Mutual repression between Gbx2 and Otx2 in sensory placodes reveals a general mechanism for ectodermal patterning

Developmental Biology

Volumn 367, Issue 1, 2012, Pages 55-65

  Steventon, Ben ^a,b   Mayor, Roberto ^b   Streit, Andrea ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Chick; Cranial ganglia; Ear; Eye; Fate map; Placodes; Trigeminal; Xenopus

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GBX2; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM DEVELOPMENT; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GASTRULATION; GENE ACTIVATION; GENE TARGETING; HEN; LENS DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEUROECTODERM; NONHUMAN; OLFACTORY DEVELOPMENT; ORGANOGENESIS; PERIPHERAL NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SENSORY PLACODE; TRIGEMINAL DEVELOPMENT; XENOPUS;

VERTEBRATA;

EID: 84861699723     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.04.025     Document Type: Article

References (94)

1. Acampora D., Mazan S., Lallemand Y., Avantaggiato V., Maury M., Simeone A., Brulet P. Forebrain and midbrain regions are deleted in Otx2 -/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 1995, 121:3279-3290.
2. Acampora D., Avantaggiato V., Tuorto F., Briata P., Corte G., Simeone A. Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation. Development 1998, 125:5091-5104.
3. Acampora D., Avantaggiato V., Tuorto F., Simeone A. Genetic control of brain morphogenesis through Otx gene dosage requirement. Development 1997, 124:3639-3650.
4. Arendt D., Technau U., Wittbrodt J. Evolution of the bilaterian larval foregut. Nature 2001, 409:81-85.
5. Anderson A.M., Weasner B.M., Weasner B.P., Kumar J.P. Dual transcriptional activities of SIX proteins define their roles in normal and ectopic eye development. Development 2012, 139:991-1000.
6. Aybar M.J., Nieto M.A., Mayor R. Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 2003, 130:483-494.
7. 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.
8. 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.
9. Baker C.V., Bronner-Fraser M. Establishing neuronal identity in vertebrate neurogenic placodes. Development 2000, 127:3045-3056.
10. Baker C.V.H., Bronner-Fraser M. Vertebrate Cranial Placodes I. Embryonic Induction. Dev. Biol. 2001, 232:1-61.
11. Bally-Cuif L., Gulisano M., Broccoli V., Bonicelli E. C-otx2 is expressed in two different phases of gastrulation and is sensitive to retinoic acid treatment in chick embryo. Mech. Dev. 1995, 49:49-63.
12. Bang A.G., Papalopulu N., Kintner C., Goulding M.D. Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development 1997, 124:2075-2085.
13. Bang A.G., Papalopulu N., Goulding M.D., Kintner C. Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm. Dev. Biol. 1999, 212:366-380.
14. Benito-Gutiérrez È. A gene catalogue of the amphioxus nervous system. Int. J. Biol. Sci. 2006, 2:149-160.
15. Basch M., Bronner-Fraser M., Garcióa-Castro M. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 2006, 41:218-222.
16. Bastidas F., De Calisto J., Mayor R. Identification of neural crest competence territory: role of Wnt signaling. Dev. Dyn. 2004, 229:109-117.
17. Bhattacharyya S., Bailey A.P., Bronner-Fraser M., Streit A. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 2004, 271:403-414.
18. Bhattacharyya S., Bronner-Fraser M. Competence, specification and commitment to an olfactory placode fate. Development 2008, 135:4165-4177.
19. Blitz I.L., Cho K.W. Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 1995, 121:993-1004.
20. Broccoli V., Boncinelli E., Wurst W. The caudal limit of Otx2 expression positions the isthmic organizer. Nature 1999, 401:164-168.
21. Brugmann S.A., Pandur P.D., Kenyon K.L., Pignoni F., Moody S.A. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 2004, 131:5871-5881.
