 15 1995 1236 1248
27. M. Lek, J.M. Dias, U. Marklund, C.W. Uhde, S. Kurdija, Q. Lei, L. Sussel, J.L. Rubenstein, M.P. Matise, and H.H. Arnold A homeodomain feedback circuit underlies step-function interpretation of a Shh morphogen gradient during ventral neural patterning Development 137 2010 4051 4060
28. Z. Lele, A. Folchert, M. Concha, G.J. Rauch, R. Geisler, F. Rosa, S.W. Wilson, M. Hammerschmidt, and L. Bally-Cuif parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube Development 129 2002 3281 3294
29. K.E. Lewis, and J.S. Eisen From cells to circuits: development of the zebrafish spinal cord Prog. Neurobiol. 69 2003 419 449
30. J. Lin, C. Wang, and C. Redies Expression of delta-protocadherins in the spinal cord of the chicken embryo J. Comp. Neurol. 520 2012 1509 1531
31. E. Martí, R. Takada, D.A. Bumcrot, H. Sasaki, and A.P. McMahon Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo Development 121 1995 2537 2547
32. S.G. Megason, and S.E. Fraser Digitizing life at the level of the cell: high-performance laser-scanning microscopy and image analysis for in toto imaging of development Mech. Dev. 120 2003 1407 1420
33. K.R. Mosaliganti, R.R. Noche, F. Xiong, I.A. Swinburne, and S.G. Megason ACME: automated cell morphology extractor for comprehensive reconstruction of cell membranes PLoS Comput. Biol. 8 2012 e1002780
34. A. Nicol, W. Rappel, H. Levine, and W.F. Loomis Cell-sorting in aggregates of Dictyostelium discoideum J. Cell Sci. 112 1999 3923 3929
35. H.C. Park, J. Shin, and B. Appel Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling Development 131 2004 5959 5969
36. J. Paulsson Summing up the noise in gene networks Nature 427 2004 415 418
37. S.R. Price, N.V. De Marco Garcia, B. Ranscht, and T.M. Jessell Regulation of motor neuron pool sorting by differential expression of type II cadherins Cell 109 2002 205 216
38. S. Rieger, N. Senghaas, A. Walch, and R.W. Köster Cadherin-2 controls directional chain migration of cerebellar granule neurons PLoS Biol. 7 2009 e1000240
39. M. Schäfer, D. Kinzel, C. Neuner, M. Schartl, J.N. Volff, and C. Winkler Hedgehog and retinoid signalling confines nkx2.2b expression to the lateral floor plate of the zebrafish trunk Mech. Dev. 122 2005 43 56
40. G.C. Schoenwolf Cell movements driving neurulation in avian embryos Development 2 Suppl 2 1991 157 168
41. J. Shin, H.-C. Park, J.M. Topczewska, D.J. Mawdsley, and B. Appel Neural cell fate analysis in zebrafish using olig2 BAC transgenics Methods Cell Sci. 25 2003 7 14
42. A. Shkumatava, S. Fischer, F. Müller, U. Strahle, and C.J. Neumann Sonic hedgehog, secreted by amacrine cells, acts as a short-range signal to direct differentiation and lamination in the zebrafish retina Development 131 2004 3849 3858
43. J.L. Smith, and G.C. Schoenwolf Neurulation: coming to closure Trends Neurosci. 20 1997 510 517
44. M.S. Steinberg Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation Science 141 1963 401 408
45. G. Sürmeli, T. Akay, G.C. Ippolito, P.W. Tucker, and T.M. Jessell Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template Cell 147 2011 653 665
46. M. Takamiya, and J.A. Campos-Ortega Hedgehog signalling controls zebrafish neural keel morphogenesis via its level-dependent effects on neurogenesis Dev. Dyn. 235 2006 978 997
47. Y. Tanabe, C. William, and T.M. Jessell Specification of motor neuron identity by the MNR2 homeodomain protein Cell 95 1998 67 80
48. C.H. Waddington The canalization of development and the inheritance of acquired characteristics Nature 150 1942 563 565
49. B. Wendik, E. Maier, and D. Meyer Zebrafish mnx genes in endocrine and exocrine pancreas formation Dev. Biol. 268 2004 372 383
50. L. Wolpert Positional information and the spatial pattern of cellular differentiation J. Theor. Biol. 25 1969 1 47
51. Q. Xu, G. Mellitzer, V. Robinson, and D.G. Wilkinson In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins Nature 399 1999 267 271
52. T. Yamada, S.L. Pfaff, T. Edlund, and T.M. Jessell Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate Cell 73 1993 673 686
53. Y. Yamaguchi, N. Shinotsuka, K. Nonomura, K. Takemoto, K. Kuida, H. Yosida, and M. Miura Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure J. Cell Biol. 195 2011 1047 1060
54. M.D. Abramoff, P.J. Magalhaes, and S.J. Ram Image Processing with ImageJ Biophotonics Int. 11 2004 36 42
55. F. Charron, E. Stein, J. Jeong, A.P. McMahon, and M. Tessier-Lavigne The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance Cell 113 2003 11 23
56. W. Chen, S. Burgess, and N. Hopkins Analysis of the zebrafish smoothened mutant reveals conserved and divergent functions of hedgehog activity Development 128 2001 2385 2396
57. H.L. Chen, C.H. Yuh, and K.K. Wu Nestin is essential for zebrafish brain and eye development through control of progenitor cell apoptosis PLoS One 5 2010 e9318
58. K. Kawakami Transgenesis and gene trap methods in zebrafish by using the Tol2 transposable element Methods Cell Biol. 77 2004 201 222
59. C.B. Kimmel, W.W. Ballard, S.R. Kimmel, B. Ullmann, and T.F. Schilling Stages of embryonic development of the zebrafish Dev. Dyn. 203 1995 253 310
60. Y. Kimura, C. Satou, and S. Higashijima V2a and V2b neurons are generated by the final divisions of pair-producing progenitors in the zebrafish spinal cord Development 135 2008 3001 3005
61. S. Kucenas, N. Takada, H.C. Park, E. Woodruff, K. Broadie, and B. Appel CNS-derived glia ensheath peripheral nerves and mediate motor root development Nat. Neurosci. 11 2008 143 151
62. K.E. Lewis, and J.S. Eisen Hedgehog signaling is required for primary motoneuron induction in zebrafish Development 128 2001 3485 3495
63. S.G. Megason In toto imaging of embryogenesis with confocal time-lapse microscopy Methods Mol. Biol. 546 2009 317 332
64. A.N. Ng, T.A. de Jong-Curtain, D.J. Mawdsley, S.J. White, J. Shin, B. Appel, P.D. Dong, D.Y. Stainier, and J.K. Heath Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis Dev. Biol. 286 2005 114 135
65. H.C. Park, A. Mehta, J.S. Richardson, and B. Appel olig2 is required for zebrafish primary motor neuron and oligodendrocyte development Dev. Biol. 248 2002 356 368
66. H. Sasaki, C. Hui, M. Nakafuku, and H. Kondoh 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 124 1997 1313 1322
67. T. Sato, M. Takahoko, and H. Okamoto HuC:Kaede, a useful tool to label neural morphologies in networks in vivo Genesis 44 2006 136 142
68. Y. Wan, H. Otsuna, C.B. Chien, and C. Hansen An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research IEEE Trans. Vis. Comput. Graph. 15 2009 1489 1496
69. M. Westerfield, J.V. McMurray, and J.S. Eisen Identified motoneurons and their innervation of axial muscles in the zebrafish J. Neurosci. 6 1986 2267 2277