Signaling mechanisms controlling cranial placode neurogenesis and delamination

Developmental Biology

Volumn 389, Issue 1, 2014, Pages 39-49

  Lassiter, Rhonda N T ^a,b   Stark, Michael R ^c   Zhao, Tianyu ^a,b   Zhou, Chengji J ^a,b  

^a SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

BMP; Cranial placodes; Delamination; FGF; Neurogenesis; Notch; Wnt

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLYCOGEN SYNTHASE KINASE 3; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ARTICLE; CELL ADHESION; CELL MIGRATION; CRANIAL PLACODE; DELAMINATION; ECTODERM; EMBRYO PATTERN FORMATION; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; METASTASIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL STEM CELL; NEUROBLAST; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; WNT SIGNALING PATHWAY; BMP SIGNALING; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; EPIBRANCHIAL PLACODE; FGF SIGNALING; NOTCH SIGNALING; OLFACTORY PLACODE; OTIC PLACODE; SENSORY NERVE CELL; TRIGEMINAL PLACODE;

BMP; CRANIAL PLACODES; DELAMINATION; FGF; NEUROGENESIS; NOTCH; WNT;

ANIMALS; BONE MORPHOGENETIC PROTEINS; ECTODERM; EPIDERMAL GROWTH FACTOR; HUMANS; MODELS, NEUROLOGICAL; NERVOUS SYSTEM; NEUROGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84897428996     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.11.025     Document Type: Article

References (109)

