The duration of Fgf8 isthmic organizer expression is key to patterning different tectal-isthmo-cerebellum structures

Development

Volumn 136, Issue 21, 2009, Pages 3617-3626

  Sato, Tatsuya ^a,b   Joyner, Alexandra L ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

Fgf17; Fibroblast growth factors; Inferior colliculus; Mice

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 17; FIBROBLAST GROWTH FACTOR 8; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL TRANSFORMATION; CEREBELLUM; CONTROLLED STUDY; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; INFERIOR COLLICULUS; MESENCEPHALON; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SUPERIOR COLLICULUS; TECTUM;

ANIMALS; BODY PATTERNING; CEREBELLUM; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; OTX TRANSCRIPTION FACTORS; TECTUM MESENCEPHALI; WNT1 PROTEIN;

MUS;

EID: 70350160202     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.041210     Document Type: Article

References (61)

1. Acampora, D., Mazan, S., Lallemand, Y., Avantaggiato, V., Maury, M., Simeone, A. and Brǔlet, P. (1995). Forebrain and midbrain regions are deleted in Otx2-/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290.
2. Ang, S. L., Conlon, R. A., Jin, O. and Rossant, J. (1994). Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120, 2979-2989.
3. Ang, S. L., Jin, O., Rhinn, M., Daigle, N., Stevenson, L. and Rossant, J. (1996). A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252.
4. Basson, A. M., Echevarria, D., Ahn, C. P., Sudarov, A., Joyner, A. L., Mason, I. J., Martinez, S. and Martin, G. R. (2008). Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135, 889-898.
5. Blaess, S., Corrales, J. D. and Joyner, A. L. (2006). Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133, 1799-1809.
6. Blunt, A. G., Lawshe, A., Cunningham, M. L., Seto, M. L., Ornitz, D. M. and MacArthur, C. A. (1997). Overlapping expression and redundant activation of mesenchymal fibroblast growth factor (FGF) receptors by alternatively spliced FGF-8 ligands. J. Biol. Chem. 272, 3733-3738.
7. Broccoli, V., Boncinelli, E. and Wurst, W. (1999). The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401, 164-168.
8. Brodski, C., Weisenhorn, D. M., Signore, M., Sillaber, I., Oesterheld, M., Broccoli, V., Acampora, D., Simeone, A. and Wurst, W. (2003). Location and size of dopaminergic and serotonergic cell populations are controlled by the position of the midbrain-hindbrain organizer. J. Neurosci. 23, 4199-4207.
9. Chi, C., Martinez, S., Wurst, W. and Martin, G. R. (2003). The isthmicorganizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130, 2633-2644.
10. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
11. Crossley, P. H., Martinez, S. and Martin, G. R. (1996). Midbrain development induced by FGF8 in the chick embryo. Nature 380, 66-68.
12. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. and McMahon, A. P. (1998). Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323-1326.
13. Feil, R., Brocard, J., Mascrez, B., LeMeur, M., Metzger, D. and Chambon, P. (1996). Ligand-activated site-specific recombination in mice. Proc. Natl. Acad. Sci. USA 93, 10887-10890.
14. Feil, R., Wagner, J., Metzger, D. and Chambon, P. (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237, 752-757.
15. Foucher, I., Mione, M., Simeone, A., Acampora, D., Bally-Cuif, L. and Houart, C. (2006). Differentiation of cerebellar cell identities in absence of Fgf signalling in zebrafish Otx morphants. Development 133, 1891-1900.
16. Grieshammer, U., Cebrián, C., Ilagan, R., Meyers, E., Herzlinger, D. and Martin, G. R. (2005). FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132, 3847-3857.
17. Guo, Q. and Li, J. Y. (2007). Distinct functions of the major Fgf8 spliceform, Fgf8b, before and during mouse gastrulation. Development 134, 2251-2260.
18. Jaszai, J., Reifers, F., Picker, A., Langenberg, T. and Brand, M. (2003). Isthmusto-midbrain transformation in the absence of midbrain-hindbrain organizer activity. Development 130, 6611-6623.
19. Joyner, A. L., Liu, A. and Millet, S. (2000). Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr. Opin. Cell Biol. 12, 736-741.
20. Katahira, T., Sato, T., Sugiyama, S., Okafuji, T., Araki, I., Funahashi, J. and Nakamura, H. (2000). Interaction between Otx2 and Gbx2 defines the organizing center for the optic tectum. Mech. Dev. 91, 43-52.
21. Larsell, O. (1952). The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J. Comp. Neurol. 97, 281-356.
22. 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.
23. Lewandoski, M., Sun, X. and Martin, G. R. (2000). Fgf8 signaling from the AER is essential for normal limb development. Nat. Genet. 26, 460-463.
24. Li, J., 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.
25. Liu, A. and Joyner, A. L. (2001). EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 128, 181-191.
26. Liu, A., Losos, K. and Joyner, A. L. (1999). FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development 126, 4827-4838.