22. Castro L.F.C., Rasmussen S.L.K., Holland P.W.H., Holland N.D., Holland L.Z. A Gbx homeobox gene in amphioxus: Insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Dev.Biol. 2006, 295:40-51.
23. Chang C., Hemmati-Brivanlou A. Neural crest induction by Xwnt7B in Xenopus. Dev. Biol. 1998, 194:129-134.
24. David R., Ahrens K., Wedlich D., Schlosser G. Xenopus Eya1 demarcates all neurogenic placodes as well as migrating hypaxial muscle precursors. Mech. Dev. 2001, 103:189-192.
25. Gallagher B.C., Henry J.J., Grainger R.M. Inductive processes leading to inner ear formation during Xenopus development. Dev. Biol. 1996, 175:95-107.
26. Garcióa-Castro, Marcelle C., Bronner-Fraser M. Ectodermal Wnt functions as a neural crest inducer. Science 2002, 297:848-851.
27. Glavic A., Gómez-Skarmeta J.L., Mayor R. The homeoprotein Xiro1 is required for midbrain-hindbrain boundary formation. Development 2002, 129:1609-1621.
28. Gomez-Skarmeta J.L., Glavic A., de la Calle-Mustienes E., Modolell J., Mayor R. Xiro, a Xenopus homolog of Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J. 1998, 17:181-190.
29. Grainger R.M., Mannion J.E., Cook T.L., Zygar C.A. Defining intermediate stages in cell determination: acquisition of a lens-forming bias in head ectoderm during lens determination. Dev. Genet. 1997, 20:246-257.
30. Groves A.K., Bronner-Fraser M. Competence, specification and commitment in otic placode induction. Development 2000, 127:3489-3499.
31. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morph. 1951, 88:49-92.
32. Harland R.M., Weintraub H. Translation of mRNA injected into Xenopus oocytes is specifically inhibited by antisense RNA. Cell Biol. 1985, 10:1511-1514.
33. Harland R.M. In situ hybridization: An improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991, 36:685-695.
34. Heisenberg C.-P., Houart C., Take-uchi M., Rauch G., Young N., Coutinho P., Masai I., Caneparo L., Concha M.L., Geisler R., et al. A mutation in the Gsk3Β-binding domain of zebrafish masterblind/axin1 leads to a fate transformation of telencephalon and eyes to diencephalon. Genes. Dev. 2001, 15:1427-1434.
35. Heller N., Brändli A.W. Xenopus Pax-2/5/8 orthologues: Novel insights into Pax gene evolution and identification of Pax-8 as the earliest marker for otic and pronephric cell lineages. Dev. Genet. 1999, 24:208-219.
36. Henry J.J., Grainger R.M. Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis. Dev. Biol. 1987, 124:200-214.
37. Hirth F., Kammermeier L., Frei E., Walldorf U., Noll M., Reichert H. An urbilaterian origin of the tripartite brain: developmental genetici nsights from Drosophila. Development 2003, 130. 2365-237.
38. Hirsch N., Harris W.A. Xenopus Pax-6 and retinal development. J. Neurobiol. 1997, 32:45-61.
39. Holland L.Z., Kene M., Williams N.A., Holland N.D. Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): the metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development 1997, 124:1723-1732.
40. Holland L.Z., Holland N.D., Schubert M. Developmental expression of AmphiWnt1, an amphioxus gene in the Wnt1/wingless subfamily. Dev. Genes. Evol. 2000, 210:522-524.
41. Holland L.Z., Short S. Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain. Brain Behav. Evol. 2008, 72:91-105.
42. Holland L.Z. Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat. Rev. Neurosci. 2009, 10:736-746.
43. Huang X., Hong C.-S., O'Donnell M., Saint-Jeannet J.-P. The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:11349-11354.
44. Katahira T., Sato T., Sugiyama S., Okafuji T., Araki I., Funahashi J.-I., Nakamura H. Interaction between Otx2 and Gbx2 defines the organizing center for the optic tectum. Mech. Dev. 2000, 91:43-52.
45. Kenyon K.L., Moody S.A., Jamrich M. A novel fork head gene mediates early steps during Xenopus lens formation. Development 1999, 126:5107-5116.