1. Abello G., Alsina B. Establishment of a proneural field in the inner ear. Int. J. Dev. Biol. 2007, 51:483-493.
2. Abello G., Khatri S., Radosevic M., Scotting P.J., Giraldez F., Alsina B. Independent regulation of Sox3 and Lmx1b by FGF and BMP signaling influences the neurogenic and non-neurogenic domains in the chick otic placode. Dev. Biol. 2010, 339:166-178.
3. Adam J., Myat A., Le Roux I., Eddison M., Henrique D., Ish-Horowicz D., Lewis J. Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 1998, 125:4645-4654.
4. Ahrens K., Schlosser G. Tissue and signals invovled in the induction of placodal Six1 expression in Xenopus laevis. Dev. Biol. 2005, 288:40-59.
5. Albo D., Akay C.L., Marshall C.L., Wilks J.A., Verstovsek G., Liu H., Agarwal N., Berger D.H., Ayala G.E. Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes. Cancer 2011, 117:4834-4845.
6. Alsina B., Abello G., Ulloa E., Henrique D., Pujades C., Giraldez F. FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev. Biol. 2004, 267:119-134.
7. Babb-Clendenon S., Shen Y.C., Liu Q., Turner K.E., Mills M.S., Cook G.W., Miller C.A., Gattone V.H., Barald K.F., Marrs J.A. Cadherin-2 participates in the morphogenesis of the zebrafish inner ear. J. Cell Sci. 2006, 119:5169-5177.
8. Bailey A.P., Bhattacharyya S., Bronner-Fraser M., Streit A. Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity. Dev. Cell 2006, 11:505-517.
9. Baker C.V., Bronner-Fraser M. Establishing neuronal identity in vertebrate neurogenic placodes. Development 2000, 127:3045-3056.
10. Baker C.V., Bronner-Fraser M. Vertebrate cranial placodes I. Embryonic induction. Dev. Biol. 2001, 232:1-61.
11. Baker C.V., Stark M.R., Bronner-Fraser M. Pax3-expressing trigeminal placode cells can localize to trunk neural crest sites but are committed to a cutaneous sensory neuron fate. Dev. Biol. 2002, 249:219-236.
12. Baker C.V., Stark M.R., Marcelle C., Bronner-Fraser M. Competence, specification and induction of Pax-3 in the trigeminal placode. Development 1999, 126:147-156.
13. Barald K.F., Kelley M.W. From placode to polarization: new tunes in inner ear development. Development 2004, 131:4119-4130.
14. Begbie J., Ballivet M., Graham A. Early steps in the production of sensory neurons by the neurogenic placodes. Mol. Cell. Neurosci. 2002, 21:502-511.
15. Begbie J., Brunet J.F., Rubenstein J.L., Graham A. Induction of the epibranchial placodes. Development 1999, 126:895-902.
16. Beites C.L., Kawauchi S., Crocker C.E., Calof A.L. Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp. Cell Res. 2005, 306:309-316.
17. Bhat N., Riley B.B. Integrin-alpha5 coordinates assembly of posterior cranial placodes in zebrafish and enhances FGF-dependent regulation of otic/epibranchial cells. PLoS One 2011, 6:e27778.
18. Blentic A., Chambers D., Skinner A., Begbie J., Graham A. The formation of the cranial ganglia by placodally-derived sensory neuronal precursors. Mol. Cell. Neurosci. 2011, 46:452-459.
19. Brown A.S., Epstein D.J. Otic ablation of smoothened reveals direct and indirect requirements for Hedgehog signaling in inner ear development. Development 2011, 138:3967-3976.
20. Canning C.A., Lee L., Luo S.x., Graham A., Jones C.M. Neural tube derived Wnt signals cooperate with FGF signaling in the formation and differentiation of the trigeminal placodes. Neural Dev. 2008, 3:35.
21. Carney P.R., Silver J. Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. J. Comp. Neurol. 1983, 215:359-369.
22. Chong L.D., Park E.K., Latimer E., Friesel R., Daar I.O. Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos. Mol. Cell. Biol. 2000, 20:724-734.
23. Covell D.A., Noden D.M. Embryonic development of the chick primary trigeminal sensory-motor complex. J. Comp. Neurol. 1989, 286:488-503.
24. Croucher S.J., Tickle C. Characterization of epithelial domains in the nasal passages of chick embryos: spatial and temporal mapping of a range of extracellular matrix and cell surface molecules during development of the nasal placode. Development 1989, 106:493-509.
25. d'Amico-Martel A., Noden D.M. An autoradiographic analysis of the development of the chick trigeminal ganglion. J. Embryol. Exp. Morphol. 1980, 55:167-182.
26. D'Amico-Martel A., Noden D.M. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am. J. Anat. 1983, 166:445-468.
27. Davies D. Temporal and spatial regulation of alpha6 integrin expression during the development of the cochlear-vestibular ganglion. J. Comp. Neurol. 2007, 502:673-682.
28. Fode C., Gradwohl G., Morin X., Dierich A., LeMeur M., Goridis C., Guillemot F. The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 1998, 20:483-494.
