Incipient forebrain boundaries traced by differential gene expression and fate mapping in the chick neural plate

Developmental Biology

Volumn 335, Issue 1, 2009, Pages 43-65

  Sánchez Arrones, Luisa ^a   Ferrán, José Luis ^a   Rodríguez Gallardo, Lucía ^b   Puelles, Luis ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

Dorsoventral patterning; Eye field; Fate map; Fate specification; Forebrain; Gastrulation; Neurulation; Regionalization; Rostrocaudal patterning; Telencephalic field

Indexed keywords

GENE PRODUCT; PROTEIN GANF; TRANSCRIPTION FACTOR SIX3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTERIOR POSTERIOR AXIS; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FOREBRAIN; GENE CONTROL; GENE EXPRESSION PROFILING; MARKER GENE; MOLECULAR DYNAMICS; MORPHOGENESIS; NEUROECTODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELENCEPHALON;

AVES;

EID: 70349786468     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.08.012     Document Type: Article

References (105)

1. Acampora D., Mazan S., Lallemand Y., Avantaggiato V., Maury M., Simeone A., and Brûlet P. Forebrain and midbrain regions are deleted in Otx2-/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121 (1995) 3279-3290
2. Alvarez I.S., and Schoenwolf G.C. Patterns of neurepithelial cell rearrangement during avian neurulation are determined prior to notochordal inductive interactions. Dev. Biol. 143 (1991) 78-92
3. Anderson R.M., Lawrence A.R., Stottmann R.W., Bachiller D., and Klingensmith J. Chordin and noggin promote organizing centers of forebrain development in the mouse. Development 129 (2002) 4975-4987
4. Andreae L.C., Peukert D., Lumsden A., and Gilthorpe J.D. Analysis of Lrrn1 expression and its relationship to neuromeric boundaries during chick neural development. Neural Dev. 31 2 (2007) 22
5. Bardet, S. M., 2007. Tesis Doctoral, Organización morfológica y citogenética del hipotálamo del pollo sobre base de mapas moleculares.
6. Bayramov A.V., Martynova N.Y., Eroshkin F.M., Ermakova G.V., and Zaraisky A.G. The homeodomain-containing transcription factor X-nkx-5.1 inhibits expression of the homeobox gene Xanf-1 during the Xenopus laevis forebrain development. Mech. Dev. 121 (2004) 1425-1441
7. Bell E., Ensini M., Gulisano M., and Lumsden A. Dynamic domains of gene expression in the early avian forebrain. Dev. Biol. 236 (2001) 76-88
8. Bertrand N., Médevielle F., and Pituello F. FGF signalling controls the timing of Pax6 activation in the neural tube. Development 127 (2000) 4837-4843
9. Bovolenta P., Mallamaci A., Puelles L., and Boncinelli E. Expression pattern of cSix3, a member of the Six/sine oculis family of transcription factors. Mech. Dev. 70 (1998) 201-203
10. Braun M.M., Etheridge A., Bernard A., Robertson C.P., and Roelink H. Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development 130 (2003) 5579-5587
11. Briscoe J., and Ericson J. Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11 (2001) 43-49
12. Cavodeassi F., Carreira-Barbosa F., Young R.M., Concha M.L., Allende M.L., Houart C., Tada M., and Wilson S.W. Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron 47 (2005) 43-56
13. Chapman S.C., Schubert F.R., Schoenwolf G.C., and Lumsden A. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 245 (2002) 187-199
14. 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
15. Cobos I., Shimamura K., Rubenstein J.L., Martinez S., and Puelles L. Fate map of the avian anterior forebrain at the four-somite stage, based on the analysis of quail-chick chimeras. Dev. Biol. 239 (2001) 46-67
16. Colombo A., Reig G., Mione M., and Concha M.L. Zebrafish BarH-like genes define discrete neural domains in the early embryo. Gene Expr. Patterns 6 (2006) 347-352
