The tale of the three brothers - Shh, Wnt, and Fgf during development of the thalamus

Frontiers in Neuroscience

Volumn , Issue MAY, 2012, Pages

  Hagemann, Anja I H ^a   Scholpp, Steffen ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Development; Diencephalon; Fgf; Forebrain; Shh; Thalamus; Wnt; Zebrafish

Indexed keywords

FIBROBLAST GROWTH FACTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

BRAIN DEVELOPMENT; BRAIN REGION; CELL ADHESION; CHICKEN; ENZYME ACTIVITY; GENE EXPRESSION; MID DIENCEPHALIC ORGANIZER; MORPHOLOGY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; THALAMUS; ZEBRA FISH;

EID: 84862228793     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00076     Document Type: Review

References (77)

1. Acampora, D., Avantaggiato, V., Tuorto, E, and Simeone, A. (1997). Genetic control of brain morphogenesis through Otx gene dosage requirement. Development 124, 3639-3650.
2. Ando, H., Kobayashi, M., Tsubokawa, T., Uyemura, K., Furuta, T., and Okamoto, H. (2005). Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev. Biol. 287, 456-468.
3. Bachy, I., Vernier, P., and Retaux, S. (2001). The LIM-homeodomain gene family in the developing Xeno-pus brain: conservation and divergences with the mouse related to the evolution of the forebrain. j. Neurosci. 21,7620-7629.
4. Barth, K. A., and Wilson, S. W. (1995). Expression of zebrafish nk2.2 is influenced by sonic hedgehog/ vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768.
5. Bergquist, H. (1932). Zur Morpholo-gie Des Zwischenhirns Bei Niederen Wirbeltieren Stockholm. Acta Zool. 1,74-221.
6. Bienz, M. (2005). Beta-Catenin: a pivot between cell adhesion and Wnt signalling. Curr. Biol. 15, R64-R67.
7. Bluske, K. K., Kawakami, Y., koyano-Nakagawa, N., and Nakagawa, Y. (2009). Differential activity of Wnt/beta-catenin signaling in the embryonic mouse thalamus. Dev. Dyn. 238, 3297-3309.
8. Braun, M. M., Etheridge, A., Bernard, A., Robertson, C. P., and Roelink, H. (2003). Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development 130, 5579-5587.
9. Chapouton, P., Webb, K. J., Stigloher, C, Alunni, A., Adolf, B., Hesl, B., Krem-mer, E., and Bally-Cuif, L. (2011). Expression of hairy/enhancer of split genes in neural progenitors and neurogenesis domains of the adult zebrafish brain.j. Cotnp. Neurol. 519, 1748-1769.
10. Chen, L., Guo, Q., and Li, J. Y. (2009). Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus. Development 136, 1317-1326.
11. Echevarria, D., Vieira, C, Gimeno, L., and Martinez, S. (2003). Neuroep-ithelial secondary organizers and cell fate specification in the developing brain. Brain Res. Brain Res. Rev. 43, 179-191.
12. Freese, J. L., Pino, D., and Pleasure, S. J. (2010). Wnt signaling in development and disease. Neurobiol. Dis. 38, 148-153.
13. Garcia-Lopez, R., Vieira, C, Echevarria, D., and Martinez, S. (2004). Fate map of the diencephalon and the zona limitans at the 10-somites stage in chick embryos. Dev. Biol. 268, 514-530.
14. Gimeno, L., and Martinez, S. (2007). Expression of chick Fgf 19 and mouse Fgf 15 orthologs is regulated in the developing brain by Fgf8 and Shh. Dev. Dyn. 236, 2285-2297.
15. Guinazu, M. E, Chambers, D., Lumsden, A., and Kiecker, C. (2007). Tissue interactions in the developing chick diencephalon. Neural Dev. 2,25.
16. Hans, S., Scheer, N., Riedl, I. V., Weiz-sacker, E., Blader, P., and Campos-Ortega, J. A. (2004). her3, a zebrafish member of the hairy-E(spl) family, is repressed by Notch signalling. Development 131,2957-2969.
17. Hashimoto, H., Yabe, T., Hirata, T., Shimizu, T., Bae, Y., Yamanaka, Y, Hirano, T., and Hibi, M. (2000). Expression of the zinc finger gene fez-like in zebrafish forebrain. Meek Dev. 97, 191-195.
18. Hashimoto-Torii, K., Motoyama, J., Hui, C. C, Kuroiwa, A., Nakafuku, M., and Shimamura, K. (2003). Differential activities of Sonic hedgehog mediated by Gli transcription factors define distinct neuronal subtypes in the dorsal thalamus. Meek Dev. 120, 1097-1111.
19. HebertJ.M. (2011).FGFs:Neurodevel-opmenfs Jack-of-all-Trades - how do they do it? Front. Neurosci. 5:133. doi:10.3389/fnins.2011.00133
20. Hirano, S., Yan, Q., and Suzuki, S. T. (1999). Expression of a novel pro-tocadherin, OL-protocadherin, in a subset of functional systems of the developing mouse brain. j. Neurosci. 19,995-1005.
21. Hirata, T., Nakazawa, M., Muraoka, O., Nakayama, R., Suda, Y, and Hibi, M. (2006). Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development 133,3993-4004.
22. Huber, O., Bierkamp, C, and Kemler, R. (1996). Cadherins and catenins in development. Curr. Opin. Cell Biol. 8,685-691.
23. Ishibashi, M., and McMahon, A. P. (2002). A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mes-encephalic primordia in the early mouse embryo. Development 129, 4807-4819.