29. Fornaro M., Geuna S., Fasolo A., Giacobini-Robecchi M.G. HuC/D confocal imaging points to olfactory migratory cells as the first cell population that expresses a post-mitotic neuronal phenotype in the chick embryo. Neuroscience 2003, 122:123-128.
30. Forni P.E., Wray S. Neural crest and olfactory system: new prospective. Mol. Neurobiol. 2012, 46:349-360.
31. Freter S., Fleenor S.J., Freter R., Liu K.J., Begbie J. Cranial neural crest cells form corridors prefiguring sensory neuroblast migration. Development 2013, 140:3595-3600.
32. Freter S., Muta Y., Mak S.S., Rinkwitz S., Ladher R.K. Progressive restriction of otic fate: the role of FGF and Wnt in resolving inner ear potential. Development 2008, 135:3415-3424.
33. Freyer L., Morrow B.E. Canonical Wnt signaling modulates Tbx1, Eya1, and Six1 expression, restricting neurogenesis in the otic vesicle. Dev. Dyn. 2010, 239:1708-1722.
34. Freyer L., Aggarwal V., Morrow B.E. Dual embryonic origin of the mammalian otic vesicle forming the inner ear. Development 2011, 138:5403-5414.
35. Gan Q., Lee A., Suzuki R., Yamagami T., Stokes A., Nguyen B., Pleasure D., Wang J., Chen H.W, Zhou C.J. Pax6 mediates ß-catenin signaling for self-renewal and neurogenesis by neocortical radial glial stem cells. Stem Cells 2013, (Epub ahead of print). 10.1002/stem.1561.
36. Glazier J.A., Zhang Y., Swat M., Zaitlen B., Schnell S. Coordinated action of N-CAM, N-cadherin, EphA4, and ephrinB2 translates genetic prepatterns into structure during somitogenesis in chick. Curr. Top. Dev. Biol. 2008, 81:205-247.
37. Graham A., Blentic A., Duque S., Begbie J. Delamination of cells from neurogenic placodes does not involve an epithelial-to-mesenchymal transition. Development 2007, 134:4141-4145.
38. Haddon C., Jiang Y.J., Smithers L., Lewis J. Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 1998, 125:4637-4644.
39. Hamada Y., Kadokawa Y., Okabe M., Ikawa M., Coleman J.R., Tsujimoto Y. Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality. Development 1999, 126:3415-3424.
40. Hammond K.L., Whitfield T.T. FGF and Hh signalling act on a symmetrical pre-pattern to specify anterior and posterior identity in the zebrafish otic placode and vesicle. Development 2011, 138:3977-3987.
41. Harlow D.E., Barlow L.A. Embryonic origin of gustatory cranial sensory neurons. Dev. Biol. 2007, 310:317-328.
42. Hartman B.H., Reh T.A., Bermingham-McDonogh O. Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:15792-15797.
43. Holzschuh J., Wada N., Wada C., Schaffer A., Javidan Y., Tallafuss A., Bally-Cuif L., Schilling T.F. Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development 2005, 132:3731-3742.
44. Hong I.K., Jeoung D.I., Ha K.S., Kim Y.M., Lee H. Tetraspanin CD151 stimulates adhesion-dependent activation of Ras, Rac, and Cdc42 by facilitating molecular association between beta1 integrins and small GTPases. J. Biol. Chem. 2012, 287:32027-32039.
45. Kageyama R., Ohtsuka T., Shimojo H., Imayoshi I. Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 2008, 11:1247-1251.
46. Kageyama R., Ohtsuka T., Shimojo H., Imayoshi I. Dynamic regulation of Notch signaling in neural progenitor cells. Curr. Opin. Cell Biol. 2009, 21:733-740.
47. Karsan A. Notch and integrin affinity: a sticky situation. Sci. Signaling 2008, 1.
48. Kawauchi S., Beites C.L., Crocker C.E., Wu H.H., Bonnin A., Murray R., Calof A.L. Molecular signals regulating proliferation of stem and progenitor cells in mouse olfactory epithelium. Dev. Neurosci. 2004, 26:166-180.
49. Kawauchi S., Shou J., Santos R., Hebert J.M., McConnell S.K., Mason I., Calof A.L. FGF8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 2005, 132:5211-5223.
50. Kerosuo L., Bronner-Fraser M. What is bad in cancer is good in the embryo: importance of EMT in neural crest development. Sem. Cell Dev. Biol. 2012, 23:320-332.
51. Kienan A.E., Xu J., Gridley T. The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet. 2006, 2:e4.
52. Kim W.Y., Wang X., Wu Y., Doble B.W., Patel S., Woodgett J.R., Snider W.D. GSK-3 is a master regulator of neural progenitor homeostasis. Nat. Neurosci. 2009, 12:1390-1397.
53. Kriebitz N.N., Kiecker C., McCormick L., Lumsden A., Graham A., Bell E. PRDC regulates placode neurogenesis in chick by modulating BMP signalling. Dev. Biol. 2009, 336:280-292.
54. Kwon H.J., Bhat N., Sweet E.M., Cornell R.A., Riley B.B. Identification of early requirements for preplacodal ectoderm and sensory organ development. PLoS Genet. 2010, 6:e1001133.
55. Ladher R.K., O'Neill P., Begbie J. From shared lineage to distinct functions: the development of the inner ear and epibranchial placodes. Development 2010, 137:1777-1785.