17. Conlon R.A., and Rossant J. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116 (1992) 357-368
18. Crossley P.H., Martinez S., Ohkubo Y., and Rubenstein J.L. Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108 (2001) 183-206
19. Danesin C., Peres J.N., Johansson M., Snowden V., Cording A., Papalopulu N., and Houart C. Integration of telencephalic Wnt and hedgehog signaling center activities by Foxg1. Dev. Cell. 16 (2009) 576-587
20. Darnell D.K., Garcia-Martinez V., Lopez-Sanchez C., Yuan S., and Schoenwolf G.C. Dynamic labeling techniques for fate mapping, testing cell commitment, and following living cells in avian embryos. Methods Mol. Biol. 135 (2000) 305-321
21. Dias M.S., and Schoenwolf G.C. Formation of ectopic neurepithelium in chick blastoderms: age-related capacities for induction and self-differentiation following transplantation of quail Hensen's nodes. Anat. Rec. 228 (1990) 437-448
22. 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
23. Echevarria D., Vieira C., Gimeno L., and Martinez S. Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res. Brain Res. Rev. 43 (2003) 179-191
24. Echevarria D., Belo J.A., and Martinez S. Modulation of Fgf8 activity during vertebrate brain development. Brain Res. Brain Res. Rev. 49 (2005) 150-157
25. Ermakova G.V., Solovieva E.A., Martynova N.Y., and Zaraisky A.G. The homeodomain factor Xanf represses expression of genes in the presumptive rostral forebrain that specify more caudal brain regions. Dev. Biol. 307 (2007) 483-497
26. Eroshkin F., Kazanskaya O., Martynova N., and Zaraisky A. Characterization of cis-regulatory elements of the homeobox gene Xanf-1. Gene 285 (2002) 279-286
27. Ezin A.M., Fraser S.E., and Bronner-Fraser M. Fate map and morphogenesis of presumptive neural crest and dorsal neural tube. Dev. Biol. 330 (2009) 221-236
28. Fernandez-Garre P., Rodriguez-Gallardo L., Gallego-Diaz V., Alvarez I.S., and Puelles L. Fate map of the chicken neural plate at stage 4. Development 129 (2002) 2807-2822
29. Ferran J.L., Sanchez-Arrones L., Sandoval J.E., and Puelles L. A model of early molecular regionalization in the chicken embryonic pretectum. J. Comp. Neurol. 505 (2007) 379-403
30. Flames N., Pla R., Gelman D.M., Rubenstein J.L., Puelles L., and Marín O. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27 (2007) 9682-9695
31. Foley A.C., Skromne I., and Stern C.D. Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127 (2000) 3839-3854
32. Foley A.C., and Stern C.D. Evolution of vertebrate forebrain development: how many different mechanisms?. J. Anat. 199 (2001) 35-52
33. García-Calero E., Garda A.L., Marín F., and Puelles L. Expression of Lrrn1 marks the prospective site of the zona limitans thalami in the early embryonic chicken diencephalon. Gene Expr. Patterns 6 (2006) 879-885
34. Garcia-Calero E., Fernandez-Garre P., Martinez S., and Puelles L. Early mammillary pouch specification in the course of prechordal ventralization of the forebrain tegmentum. Dev. Biol. 320 (2008) 366-377
35. Gestri G., Carl M., Appolloni I., Wilson S.W., Barsacchi G., and Andreazzoli M. Six3 functions in anterior neural plate specification by promoting cell proliferation and inhibiting Bmp4 expression. Development 132 (2005) 2401-2413
36. Hamburger V., and Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morph. 88 (1951) 49-92
37. Hashimoto H., Yabe T., Hirata T., Shimizu T., Bae Y., Yamanaka Y., Hirano T., and Hibi M. Expression of the zinc finger gene fez-like in zebrafish forebrain. Mech. Dev. 97 (2000) 191-195
38. Hensen V. Beobachtungen über die Befruchtung und Entwicklung des Kaninchens und Meerschweinchens. 2. Anat. EntwGesch. 1 (1876) 353-423
