Dorsal-ventral patterning of the neural tube: A tale of three signals

Developmental Neurobiology

Volumn 72, Issue 12, 2012, Pages 1471-1481

  Le Dréau, Gwenvael ^a   Martí, Elisa ^a  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

BMPs; Dorsal ventral patterning; Sonic Hedgehog; Vertebrate neural tube; Wnts

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ARTICLE; CENTRAL NERVOUS SYSTEM; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GLIA CELL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; SPINAL CORD; VERTEBRATE;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; HEDGEHOG PROTEINS; HUMANS; NEURAL TUBE; NEUROGENESIS; WNT PROTEINS;

EID: 84868537976     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22015     Document Type: Article

References (53)

1. Abbasi AA, Paparidis Z, Malik S, Goode DK, Callaway H, Elgar G, Grzeschik KH. 2007. Human GLI3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS One 2: e366.
2. Alvarez-Medina R, Cayuso J, Okubo T, Takada S, Marti E. 2008. Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development 135: 237-247.
3. Alvarez-Medina R, Le Dreau G, Ros M, Marti E. 2009. Hedgehog activation is required upstream of Wnt signalling to control neural progenitor proliferation. Development 136: 3301-3309.
4. Basch ML, Bronner-Fraser M, Garcia-Castro MI. 2006. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441: 218-222.
5. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. 2011. Bone morphogenetic proteins: A critical review. Cell Signal 23: 609-620.
6. Cayuso J, Ulloa F, Cox B, Briscoe J, Marti E. 2006. The Sonic hedgehog pathway independently controls the patterning, proliferation and survival of neuroepithelial cells by regulating Gli activity. Development 133: 517-528.
7. 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.
8. Chesnutt C, Burrus LW, Brown AM, Niswander L. 2004. Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev Biol 274: 334-347.
9. 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.
10. 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.
11. Dessaud E, Ribes V, Balaskas N, Yang LL, Pierani A, Kicheva A, Novitch BG, et al. 2010. Dynamic assignment and maintenance of positional identity in the ventral neural tube by the morphogen sonic hedgehog. PLoS Biol 8: e1000382.
12. Dickinson ME, Krumlauf R, McMahon AP. 1994. Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development 120: 1453-1471.
13. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K. 2003. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65-79.
14. Dudley AT, Robertson EJ. 1997. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev Dyn 208: 349-362.
15. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75: 1417-1430.
16. Feng XH, Derynck R. 2005. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21: 659-693.
17. Garcia-Campmany L, Marti E. 2007. The TGFbeta intracellular effector Smad3 regulates neuronal differentiation and cell fate specification in the developing spinal cord. Development 134: 65-75.
18. Goetz SC, Anderson KV. 2010. The primary cilium: A signalling centre during vertebrate development. Nat Rev Genet 11: 331-344.
19. Goulding MD, Chalepakis G, Deutsch U, Erselius JR, Gruss P. 1991. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10: 1135-147.
20. Hazen VM, Phan KD, Hudiburgh S, Butler SJ. 2011. Inhibitory Smads differentially regulate cell fate specification and axon dynamics in the dorsal spinal cord. Dev Biol 356: 566-575.
21. Hogan BL. 1996. Bone morphogenetic proteins in development. Curr Opin Genet Dev 6: 432-438.
22. Hollyday M, McMahon JA, McMahon AP. 1995. Wnt expression patterns in chick embryo nervous system. Mech Dev 52: 9-25.
23. Hu Q, Ueno N, Behringer RR. 2004. Restriction of BMP4 activity domains in the developing neural tube of the mouse embryo. EMBO Rep 5: 734-739.
24. Ingham PW, Nakano Y, Seger C. 2011. Mechanisms and functions of Hedgehog signalling across the metazoa. Nat Rev Genet 12: 393-406.
25. Lancaster MA, Schroth J, Gleeson JG. 2011. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat Cell Biol 13: 700-707.
26. Le Dreau G, Garcia-Campmany L, Rabadan MA, Ferronha T, Tozer S, Briscoe J, Marti E. 2012. Canonical BMP7 activity is required for the generation of discrete neuronal populations in the dorsal spinal cord. Development 139: 259-268.
27. Lee KJ, Dietrich P, Jessell TM. 2000. Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403: 734-740.
28. Lee KJ, Mendelsohn M, Jessell TM. 1998. Neuronal patterning by BMPs: A requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev 12: 3394-3407.
29. Li XJ, Zhang X, Johnson MA, Wang ZB, Lavaute T, Zhang SC. 2009. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 136: 4055-4063.
30. Liem KFJr, Tremml G, Jessell TM. 1997. A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91: 127-138.
31. Liem KFJr, Tremml G, Roelink H, Jessell TM. 1995. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82: 969-979.
32. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
33. Lyons KM, Hogan BL, Robertson EJ. 1995. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev 50: 71-83.
34. Mansouri A, Hallonet M, Gruss P. 1996. Pax genes and their roles in cell differentiation and development. Curr Opin Cell Biol 8: 851-857.
35. Marti E, Bumcrot DA, Takada R, McMahon AP. 1995a. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375: 322-325.
36. Marti E, Takada R, Bumcrot DA, Sasaki H, McMahon AP. 1995b. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121: 2537-2547.
37. Megason SG, McMahon AP. 2002. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129: 2087-2098.
38. Millonig JH, Millen KJ, Hatten ME. 2000. The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403: 764-769.
39. 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.
40. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, et al. 2000. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 97: 2626-2631.
41. Parr BA, Shea MJ, Vassileva G, McMahon AP. 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119: 247-261.
42. Pituello F, Yamada G, Gruss P. 1995. Activin A inhibits Pax-6 expression and perturbs cell differentiation in the developing spinal cord in vitro. Proc Natl Acad Sci USA 92: 6952-6956.
43. Ribes V, Briscoe J. 2009. Establishing and interpreting graded Sonic Hedgehog signaling during vertebrate neural tube patterning: The role of negative feedback. Cold Spring Harb Perspect Biol 1: a002014.
44. Robertson CP, Braun MM, Roelink H. 2004. Sonic hedgehog patterning in chick neural plate is antagonized by a Wnt3-like signal. Dev Dyn 229: 510-519.
45. 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.
46. Shi Y, Massague J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
47. Solloway MJ, Robertson EJ. 1999. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126: 1753-1768.
48. Timmer JR, Wang C, Niswander L. 2002. BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development 129: 2459-2472.
49. Ulloa F, Itasaki N, Briscoe J. 2007. Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signaling. Curr Biol 17: 545-550.
50. Wilson L, Maden M. 2005. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282: 1-13.
51. Wine-Lee L, Ahn KJ, Richardson RD, Mishina Y, Lyons KM, Crenshaw EBIII. 2004. Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. Development 131: 5393-5403.
52. Yu W, McDonnell K, Taketo MM, Bai CB. 2008. Wnt signaling determines ventral spinal cord cell fates in a time-dependent manner. Development 135: 3687-3696.
53. Zechner D, Muller T, Wende H, Walther I, Taketo MM, Crenshaw EBIII, Treier M, et al. 2007. Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev Biol 303: 181-190.