56. Lassiter R.N., Ball M.K., Adams J.S., Wright B.T., Stark M.R. Sensory neuron differentiation is regulated by notch signaling in the trigeminal placode. Dev. Biol. 2010, 344:836-848.
57. Lassiter R.N., Dude C.M., Reynolds S.B., Winters N.I., Baker C.V., Stark M.R. Canonical Wnt signaling is required for ophthalmic trigeminal placode cell fate determination and maintenance. Dev. Biol. 2007, 308:392-406.
58. Lassiter R.N., Reynolds S.B., Marin K.D., Mayo T.F., Stark M.R. FGF signaling is essential for ophthalmic trigeminal placode cell delamination and differentiation. Dev. Dyn. 2009, 238:1073-1082.
59. Leung A.W., Kent Morest D., Li J.Y. Differential BMP signaling controls formation and differentiation of multipotent preplacodal ectoderm progenitors from human embryonic stem cells. Dev. Biol. 2013, 379:208-220.
60. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327:542-545.
61. Litsiou A., Hanson S., Streit A. A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. Development 2005, 132:4051-4062.
62. Liu Z., Owen T., Fang J., Zuo J. Overactivation of Notch1 signaling induces ectopic hair cells in the mouse inner ear in an age-dependent manner. PLoS One 2012, 7:e34123.
63. Maier E., Gunhaga L. Dynamic expression of neurogenic markers in the developing chick olfactory epithelium. Dev. Dyn. 2009, 238:1617-1625.
64. Maier E., Nord H., von Hofsten J., Gunhaga L. A balance of BMP and notch activity regulates neurogenesis and olfactory nerve formation. PLoS One 2011, 6:e17379.
65. Maier E., von Hofsten J., Nord H., Fernandes M., Paek H., Hebert J.M., Gunhaga L. Opposing FGF and BMP activities regulate the specification of olfactory sensory and respiratory epithelial cell fates. Development 2010, 137:1601-1611.
66. McCabe K.L., Bronner M. Tetraspanin, CD151, is required for maintenance of trigeminal placode identity. J. Neurochem. 2011, 117:221-230.
67. McCabe K.L., Sechrist J.W., Bronner-Fraser M. Birth of ophthalmic trigeminal neurons initiates early in the placodal ectoderm. J. Comp. Neurol. 2009, 514:161-173.
68. Mendoza A.S., Breipohl W., Miragall F. Cell migration from the chick olfactory placode: a light and electron microscopic study. J. Embryol. Exp. Morphol. 1982, 69:47-59.
69. Moody S.A., Quigg M.S., Frankfurter A. Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J. Comp. Neurol. 1989, 279:567-580.
70. Moody S.A., Quigg M.S., Little C.D. Extracellular matrix components of the peripheral pathway of chick trigeminal axons. J. Comp. Neurol. 1989, 283:38-53.
71. Nechiporuk A., Linbo T., Poss K.D., Raible D.W. Specification of epibranchial placodes in zebrafish. Development 2007, 134:611-623.
72. Nechiporuk A., Linbo T., Raible D.W. Endoderm-derived FGF3 is necessary and sufficient for inducing neurogenesis in the epibranchial placodes in zebrafish. Development 2005, 132:3717-3730.
73. Nichols D.H. Mesenchyme formation from the trigeminal placodes of the mouse embryo. Am. J. Anat. 1986, 176:19-31.
74. Nikaido M., Doi K., Shimizu T., Hibi M., Kikuchi Y., Yamasu K. Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal. Dev. Dyn. 2007, 236:564-571.
75. Northcutt R.G. Taste buds: development and evolution. Brain Behav. Evol. 2004, 64:198-206.
76. Ohyama T., Mohamed O.A., Taketo M.M., Dufort D., Groves A.K. Wnt signals mediate a fate decision between otic placode and epidermis. Development 2006, 133:865-875.
77. Pan W., Jin Y., Stanger B., Kiernan A.E. Notch signaling is required for the generation of hair cells and supporting cells in the mammalian inner ear. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:15798-15803.
78. Paschaki M., Cammas L., Muta Y., Matsuoka Y., Mak S.S., Rataj-Baniowska M., Fraulob V., Dolle P., Ladher R.K. Retinoic acid regulates olfactory progenitor cell fate and differentiation. Neural Dev. 2013, 8:13.
79. de la Pompa J.L., Wakeham A., Correia K.M., Samper E., Brown S., Aguilera R.J., Nakano T., Honjo T., Mak T.W., Rossant J., Conlon R.A. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 1997, 124:1139-1148.
80. Rousso D.L., Pearson C.A., Gaber Z.B., Miquelajauregui A., Li S., Portera-Cailliau C., Morrisey E.E., Novitch B.G. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 2012, 74:314-330.
81. Rubel E.W., Fritzsch B. Auditory system development: primary auditory neurons and their targets. Annu. Rev. Neurosci. 2002, 25:51-101.
82. Saeger B.M., Suhm M., Neubuser A. Ephrin/ephrin receptor expression during early stages of mouse inner ear development. Dev. Dyn. 2011, 240:1578-1585.