39. Hidalgo-Sánchez M., Simeone A., and Alvarado-Mallart R.M. Fgf8 and Gbx2 induction concomitant with Otx2 repression is correlated with midbrain-hindbrain fate of caudal prosencephalon. Development 126 (1999) 3191-3203
40. Hidalgo-Sánchez M., Millet S., Bloch-Gallego E., and Alvarado-Mallart R.M. Formation of the boundary between the midbrain and the hindbrain: involvement of Otx2 and Gbx2 genes. J. Soc. Biol. 194 (2000) 113-118
41. Houart C., Westerfield M., and Wilson S.W. A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature 391 (1998) 788-792
42. Houart C., Caneparo L., Heisenberg C., Barth K., Take-Uchi M., and Wilson S. Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling. Neuron 35 (2002) 255-265
43. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
44. Khudyakov J., and Bronner-Fraser M. Comprehensive spatiotemporal analysis of early chick neural crest network genes. Dev. Dyn. 238 (2009) 716-723
45. Kiecker C., and Niehrs C. The role of prechordal mesendoderm in neural patterning. Curr. Opin. Neurobiol. 11 (2001) 27-33
46. Kiecker C., and Lumsden A. Compartments and their boundaries in vertebrate brain development. Nat. Rev. Neurosci. 6 (2005) 553-564
47. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
48. Knoetgen H., Viebahn C., and Kessel M. Head induction in the chick by primitive endoderm of mammalian, but not avian origin. Development 126 (1999) 815-825
49. Kobayashi D., Kobayashi M., Matsumoto K., Ogura T., Nakafuku M., and Shimamura K. Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129 (2002) 83-93
50. Lagutin O.V., Zhu C.C., Kobayashi D., Topczewski J., Shimamura K., Puelles L., Russell H.R., McKinnon P.J., Solnica-Krezel L., and Oliver G. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17 (2003) 368-379
51. Lavado A., Lagutin O.V., and Oliver G. Six3 inactivation causes progressive caudalization and aberrant patterning of the mammalian diencephalon. Development 135 (2008) 441-450
52. Lemaire L., and Kessel M. Gastrulation and homeobox genes in chick embryos. Mech. Dev. 67 (1997) 3-16
53. Linker C., and Stern C.D. Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 131 (2004) 5671-5681
54. Lopez-Sanchez C., Garcia-Martinez V., and Schoenwolf G.C. Localization of cells of the prospective neural plate, heart and somites within the primitive streak and epiblast of avian embryos at intermediate primitive-streak stages. Cells Tissues Organs 169 (2001) 334-346
55. Lopez-Sanchez C., Puelles L., Garcia-Martinez V., and Rodriguez-Gallardo L. Morphological and molecular analysis of the early developing chick requires an expanded series of primitive streak stages. J. Morphol. 264 (2005) 105-116
56. Manning L., Ohyama K., Saeger B., Hatano O., Wilson S.A., Logan M., and Placzek M. Regional morphogenesis in the hypothalamus: a BMP-Tbx2 pathway coordinates fate and proliferation through Shh downregulation. Dev. Cell 11 (2006) 873-885
57. Martí E., Takada R., Bumcrot D.A., Sasaki H., and McMahon A.P. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121 (1995) 2537-2547
58. Martinez-Barbera J.P., and Beddington R.S. Getting your head around Hex and Hesx1: forebrain formation in mouse. Int. J. Dev. Biol. 45 (2001) 327-336
59. Martinez-Barbera J.P., Signore M., Boyl P.P., Puelles E., Acampora D., Gogoi R., Schubert F., Lumsden A., and Simeone A. Regionalisation of anterior neuroectoderm and its competence in responding to forebrain and midbrain inducing activities depend on mutual antagonism between OTX2 and GBX2. Development 128 (2001) 4789-4800
