Differentiation of cerebellar cell identities in absence of Fgf signalling in zebrafish Otx morphants

Development

Volumn 133, Issue 10, 2006, Pages 1891-1900

  Foucher, Isabelle ^a   Mione, Marina ^b   Simeone, Antonio ^a,c,d   Acampora, Dario ^a,c,d   Bally Cuif, Laure ^e,f   Houart, Corinne ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cerebellum; Fgf8; Isthmic organizer; Otx2

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; TRANSCRIPTION FACTOR OTX;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL TRANSFORMATION; CEREBELLUM; CONTROLLED STUDY; EMBRYO; GENE FUNCTION; MESENCEPHALON; MORPHOGENESIS; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; ZEBRA FISH;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; EMBRYO, NONMAMMALIAN; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; MESENCEPHALON; MICROINJECTIONS; MUTATION; OLIGONUCLEOTIDES, ANTISENSE; OTX TRANSCRIPTION FACTORS; PYRROLES; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 33745061614     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02352     Document Type: Article

References (77)

1. Acampora, D., Avantaggiato, V., Tuorto, F. and Simeone, A. (1997). Genetic control of brain morphogenesis through Otx gene dosage requirement. Development 124, 3639-3650.
2. Acampora, D., Gulisano, M., Broccoli, V. and Simeone, A. (2001). Otx genes in brain morphogenesis. Prog. Neurobiol. 64, 69-95.
3. Acampora, D., Annino, A., Puelles, E., Alfano, I., Tuorto, F. and Simeone, A. (2003). OTX1 compensates for OTX2 requirement in regionalisation of anterior neuroectoderm. Gene Expr. Patterns 3, 497-501.
4. Adolf, B., Bellipanni, G., Huber, V. and Bally-Cuif, L. (2004). atoh1.2 and beta3.1 are two new bHLH-encoding genes expressed in selective precursor cells of the zebrafish anterior hindbrain. Gene Expr. Patterns 5, 35-41.
5. Alvarado-Mallart, R. M., Martinez, S. and Lance-Jones, C. C. (1990). Pluripotentiality of the 2-day-old avian germinative neuroepithelium. Dev. Biol. 139, 75-88.
6. Bellipanni, G., Murakami, T., Doerre, O. G., Andermann, P. and Weinberg, E. S. (2000). Expression of Otx homeodomain proteins induces cell aggregation in developing zebrafish embryos. Dev. Biol. 223, 339-353.
7. Chi, C. L., Martinez, S., Wurst, W. and Martin, G. R. (2003). The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130, 2633-2644.
8. Cooke, J., Moens, C., Roth, L., Durbin, L., Shiomi, K., Brennan, C., Kimmel, C., Wilson, S. and Holder, N. (2001). Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 128, 571-580.
9. Costagli, A., Kapsimali, M., Wilson, S. W. and Mione, M. (2002). Conserved and divergent patterns of Reelin expression in the zebrafish central nervous system. J. Comp. Neurol. 450, 73-93.
10. Crossley, P. H., Martinez, S. and Martin, G. R. (1996). Midbrain development induced by FGF8 in the chick embryo. Nature 380, 66-68.
11. Echevarria, D., Vieira, C., Gimeno, L. and Martinez, S. (2003). Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res. Brain Res. Rev. 43, 179-191.
12. Eddison, M., Toole, L., Bell, E. and Wingate, R. J. (2004). Segmental identity and cerebellar granule cell induction in rhombomere 1. BMC Biol. 2, 14.
13. Furthauer, M., Reifers, F., Brand, M., Thisse, B. and Thisse, C. (2001). sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish. Development 128, 2175-2186.
14. Furthauer, M., Lin, W., Ang, S. L., Thisse, B. and Thisse, C. (2002). Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat. Cell Biol. 4, 170-174.
15. Garda, A. L., Echevarria, D. and Martinez, S. (2001). Neuroepithelial co-expression of Gbx2 and Otx2 precedes Fgf8 expression in the isthmic organizer. Mech. Dev. 101, 111-118.
16. Gavalas, A., Davenne, M., Lumsden, A., Chambon, P. and Rijli, F. M. (1997). Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3693-3702.
17. Guo, S., Brush, J., Teraoka, H., Goddard, A., Wilson, S. W., Mullins, M. C. and Rosenthal, A. (1999). Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 24, 555-566.
18. Houart, C., Westerfield, M. and Wilson, S. W. (1998). A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature 391, 788-792.
19. Hudson, C., Darras, S., Caillol, D., Yasuo, H. and Lemaire, P. (2003). A conserved role for the MEK signalling pathway in neural tissue specification and posteriorisation in the invertebrate chordate, the ascidian Ciona intestinalis. Development 130, 147-159.
20. Irving, C. and Mason, I. (1999). Regeneration of isthmic tissue is the result of a specific and direct interaction between rhombomere 1 and midbrain. Development 126, 3981-3989.