83. Saravanamuthu S.S., Gao C.Y., Zelenka P.S. Notch signaling is required for lateral induction of Jagged1 during FGF-induced lens fiber differentiation. Dev. Biol. 2009, 332:166-176.
84. Schlosser G. Induction and specification of cranial placodes. Dev. Biol. 2006, 294:303-351.
85. Schlosser G. Making senses development of vertebrate cranial placodes. Int. Rev. Cell Mol. Biol. 2010, 283:129-234.
86. Schlosser G., Northcutt R.G. Development of neurogenic placodes in Xenopus laevis. J. Comp. Neurol. 2000, 418:121-146.
87. Schneider-Maunoury S., Pujades C. Hindbrain signals in otic regionalization: walk on the wild side. Int. J. Dev. Biol. 2007, 51:495-506.
88. Schwarting G.A., Gridley T., Henion T.R. Notch1 expression and ligand interactions in progenitor cells of the mouse olfactory epithelium. J. Mol. Histol. 2007, 38:543-553.
89. Shiau C.E., Das R.M., Storey K.G. An effective assay for high cellular resolution time-lapse imaging of sensory placode formation and morphogenesis. BMC Neurosci. 2011, 12:37.
90. Shimojo H., Ohtsuka T., Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008, 58:52-64.
91. Shou J., Murray R.C., Rim P.C., Calof A.L. Opposing effects of bone morphogenetic proteins on neuron production and survival in the olfactory receptor neuron lineage. Development 2000, 127:5403-5413.
92. Shou J., Rim P.C., Calof A.L. BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat. Neurosci. 1999, 2:339-345.
93. Sjodal M., Edlund T., Gunhaga L. Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev. Cell 2007, 13:141-149.
94. Stainier D.Y., Gilbert W. Neuronal differentiation and maturation in the mouse trigeminal sensory system, in vivo and in vitro. J. Comp. Neurol. 1991, 311:300-312.
95. Stark M.R., Biggs J.J., Schoenwolf G.C., Rao M.S. Characterization of avian frizzled genes in cranial placode development. Mech. Dev. 2000, 93:195-200.
96. Stark M.R., Sechrist J., Bronner-Fraser M., Marcelle C. Neural tube-ectoderm interactions are required for trigeminal placode formation. Development 1997, 124:4287-4295.
97. Sun S.K., Dee C.T., Tripathi V.B., Rengifo A., Hirst C.S., Scotting P.J. Epibranchial and otic placodes are induced by a common FGF signal, but their subsequent development is independent. Dev. Biol. 2007, 303:675-686.
98. Tarozzo G., Peretto P., Fasolo A. Cell migration from the olfactory placode and the ontogeny of the neuroendocrine compartments. Zool. Sci. 1995, 12:367-383.
99. Toledo M.S., Suzuki E., Handa K., Hakomori S. Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J. Biol. Chem. 2005, 280:16227-16234.
100. Torres M., Giraldez F. The development of the vertebrate inner ear. Mech. Dev. 1998, 71:5-21.
101. Tripathi V.B., Ishii Y., Abu-Elmagd M.M., Scotting P.J. The surface ectoderm of the chick embryo exhibits dynamic variation in its response to neurogenic signals. Int. J. Dev. Biol. 2009, 53:1023-1033.
102. Trokovic N., Trokovic R., Partanen J. Fibroblast growth factor signalling and regional specification of the pharyngeal ectoderm. Int. J. Dev. Biol. 2005, 49:797-805.
103. Vergano-Vera E., Mendez-Gomez H.R., Hurtado-Chong A., Cigudosa J.C., Vicario-Abejon C. Fibroblast growth factor-2 increases the expression of neurogenic genes and promotes the migration and differentiation of neurons derived from transplanted neural stem/progenitor cells. Neuroscience 2009, 162:39-54.
104. Verwoerd C.D., van Oostrom C.G., Verwoerd-Verhoef H.L. Otic placode and cephalic neural crest. Acta Otolaryngol. 1981, 91:431-435.
105. Wang Y., Song L., Zhou C.J. The canonical Wnt/beta-catenin signaling pathway regulates FGF signaling for early facial development. Dev. Biol. 2011, 349:250-260.
106. Wang Y.Z., Plane J.M., Jiang P., Zhou C.J., Deng W. Concise review: quiescent and active states of endogenous adult neural stem cells: identification and characterization. Stem Cells 2011, 29:907-912.
107. Wang Y.Z., Yamagami T., Gan Q., Wang Y., Zhao T., Hamad S., Lott P., Schnittke N., Schwob J.E., Zhou C.J. Canonical Wnt signaling promotes the proliferation and neurogenesis of peripheral olfactory stem cells during postnatal development and adult regeneration. J. Cell Sci. 2011, 124:1553-1563.
108. Xu H., Dude C.M., Baker C.V. Fine-grained fate maps for the ophthalmic and maxillomandibular trigeminal placodes in the chick embryo. Dev. Biol. 2008, 317:174-186.
109. Zhao, T., Gan, Q., Stokes, A., Lassiter, R.N.T., Wang, Y., Chan, J., Han, J.X., Pleasure, D.E., Epstein, J.A., Zhou, C.J. (2013). ß-catenin regulates Pax3 and Cdx2 for caudal neural tube closure and elongation. Development, (Epub ahead of print). http://dx.doi.org/10.1242/dev.101550.