Modeling the spatio-temporal network that drives patterning in the vertebrate central nervous system

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1789, Issue 4, 2009, Pages 299-305

  Nishi, Yuichi ^a   Ji, Hongkai ^b   Wong, Wing H ^c   McMahon, Andrew P ^a,d   Vokes, Steven A ^a  

^a HARVARD UNIVERSITY   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c STANFORD UNIVERSITY   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

cis element; Development; Gene regulation; Gli; Hedgehog; Neural tube

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR;

CELL FATE; CENTRAL NERVOUS SYSTEM; DRUG DISTRIBUTION; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE REPRESSION; MODEL; NERVE CELL NETWORK; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; VERTEBRATE;

ANIMALS; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); VERTEBRATES;

ERINACEIDAE; VERTEBRATA;

EID: 64249089527     PISSN: 18749399     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2009.01.002     Document Type: Review

References (77)

1. Wilson L., and Maden M. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev. Biol. 282 (2005) 1-13
2. Marti E., Bumcrot D.A., Takada R., and McMahon A.P. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375 (1995) 322-325
3. Roelink H., Porter J.A., Chiang C., Tanabe Y., Chang D.T., Beachy P.A., and Jessell T.M. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81 (1995) 445-455
4. Briscoe J., Chen Y., Jessell T.M., and Struhl G. A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 7 (2001) 1279-1291
5. Gritli-Linde A., Lewis P., McMahon A.P., and Linde A. The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev. Biol. 236 (2001) 364-386
6. McMahon A.P., Ingham P.W., and Tabin C.J. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53 (2003) 1-114
7. Jacob J., and Briscoe J. Gli proteins and the control of spinal-cord patterning. EMBO Rep. 4 (2003) 761-765
8. Echelard Y., Epstein D.J., St-Jacques B., Shen L., Mohler J., McMahon J.A., and McMahon A.P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75 (1993) 1417-1430
9. Krauss S., Concordet J.P., and Ingham P.W. 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
10. Matise M.P., Epstein D.J., Park H.L., Platt K.A., and Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125 (1998) 2759-2770 (Cambridge, England)
11. Jeong J., and McMahon A. 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 (Cambridge, England)
12. Chamberlain C.E., Jeong J., Guo C., Allen B.L., and McMahon A.P. 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 (2008) (Cambridge, England)
13. Ericson J., Muhr J., Placzek M., Lints T., Jessell T.M., and Edlund T. Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81 (1995) 747-756
14. Goodrich L.V., Milenkovic L., Higgins K.M., and Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 (1997) 1109-1113 New York, N.Y
15. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., and Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
16. Stamataki D., Ulloa F., Tsoni S.V., Mynett A., and Briscoe J. A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev. 19 (2005) 626-641
17. Bai C.B., Stephen D., and Joyner A.L. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 6 (2004) 103-115
18. Dessaud E., Yang L.L., Hill K., Cox B., Ulloa F., Ribeiro A., Mynett A., Novitch B.G., and Briscoe J. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450 (2007) 717-720
19. Pan Y., Bai C.B., Joyner A.L., and Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol. 26 (2006) 3365-3377
20. Tempe D., Casas M., Karaz S., Blanchet-Tournier M.F., and Concordet J.P. Multisite protein kinase A and glycogen synthase kinase 3beta phosphorylation leads to Gli3 ubiquitination by SCFbetaTrCP. Mol. Cell. Biol. 26 (2006) 4316-4326
21. Aza-Blanc P., Ramirez-Weber F.A., Laget M.P., Schwartz C., and Kornberg T.B. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89 (1997) 1043-1053
22. Wang B., Fallon J.F., and Beachy P.A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100 (2000) 423-434
23. Ohlmeyer J.T., and Kalderon D. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396 (1998) 749-753
24. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.C., Nakashima M., and Joyner A.L. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127 (2000) 1593-1605 (Cambridge, England)
25. Bai C.B., and Joyner A.L. Gli1 can rescue the in vivo function of Gli2. Development 128 (2001) 5161-5172 (Cambridge, England)
26. Bai C.B., Auerbach W., Lee J.S., Stephen D., and Joyner A.L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129 (2002) 4753-4761 (Cambridge, England)
27. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., and Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 126 (1999) 3915-3924 (Cambridge, England)
28. Dai P., Akimaru H., Tanaka Y., Maekawa T., Nakafuku M., and Ishii S. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274 (1999) 8143-8152
29. Sasaki H., Hui C., Nakafuku M., and Kondoh H. 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 (Cambridge, England)
30. Lei Q., Jeong Y., Misra K., Li S., Zelman A.K., Epstein D.J., and Matise M.P. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev. Cell 11 (2006) 325-337
31. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J., Davidson E.H., Wong W.H., and McMahon A.P. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134 (2007) 1977-1989 (Cambridge, England)
32. Hui C.C., Slusarski D., Platt K.A., Holmgren R., and Joyner A.L. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 162 (1994) 402-413
33. Wijgerde M., McMahon J.A., Rule M., and McMahon A.P. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 16 (2002) 2849-2864
34. Pierani A., Brenner-Morton S., Chiang C., and Jessell T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97 (1999) 903-915
35. Litingtung Y., and Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3 (2000) 979-985
36. Persson M., Stamataki D., te Welscher P., Andersson E., Bose J., Ruther U., Ericson J., and Briscoe J. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16 (2002) 2865-2878
37. Briscoe J., Pierani A., Jessell T.M., and Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000) 435-445
38. Shimamura K., Hartigan D.J., Martinez S., Puelles L., and Rubenstein J.L. Longitudinal organization of the anterior neural plate and neural tube. Development 121 (1995) 3923-3933 (Cambridge, England)
39. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., and Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90 (1997) 169-180
40. Muhr J., Andersson E., Persson M., Jessell T.M., and Ericson J. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104 (2001) 861-873
41. Rangini Z., Ben-Yehuda A., Shapira E., Gruenbaum Y., and Fainsod A. CHox E, a chicken homeogene of the H2.0 type exhibits dorso-ventral restriction in the proliferating region of the spinal cord. Mech. Dev. 35 (1991) 13-24
42. Lu S., Bogarad L.D., Murtha M.T., and Ruddle F.H. Expression pattern of a murine homeobox gene, Dbx, displays extreme spatial restriction in embryonic forebrain and spinal cord. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 8053-8057
43. Pierani A., Moran-Rivard L., Sunshine M.J., Littman D.R., Goulding M., and Jessell T.M. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29 (2001) 367-384
44. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., and Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109 (2002) 75-86
45. Zhou Q., and Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109 (2002) 61-73
46. Charrier J.B., Lapointe F., Le Douarin N.M., and Teillet M.A. Dual origin of the floor plate in the avian embryo. Development 129 (2002) 4785-4796 (Cambridge, England)
47. Placzek M., and Briscoe J. The floor plate: multiple cells, multiple signals. Nat. Rev. 6 (2005) 230-240
48. Wichterle H., Lieberam I., Porter J.A., and Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 110 (2002) 385-397
49. Diez del Corral R., Olivera-Martinez I., Goriely A., Gale E., Maden M., and Storey K. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40 (2003) 65-79
50. Novitch B.G., Wichterle H., Jessell T.M., and Sockanathan S. A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40 (2003) 81-95
51. Parr B.A., Shea M.J., Vassileva G., and McMahon A.P. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119 (1993) 247-261 (Cambridge, England)