27. Liu, Z., Xu, J., Colvin, J. S. and Ornitz, D. M. (2002). Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev. 16, 859-869.
28. Liu, A., Li, J. Y. H., Bromleigh, C., Lao, Z., Niswander, L. A. and Joyner, A. L. (2003). FGF17 and FGF18 have different midbrain regulatory properties from FGF8b and activated FGF Receptors. Development 130, 6175-6185.
29. Martínez, S. (2001). The isthmic organizer and brain regionalization. Int. J. Dev. Biol. 45, 367-371.
30. 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.
31. 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.
32. Maruoka, Y., Ohbayashi, N., Hoshikawa, M., Itoh, N., Hogan, B. M. and Furuta, Y. (1998). Comparison of the expression of three highly related genes, Fgf8, Fgf17 and Fgf18, in the mouse embryo. Mech. Dev. 74, 175-177.
33. Matsunaga, E., Katahira, T. and Nakamura, H. (2002). Role of Lmx1b and Wnt1 in mesencephalon and metencephalon development. Development 129, 5269-5277.
34. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N. and Aizawa, S. (1995). Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9, 2646-2658.
35. 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.
36. Millet, S., Campbell, K., Epstein, D. J., Losos, K., Harris, E. and Joyner, A. L. (1999). A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature 401, 161-164.
37. Minowada, G., Jarvis, L. A., Chi, C. L., Neubuser, A., Sun, X., Hacohen, N., Krasnow, M. A. and Martin, G. R. (1999). Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475.
38. Nakamura, H. (2001). Regionalization of the optic tectum: combinations of gene expression that define the tectum. Trends Neurosci. 24, 32-39.
39. Nakamura, H., Sato, T. and Suzuki-Hirano, A. (2008). Isthmus organizer for mesencephalon and metencephalon. Dev. Growth Differ. 50, 113-118.
40. Ohbayashi, N., Shibayama, M., Kurotaki, Y., Imanishi, M., Fujimori, T., Itoh, N. and Takada, S. (2002). FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 16, 870-879.
41. Olsen, S. K., Li, J. Y. H., Bromleigh, C., Eliseenkova, A. V., Ibrahimi, O., Lao, Z., Zhang, F., Linhardt, R. J., Joyner, A. L. and Mohammadi, M. (2006). Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 20, 185-198.
42. Parr, B. A., Shea, M. J., Vassileva, G. and McMahon, A. P. (1993). Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247-261.
43. Prakash, N., Brodski, C., Naserke, T., Puelles, E., Gogoi, R., Hall, A., Panhuysen, M., Echevarria, D., Sussel, L., Weisenhorn et al. (2006). A Wnt1-regulated genetic network controls the identity and fate of midbrain-dopaminergic progenitors in vivo. Development 133, 89-98.
44. Rhinn, M. and Brand, M. (2001). The midbrain-hindbrain boundary organizer. Curr. Opin. Neurobiol. 11, 34-42.
45. 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.
46. Robinson, S. P., Langan-Fahey, S. M., Johnson, D. A. and Jordan, V. C. (1991). Metabolites, pharmacodynamics, and pharmacokinetics of tamoxifen in rats and mice compared to the breast cancer patient. Drug Metab. Dispos. 19, 36-34.
47. Saarimäki-Vire, J., Peltopuro, P., Lahti, L., Naserke, T., Blak, A. A., Vogt Weisenhorn, D. M., Yu, K., Ornitz, D. M., Wurst, W. and Partanen, J. (2007). Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J. Neurosci. 27, 8581-8592.
48. Sato, T. and Nakamura, H. (2004). The Fgf8 signal causes cerebellar differentiation by activating Ras-ERK signaling pathway. Development 131, 4275-4285.
49. Sato, T., Araki, I. and Nakamura, H. (2001). Inductive signal and tissue responsiveness defining the tectum and the cerebellum. Development 128, 2461-2469.
50. Sato, T., Joyner, A. L. and Nakamura, H. (2004). How does Fgf signaling from the isthmic organizer induce midbrain and cerebellum development? Dev. Growth Differ. 46, 487-494.
51. Sgaier, S. K., Millet, S., Villanueva, M. P., Berenshteyn, F., Song, C., Joyner, A. L. (2005). Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45, 27-40.
52. Shamim, H., Mahmood, R., Logan, C., Doherty, P., Lumsden, A. and Mason, I. (1999). Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 126, 945-959.
53. Simeone, A. (2000). Positioning the isthmic organizer where Otx2 and Gbx2 meet. Trends Genet. 16, 237-240.
54. Suzuki-Hirano, A., Sato, T. and Nakamura, H. (2005). Regulation of isthmic Fgf8 signal by sprouty2. Development 132, 257-265.
55. 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 forsustained response to isthmic signals. EMBO J. 22, 1811-1823.
56. 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.
57. Wurst, W. and Bally-Cuif, L. (2001). Neural plate patterning: upstream and downstream of the isthmic organizer. Nat. Rev. Neurosci. 2, 99-108.
58. 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.
59. Xu, J., Lawshe, A., MacArthur, C. A. and Ornitz, D. M. (1999). Genomic structure, mapping, activity and expression of fibroblast growth factor 17. Mech. Dev. 83, 165-178.
60. Ye, W., Shimamura, K., Rubenstein, J. L., Hynes, M. A. and Rosenthal, A. (1998). FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766.
61. 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.