21. Jaszai, J., Reifers, F., Picker, A., Langenberg, T. and Brand, M. (2003). Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity. Development 130, 6611-6623.
22. Jessell, T. M. and Sanes, J. R. (2000). Development. The decade of the developing brain. Curr. Opin. Neurobiol. 10, 599-611.
23. Kawahara, A., Chien, C. B. and Dawid, I. B. (2002). The homeobox gene mbx is involved in eye and tectum development. Dev. Biol. 248, 107-117.
24. Kawakami, Y., Rodriguez-Leon, J., Koth, C. M., Buscher, D., Itoh, T., Raya, A., Ng, J. K., Esteban, C. R., Takahashi, S., Henrique, D. et al. (2003). MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat. Cell Biol. 5, 513-519.
25. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
26. Koster, R. W. and Fraser, S. E. (2001). Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr. Biol. 11, 1858-1863.
27. Kudoh, T. and Dawid, I. B. (2001). Zebrafish mab21l2 is specifically expressed in the presumptive eye and tectum from early somitogenesis onwards. Mech. Dev. 109, 95-98.
28. Lam, C. S., Sleptsova-Friedrich, I., Munro, A. D. and Korzh, V. (2003). SHH and FGF8 play distinct roles during development of noradrenergic neurons in the locus coeruleus of the zebrafish. Mol. Cell. Neurosci. 22, 501-515.
29. Lannoo, M. J., Ross, L., Maler, L. and Hawkes, R. (1991). Development of the cerebellum and its extracerebellar Purkinje cell projection in teleost fishes as determined by zebrin II immunocytochemistry. Prog. Neurobiol. 37, 329-363.
30. Lecaudey, V., Anselme, I., Dildrop, R., Ruther, U. and Schneider-Maunoury, S. (2005). Expression of the zebrafish Iroquois genes during early nervous system formation and patterning. J. Comp. Neurol. 492, 289-302.
31. Lee, S. M., Danielian, P. S., Fritzsch, B. and McMahon, A. P. (1997). Evidence that FGF8 signalling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124, 959-969.
32. Li, J. Y., Lao, Z. and Joyner, A. L. (2002). Changing requirements for Gbx2 in development of the cerebellum and maintenance of the mid/ hindbrain organizer. Neuron 36, 31-43.
33. Liu, A. and Joyner, A. L. (2001). Early anterior/posterior patterning of the midbrain and cerebellum. Annu. Rev. Neurosci. 24, 869-896.
34. Louvi, A., Alexandre, P., Metin, C., Wurst, W. and Wassef, M. (2003). The isthmic neuroepithelium is essential for cerebellar midline fusion. Development 130, 5319-5330.
35. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
36. Lun, K. and Brand, M. (1998). A series of no isthmus (noi) alleles of the zebrafish pax2.1 gene reveals multiple signaling events in development of the midbrain-hindbrain boundary. Development 125, 3049-3062.
37. Mallamaci, A., Di Blas, E., Briata, P., Boncinelli, E. and Corte, G. (1996). OTX2 homeoprotein in the developing central nervous system and migratory cells of the olfactory area. Mech. Dev. 58, 165-178.
38. Martinez, S., Wassef, M. and Alvarado-Mallart, R. M. (1991). Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene en. Neuron 6, 971-981.
39. Martinez, S., Marin, F., Nieto, M. A. and Puelles, L. (1995). Induction of ectopic engrailed expression and fate change in avian rhombomeres: intersegmental boundaries as barriers. Mech. Dev. 51, 289-303.
40. Martinez, S., Crossley, P. H., Cobos, I., Rubenstein, J. L. and Martin, G. R. (1999). FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 126, 1189-1200.
41. Martinez-Barbera, J. P., Signore, M., Boyl, P. P., Puelles, E., Acampora, D., Gogoi, R., Schubert, F., Lumsden, A. and Simeone, A. (2001). 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, 4789-4800.
42. Martinez-Morales, J. R., Signore, M., Acampora, D., Simeone, A. and Bovolenta, P. (2001). Otx genes are required for tissue specification in the developing eye. Development 128, 2019-2030.
43. Matsumoto, K., Nishihara, S., Kamimura, M., Shiraishi, T., Otoguro, T., Uehara, M., Maeda, Y., Ogura, K., Lumsden, A. and Ogura, T. (2004). The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat. Neurosci. 7, 605-612.
44. Maves, L., Jackman, W. and Kimmel, C. B. (2002). FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129, 3825-3837.
45. McMahon, A. P. and Bradley, A. (1990). The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62, 1073-1085.
46. Mercier, P., Simeone, A., Cotelli, F. and Boncinelli, E. (1995). Expression pattern of two otx genes suggests a role in specifying anterior body structures in zebrafish. Int. J. Dev. Biol. 39, 559-573.
47. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998). An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet 18, 136-141.