52. Megason S.G., and McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129 (2002) 2087-2098 (Cambridge, England)
53. Pozniak C.D., and Pleasure S.J. A tale of two signals: Wnt and Hedgehog in dentate neurogenesis. Sci. STKE 319 (2006) pe5
54. Alvarez-Medina R., Cayuso J., Okubo T., Takada S., and Marti E. Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development 135 (2008) 237-247 (Cambridge, England)
55. Ulloa F., Itasaki N., and Briscoe J. Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signaling. Curr. Biol. 17 (2007) 545-550
56. Basler K., Edlund T., Jessell T.M., and Yamada T. Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGF beta family member. Cell 73 (1993) 687-702
57. Liem Jr. K.F., Tremml G., Roelink H., and Jessell T.M. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82 (1995) 969-979
58. Lee K.J., Mendelsohn M., and Jessell T.M. 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 (1998) 3394-3407
59. Lee K.J., and Jessell T.M. The specification of dorsal cell fates in the vertebrate central nervous system. Ann. Rev. Neurosci. 22 (1999) 261-294
60. Liem Jr. K.F., Jessell T.M., and Briscoe J. Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127 (2000) 4855-4866 (Cambridge, England)
61. Connolly D.J., Patel K., and Cooke J. Chick noggin is expressed in the organizer and neural plate during axial development, but offers no evidence of involvement in primary axis formation. Int. J. Dev. Biol. 41 (1997) 389-396
62. Dale K., Sattar N., Heemskerk J., Clarke J.D., Placzek M., and Dodd J. Differential patterning of ventral midline cells by axial mesoderm is regulated by BMP7 and chordin. Development 126 (1999) 397-408 (Cambridge, England)
63. Graham A., and Lumsden A. Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain. Development 122 (1996) 473-480 (Cambridge, England)
64. McMahon J.A., Takada S., Zimmerman L.B., Fan C.M., Harland R.M., and McMahon A.P. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12 (1998) 1438-1452
65. Liu F., Massague J., and Ruiz i Altaba A. Carboxy-terminally truncated Gli3 proteins associate with Smads. Nat. Genet. 20 (1998) 325-326
66. Fuentealba L.C., Eivers E., Ikeda A., Hurtado C., Kuroda H., Pera E.M., and De Robertis E.M. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131 (2007) 980-993
67. Segal E., Raveh-Sadka T., Schroeder M., Unnerstall U., and Gaul U. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451 (2008) 535-540
68. Hallikas O., Palin K., Sinjushina N., Rautiainen R., Partanen J., Ukkonen E., and Taipale J. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124 (2006) 47-59
69. Ji H., and Wong W.H. Computational biology: toward deciphering gene regulatory information in mammalian genomes. Biometrics 62 (2006) 645-663
70. Lettice L.A., Heaney S.J., Purdie L.A., Li L., de Beer P., Oostra B.A., Goode D., Elgar G., Hill R.E., and de Graaff E. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12 (2003) 1725-1735
71. Sagai T., Hosoya M., Mizushina Y., Tamura M., and Shiroishi T. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132 (2005) 797-803 (Cambridge, England)
72. Ling J.Q., Li T., Hu J.F., Vu T.H., Chen H.L., Qiu X.W., Cherry A.M., and Hoffman A.R. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312 (2006) 269-272 New York, N.Y
73. Lomvardas S., Barnea G., Pisapia D.J., Mendelsohn M., Kirkland J., and Axel R. Interchromosomal interactions and olfactory receptor choice. Cell 126 (2006) 403-413
74. Sasaki H., and Hogan B.L. HNF-3 beta as a regulator of floor plate development. Cell 76 (1994) 103-115
75. Sasaki H., and Hogan B.L. Enhancer analysis of the mouse HNF-3 beta gene: regulatory elements for node/notochord and floor plate are independent and consist of multiple sub-elements. Genes Cells 1 (1996) 59-72
76. Sun T., Hafler B.P., Kaing S., Kitada M., Ligon K.L., Widlund H.R., Yuk D.I., Stiles C.D., and Rowitch D.H. Evidence for motoneuron lineage-specific regulation of Olig2 in the vertebrate neural tube. Dev. Biol. 292 (2006) 152-164
77. Santagati F., Abe K., Schmidt V., Schmitt-John T., Suzuki M., Yamamura K., and Imai K. Identification of cis-regulatory elements in the mouse Pax9/Nkx2-9 genomic region: implication for evolutionary conserved synteny. Genetics 165 (2003) 235-242