46. Kim C.-H., Oda T., Itoh M., Jiang D., Artinger K.B., Chandrasekharappa S.C., Driever W., Chitnis A.B. Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 2000, 407:913-916.
47. Kobayashi M., Osanai H., Kawakami K., Yamamoto M. Expression of three zebrafish Six4 genes in the cranial sensory placodes and the developing somites. Mech. Dev. 2000, 98:151-155.
48. Kozlowski D.J., Murakami T., Ho R.K., Weinberg E.S. Regional cell movement and tissue patterning in the zebrafish embryo revealed by fate mapping with caged fluorescein. Biochem. Cell Biol. 1997, 75:551-562.
49. 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.
50. Li J.Y.H., Joyner A.L. Otx2 and Gbx2 are required for refinement and not induction of mid-hindbrain gene expression. Development 2001, 128:4979-4991.
51. Li J.Y.H., Lao Z., Joyner A.L. New regulatory interactions and cellular responses in the isthmic organizer region revealed by altering Gbx2 expression. Development 2005, 132:1971-1981.
52. Li B., Kuriyama S., Moreno M., Mayor R. The posteriorizing gene Gbx2 is a direct target of Wnt signalling and the earliest factor in neural crest induction. Development 2009, 136:3267-3278.
53. Lin Z., Cantos R., Patente M., Wu D.K. Gbx2 is required for the morphogenesis of the mouse inner ear: a downstream candidate of hindbrain signaling. Development 2005, 132:2309-2318.
54. McCabe K.L., Bronner-Fraser M. Molecular and tissue interactions governing induction of cranial ectodermal placodes. Dev. Biol. 2009, 332:189-195.
55. McLarren K.W., Litsiou A., Streit A. DLX5 positions the neural crest and pre-placodal region at the border of the neural plate. Dev. Biol. 2003, 259:34-47.
56. Meulemans D., Bronner-Fraser M. Insights from Amphioxus into the evolution of vertebrate cartilage. PLoS ONE 2007, 2:e787.
57. Millet S., Campbell K., Epstein D.J., Losos K., Harris E., Joyner A.L. A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature 1999, 401:161-164.
58. Nakamura H., Watanabe Y. Isthmus organizer and regionalization of the mesencephalon and metencephalon. Int. J. Dev. Biol. 2005, 49:231-235.
59. New D.A.T. A new technique for the cultivation of the chick embryo in vitro. J. Embryol. Exp. Morphol. 1955, 3:326-331.
60. Nieuwkoop P.D., Faber J. Normal table of Xenopus laevis 1967, Daudin, North Holland, Amsterdam. 2nd edn.
61. Northcutt R.G., Gans C. The genesis of neural crest and epidermal placodes: are interpretation of vertebrate origins. Science 1983, 158:1-28.
62. Ogino H., Fisher M., Grainger R.M. Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 2008, 135:249-258.
63. Park B.-Y., Saint-Jeannet J.-P. Expression analysis of Runx3 and other Runx family members during Xenopus development. Gene Expression Pattern 2010, 10:159-166.
64. Patthey C.D., Gunhaga L., Edlund T. Early development of the central and peripheral nervous system is coordinated byWnt and BMP signals. PLoS ONE 2008, 3:e1625.
65. Pieper M., Eagleson G.W., Wosniok W., Schlosser G. Origin and segregation of cranial placodes in Xenopus laevis. Dev. Biol. 2011, 360:257-275.
66. Raible F., Brand M. Divide et impera - the midbrain-hindbrain boundary and its organizer. Trends Neurosci. 2004, 27:727-734.
67. Rhinn M., Dierich A., Shawlot W., Behringer R.R., Le Meur M., Ang S.L. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development 1998, 125:845-856.
68. Sato S., Ikeda K., Shioi G., Ochi H., Ogino H., Yajima H., Kawakami K. Conserved expression of mouse Six1 in the pre-placodal region (PPR) and identification of an enhancer for the rostral PPR. Dev. Biol. 2010, 344:158-171.
69. Schlosser G. Induction and specification of cranial placodes. Dev. Biol. 2006, 294:303-351.
70. Schlosser G. Making Senses: Development of vertebrate cranial placodes. Int. Rev. Cell Mol. Biol. 2010, 283:129-234.