60. Martynova N., Eroshkin F., Ermakova G., Bayramov A., Gray J., Grainger R., and Zaraisky A. Patterning the forebrain: FoxA4a/Pintallavis and Xvent2 determine the posterior limit of Xanf1 expression in the neural plate. Development 131 (2004) 2329-2338
61. New D.A.T. A new technique for the cultivation of the chick embryo in vitro. J. Embryol. Exp. Morph. 3 (1955) 326-331
62. Nieuwkoop P.D., Botterenbrood E.C., Kremer A., Bloesma FFSN., Hoessels ELMJ., Meyer G., et al. Activation and organization of the central nervous system in Amphibians. J. Exp. Zool. 120 (1952) 1-108
63. Nieuwkoop P.D., and Nigtevecht G.V. Neural activation and transformation in explants of competent ectoderm under the influence of fragments of anterior notochord in urodeles. J. Embryol. Exp. Morphol. 2 (1954) 175-193
64. Nordström U., Jessell T.M., and Edlund T. Progressive induction of caudal neural character by graded Wnt signaling. Nat. Neurosci. 5 (2002) 525-532
65. Ohkubo Y., Chiang C., and Rubenstein J.L. Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111 (2002) 1-17
66. Olander S., Nordstrom U., Patthey C., and Edlund T. Convergent Wnt and FGF signaling at the gastrula stage induce the formation of the isthmic organizer. Mech. Dev. 123 (2006) 166-176
67. Papanayotou C., Mey A., Birot A.M., Saka Y., Boast S., Smith J.C., Samarut J., and Stern C.D. A mechanism regulating the onset of Sox2 expression in the embryonic neural plate. PLoS Biol. e2 (2008) 6
68. Pera E., Stein S., and Kessel M. Ectodermal patterning in the avian embryo: epidermis versus neural plate. Development 126 (1999) 63-73
69. Placzek M., and Briscoe J. The floor plate: multiple cells, multiple signals. Nat. Rev. Neurosci. 6 (2005) 230-240
70. Pombero A., and Martinez S. Telencephalic morphogenesis during the process of neurulation: an experimental study using quail-chick chimeras. J. Comp. Neurol. 512 (2009) 784-797
71. Puelles L., Amat J.A., and Martinez-de-la-Torre M. Segment-related, mosaic neurogenetic pattern in the forebrain and mesencephalon of early chick embryos: I. Topography of AChE-positive neuroblasts up to stage HH18. J. Comp. Neurol. 266 (1987) 247-268
72. Puelles L., and Rubenstein J.L. Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16 (1993) 472-479
73. Puelles L. A segmental morphological paradigm for understanding vertebrate forebrains. Brain. Behav. Evol. 46 (1995) 319-337
74. Puelles L. Brain segmentation and forebrain development in amniotes. Brain Res. Bull. 55 (2001) 695-710
75. Puelles L., and Rubenstein J.L. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 26 (2003) 469-476
76. Puelles L., Fernandez-Garre P., Sanchez-Arrones L., Garcia-Calero E., and Rodriguez-Gallardo L. Correlation of a chicken stage 4 neural plate fate map with early gene expression patterns. Brain Res. Brain Res. Rev. 49 (2005) 167-178
77. Puelles, L., Martinez-de-la-Torre, M., Paxinos, G., Watson, C., Martinez, S., 2007. The chick brain in stereotaxic coordinates. An atlas featuring neuromeric subdivisions and mammalian homologies.
78. Regad T., Roth M., Bredenkamp N., Illing N., and Papalopulu N. The neural progenitor-specifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat. Cell Biol. 9 (2007) 531-540
79. Rex M., Orme A., Uwanogho D., Tointon K., Wigmore P.M., Sharpe P.T., and Scotting P.J. Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev. Dyn. 209 (1997) 323-332
80. Rodriguez-Gallardo L., Sanchez-Arrones L., Fernandez-Garre P., and Puelles L. Agreement and disagreement among fate maps of the chick neural plate. Brain Res. Brain Res. Rev. 49 (2005) 191-201
81. Rubenstein J.L., Shimamura K., Martinez S., and Puelles L. Regionalization of the prosencephalic neural plate. Annu. Rev. Neurosci. 21 (1998) 445-477