48. Millet, S., Bloch-Gallego, E., Simeone, A. and Alvarado-Mallart, R. M. (1996). The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridisation and chick/quail homotopic grafts. Development 122, 3785-3797.
49. Miyamura, Y. and Nakayasu, H. (2001). Zonal distribution of Purkinje cells in the zebrafish cerebellum: analysis by means of a specific monoclonal antibody. Cell Tissue Res. 305, 299-305.
50. Mohammadi, M., McMahon, G., Sun, L., Tang, C., Hirth, P., Yeh, B. K., Hubbard, S. R. and Schlessinger, J. (1997). Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276, 955-960.
51. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
52. Prince, V. E., Moens, C. B., Kimmel, C. B. and Ho, R. K. (1998). Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentino. Development 125, 393-406.
53. Raible, F. and Brand, M. (2004). Divide et Impera - the midbrain-hindbrain boundary and its organizer. Trends Neurosci. 27, 727-734.
54. Reifers, F., Bohli, H., Walsh, E. C., Crossley, P. H., Stainier, D. Y. and Brand, M. (1998). Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125, 2381-2395.
55. Rhinn, M., Lun, K., Amores, A., Yan, Y. L., Postlethwait, J. H. and Brand, M. (2003). Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech. Dev. 120, 919-936.
56. Roehl, H. and Nusslein-Volhard, C. (2001). Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr. Biol. 11, 503-507.
57. Sato, T. and Nakamura, H. (2004). The Fgf8 signal causes cerebellar differentiation by activating the Ras-ERK signaling pathway. Development 131, 4275-4285.
58. Sato, T., Araki, I. and Nakamura, H. (2001). Inductive signal and tissue responsiveness defining the tectum and the cerebellum. Development 128, 2461-2469.
59. Schwarz, M., Alvarez-Bolado, G., Urbanek, P., Busslinger, M. and Gruss, P. (1997). Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: evidence from targeted mutations. Proc. Natl. Acad. Sci. USA 94, 14518-14523.
60. Sotelo, C. (2004). Cellular and genetic regulation of the development of the cerebellar system. Prog. Neurobiol. 72, 295-339.
61. Suda, Y., Matsuo, I. and Aizawa, S. (1997). Cooperation between Otx1 and Otx2 genes in developmental patterning of rostral brain. Mech. Dev. 69, 125-141.
62. Sun, X., Meyers, E. N., Lewandoski, M. and Martin, G. R. (1999). Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 13, 1834-1846.
63. Suzuki-Hirano, A., Sato, T. and Nakamura, H. (2005). Regulation of isthmic Fgf8 signal by sprouty2. Development 132, 257-265.
64. Tallafuss, A. and Bally-Cuif, L. (2003). Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance. Development 130, 4307-4323.
65. Tallafuss, A., Wilm, T. P., Crozatier, M., Pfeffer, P., Wassef, M. and Bally-Cuif, L. (2001). The zebrafish buttonhead-like factor Bts1 is an early regulator of pax2.1 expression during mid-hindbrain development. Development 128, 4021-4034.
66. Trokovic, R., Trokovic, N., Hernesniemi, S., Pirvola, U., Vogt Weisenhorn, D. M., Rossant, J., McMahon, A. P., Wurst, W. and Partanen, J. (2003). FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J. 22, 1811-1823.
67. Wassarman, K. M., Lewandoski, M., Campbell, K., Joyner, A. L., Rubenstein, J. L., Martinez, S. and Martin, G. R. (1997). Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124, 2923-2934.
68. Wechsler-Reya, R. J. and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
69. Westerfield, M. (2000). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: Institute of Neuroscience, University of Oregon.
70. Williams, N. A. and Holland, P. W. (1998). Gene and domain duplication in the chordate Otx gene family: insights from amphioxus Otx. Mol. Biol. Evol. 15, 600-607.
71. Wilson, S. W. and Houart, C. (2004). Early steps in the development of the forebrain. Dev. Cell 6, 167-181.
72. Wingate, R. J. and Hatten, M. E. (1999). The role of the rhombic lip in avian cerebellum development. Development 126, 4395-4404.
73. Wullimann, M. F., Rupp, B. and Reichert, H. (1996). Neuroanatomy of the Zebrafish Brain: A Topological Atlas. Basel, Boston, Berlin: Birkhauser Verlag.
74. Wurst, W. and Bally-Cuif, L. (2001). Neural plate patterning: upstream and downstream of the isthmic organizer. Nat. Rev. Neurosci. 2, 99-108.
75. Wurst, W., Auerbach, A. B. and Joyner, A. L. (1994). Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065-2075.
76. Xu, J., Liu, Z. and Ornitz, D. M. (2000). Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127, 1833-1843.
77. Zervas, M., Millet, S., Ahn, S. and Joyner, A. L. (2004). Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43, 345-357.