71. Shamim H., Mason I. Expression of Gbx-2 during early development of the chick embryo. Mech. Dev. 1998, 76:157-159.
72. Simeone A., Acampora D., Gulisano M., Stornaiuolo A., Boncinelli E. Nested expression domains of four homeobox genes in developing rostral brain. Nature 1992, 358:687-690.
73. Simeone A., Acampora D., Mallamaci A., Stornaiuolo A., D'Apice M.R., Nigro V., Boncinelli E. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 1993, 12:2735-2747.
74. Steinmetz P.R.H., Zelada-Gonzales F., Burgtorf C., Wittbrodt J., Arendt D. Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation. Proc. Nat. Acad. Sci. 2007, 104:2727-2732.
75. Steinmetz P.R.H., Kostyuchenko R.P., Fischer A., Arendt D. The segmental pattern of Otx, Gbx, and Hox genes in the annelid Platynereis dumerilii. Evol. Dev. 2011, 13:72-79.
76. Stern C.D., Ireland.G.W. An integrated experimental study of endoderm formation in avian embryos. Anat. Embryol. 1981, 163:245-263.
77. Steventon B., Araya C., Linker C., Kuriyama S., Mayor R. Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. Development 2009, 136:771-779.
78. Streit A. Extensive cell movements accompany formation of the otic placode. Dev. Biol. 2002, 249:237-254.
79. Streit A. The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int. J. Dev. Biol. 2007, 51:447-461.
80. Streit A., Sockanathan S., Perez L., Rex M., Scotting P.J., Sharpe P.T., Lovell-Badge R., Stern C.D. Preventing the loss of competence for neural induction: HGF/SF, L5 and Sox-2. Development 1997, 124:1191-1202.
81. Sunmonu N.A., Li K., Guo Q., Li J.Y.H. Gbx2 and Fgf8 are sequentially required for formation of the midbrain-hindbrain compartment boundary. Development 2011, 138:725-734.
82. Tour E., Pillemer G., Gruenbaum Y., Fainsod A. The two Xenopus Gbx2 genes exhibit similar, but not identical expression patterns and can affect head formation. FEBS Lett. 2001, 507:205-209.
83. Tour E., Pillemer G., Gruenbaum Y., Fainsod A. Gbx2 interacts with Otx2 and patterns the anterior-posterior axis during gastrulation in Xenopus. Mech. Dev. 2002, 112:141-151.
84. Tour E., Pillemer G., Gruenbaum Y., Fainsod A. Otx2 can activate the isthmic organizer genetic network in the Xenopus embryo. Mech. Dev. 2002, 110:3-13.
85. Villanueva S., Glavic A., Ruiz P., Mayor R. Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev. Biol. 2002, 241:289-301.
86. von Bubnoff A., Schmidt J.E., Kimelman D. The Xenopus laevis homeobox gene Xgbx-2 is an early marker of anteroposterior patterning in the ectoderm. Mech. Dev. 1996, 54:149-160.
87. Wada H., Escriva H., Zhang S., Laudet V. Conserved RARE localization in amphioxus Hox clusters and implications for hox code evolution in the vertebrate neural crest. Dev. Dyn. 2006, 235:1522-1531.
88. Wakamatsu Y. Mutual repression between Pax3 and Pax6 is involved in the positioning of ophthalmic trigeminal placode in avian embryo. Dev. Growth Differ. 2011, 53:994-1003.
89. Wassarman K.M., Lewandoski M., Campbell K., Joyner A.L., Rubenstein J.L., Martinez S., Martin G.R. Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 1997, 124:2923-2934.
90. Williams N.A., Holland P.W. Gene and domain duplication in the chordate Otx gene family: insights from amphioxus Otx. Mol. Biol. Evol. 1998, 15:600-607.
91. Williams N., Holland P. Old head on young shoulders. Nature 1996, 383:490.
92. Wilson S.W., Houart C. Early steps in the development of the forebrain. Dev. Cell 2004, 6:167-181.
93. Xu H., Dude C.M., Baker C.V.H. Fine-grained fate maps for the ophthalmic and maxillomandibular trigeminal placodes in the chick embryo. Dev. Biol. 2008, 317:174-186.
94. Zervas M., Millet S., Ahn S., Joyner A.L. Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 2004, 43:345-357.