82. Rubenstein J.L., and Beachy P.A. Patterning of the embryonic forebrain. Curr. Opin. Neurobiol. 8 (1998) 18-26
83. Ruiz i Altaba A. Induction and axial patterning of the neural plate: planar and vertical signals. J. Neurobiol. 24 (1993) 1276-1304
84. Saha M.S., and Grainger R.M. A labile period in the determination of the anterior-posterior axis during early neural development in Xenopus. Neuron 8 (1992) 1003-1014
85. Schoenwolf G.C., and Sheard P. Fate mapping the avian epiblast with focal injections of a fluorescent-histochemical marker: ectodermal derivatives. J. Exp. Zool. 255 (1990) 323-339
86. Scholpp S., Lohs C., and Brand M. Engrailed and Fgf8 act synergistically to maintain the boundary between diencephalon and mesencephalon. Development 130 (2003) 4881-4893
87. Seiliez I., Thisse B., and Thisse C. FoxA3 and goosecoid promote anterior neural fate through inhibition of Wnt8a activity before the onset of gastrulation. Dev. Biol. 290 (2006) 152-163
88. Sheng G., dos R.M., and Stern C.D. Churchill, a zinc finger transcriptional activator, regulates the transition between gastrulation and neurulation. Cell 115 (2003) 603-613
89. Shimamura K., Hirano S., McMahon A.P., and Takeichi M. Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development 120 (1994) 2225-2234
90. 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
91. Shimamura K., and Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development 124 (1997) 2709-2718
92. Simeone A., Acampora D., Gulisano M., Stornaiuolo A., and Boncinelli E. Nested expression domains of four homeobox genes in developing rostral brain. Nature 358 (1992) 687-690
93. Spieler D., Bäumer N., Stebler J., Köprunner M., Reichman-Fried M., Teichmann U., Raz E., Kessel M., and Wittler L. Involvement of Pax6 and Otx2 in the forebrain-specific regulation of the vertebrate homeobox gene ANF/Hesx1. Dev. Biol. 269 (2004) 567-579
94. Staudt N., and Houart C. The prethalamus is established during gastrulation and influences diencephalic regionalization. PLoS Biol. e69 (2007) 5
95. Stern C.D., and Bachvarova R. Early chick embryos in vitro. Int. J. Dev. Biol. 41 (1997) 379-387
96. Stigloher C., Ninkovic J., Laplante M., Geling A., Tannhäuser B., Topp S., Kikuta H., Becker T.S., Houart C., and Bally-Cuif L. Segregation of telencephalic and eye-field identities inside the zebrafish forebrain territory is controlled by Rx3. Development 133 (2006) 2925-2935
97. Storey K.G., Crossley J.M., De Robertis E.M., Norris W.E., and Stern C.D. Neural induction and regionalisation in the chick embryo. Development 114 (1992) 729-741
98. Streit A., and Stern C.D. Establishment and maintenance of the border of the neural plate in the chick: involvement of FGF and BMP activity. Mech. Dev. 82 (1999) 51-66
99. Streit A., Berliner A.J., Papanayotou C., Sirulnik A., and Stern C.D. Initiation of neural induction by FGF signalling before gastrulation. Nature 406 (2000) 74-78
100. Tendeng C., and Houart C. Cloning and embryonic expression of five distinct sfrp genes in the zebrafish Danio rerio. Gene Expr. Patterns 6 (2006) 761-771
101. Theiler, K. 1989. The House Mouse: Atlas of the Embryonic Development.
102. Wilson S.W., and Rubenstein J.L. Induction and dorsoventral patterning of the telencephalon. Neuron 28 (2000) 641-651
103. Wilson S.W., and Houart C. Early steps in the development of the forebrain. Dev. Cell. 6 (2004) 167-181
104. Wittler L., and Kessel M. The acquisition of neural fate in the chick. Mech. Dev. 121 (2004) 1031-1042
105. Xuan S., Baptista C.A., Balas G., Tao W., Soares V.C., and Lai E. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14 (1995) 1141-1152