24. Jeong, J. Y, Einhorn, Z., Mathur, P., Chen, L., Lee, S., Kawakami, K., and Guo, S. (2007). Patterning the zebrafish diencephalon by the conserved zinc-finger protein Fezl. Development 134,127-136.
25. Jeong, Y, Dolson, D. K., Waclaw, R. R., Matise, M. P., Sussel, L., Campbell, K., Kaestner, K. H., and Epstein, D. J. (2011). Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development 138,531-541.
26. Jones, E. G., and Rubenstein, J. L. (2004). Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. j. Comp. Neurol. 477, 55-80.
27. Kataoka, A., and Shimogori, T. (2008). Fgf8 controls regional identity in the developing thalamus. Development 135,2873-2881.
28. Kiecker, C, and Lumsden, A. (2004). Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat. Neurosci. 7,1242-1249.
29. Kim, S. Y, Yasuda, S., Tanaka, H., Yama-gata, K., and Kim, H. (2011). Non-clustered protocadherin. Cell Adk Migr. 5, 97-105.
30. Lakhina, V., Falnikar, A., Bhatnagar, L., and Tole, S. (2007). Early thalam-ocortical tract guidance and topographic sorting of thalamic projections requires LIM-homeodomain gene Lhx2. Dev. Biol. 306, 703-713.
31. Lee, S. K., and Pfaff, S. L. (2003). Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and home-odomain transcription factors. Neuron 38, 731-745.
32. Mangale, V. S., Hirokawa, K. E., Satyaki, P. R., Gokulchandran, N., Chikbire, S., Subramanian, L., Shetty, A. S., Martynoga, B., Paul, J., Mai, M. V., Li, Y, Flanagan, L. A., Tole, S., and Monuki, E. S. (2008). Lhx2 selector activity specifies cortical identity and suppresses hippocam-pal organizer fate. Science 319, 304-309.
33. Martinez-Ferre, A., and Martinez, S. (2009). The development of the thalamic motor learning area is regulated by Fgf8 expression. j. Neurosci. 29,13389-13400.
34. Matsuo-Takasaki, M., Lim, J. H., Beanan, M. J., Sato, S. M., and Sargent, T. D. (2000). Cloning and expression of a novel zinc finger gene, Fez, transcribed in the forebrain of Xenopus and mouse embryos. Meek Dev. 93, 201-204.
35. Mattes, B., Weber, S., Chen, Q., Davidson, G., Houart, C, and Scholpp, S. (2012). Wnt3 and Wnt3a are required for induction of the mid-diencephalic organizer in the caudal forebrain. Neural Dev. 7, 12.
36. Meinhardt, H. (2009). Models for the generation and interpretation of gradients. Cold Spring Harb. Per-spect. Biol. 4, 1-14.
37. Miyake, A., Nakayama, Y, Konishi, M., and Itoh, N. (2005). Fgfl9 regulated by Hh signaling is required for zebrafish forebrain development. Dev. Biol. 288, 259-275.
38. Miyashita-Lin, E. M., Hevner, R., Was-sarman, K. M., Martinez, S., and Rubenstein, J. L. (1999). Early neocortical regionalization in the absence of thalamic innervation. Science 285, 906-909.
39. Moreno, N., Bachy, I., Retaux, S., and Gonzalez, A. (2004). LIM-homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions. j. Comp. Neurol. 472, 52-72.
40. Murakami, T., Hijikata, T., Matsukawa, M., Ishikawa, H., and Yorifuji, H. (2006). Zebrafish protocadherin 10 is involved in paraxial meso-derm development and somitogen-esis. Dev. Dyn. 235, 506-514.
41. Murray, K. D., Choudary, P. V., and Jones, E. G. (2007). Nucleus- and cell-specific gene expression in monkey thalamus. Proc. Natl. Acad. Sci. U.S.A. 104, 1989-1994.
42. Nakagawa, Y, and O'Leary, D. D. (2001). Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. j. Neurosci. 21, 2711-2725.
43. Nakao, S., Uemura, M., Aoki, E., Suzuki, S. T., Takeichi, M., and Hirano, S. (2005). Distribution of OL-protocadherin in axon fibers in the developing chick nervous system. Brain Res. Mol. Brain Res. 134, 294-308.
44. Osorio, J., Mazan, S., and Retaux, S. (2005). Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from. LIM-homeodomain, Pax and hedgehog genes. Dev. Biol. 288, 100-112.
45. Peng, G., and Westerfield, M. (2006). Lhx5 promotes forebrain development and activates transcription of secreted Wnt antagonists. Development 133,3191-3200.
46. Peukert, D., Weber, S., Lumsden, A., and Scholpp, S. (2011). Lhx2 and Ihx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating wnt signaling. PLoS Biol. 9, el001218. doi:10.1371/joumal.pbio.l001218
47. Potter, P. E., Thorne, B., and Gaughan, C. (1997). Modulation of hip-pocampal norepinephrine release by cholinergic agonists is altered by AF64A lesion. Brain Res. Bull. 42, 153-160.
48. Puelles, L., and Martinez-de-la-Torre, M. (1987). Autoradiographic and Golgi study on the early development of n. Isthmi principalis and adjacent grisea in the chick embryo: a tridimensional viewpoint. Anat. Embryol. (Bert) 176, 19-34.
49. Puelles, L., and Rubenstein, J. L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16,472-479.
50. Puelles, L., and Rubenstein, J. L. (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 26, 469-476.
51. Quinlan, R., Graf, M., Mason, I., Lumsden, A., and Kiecker, C. (2009). Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev. 4, 35.
52. Redies, C, Ast, M., Nakagawa, S., Takeichi, M., Martinez-de-la-Torre, M., and Puelles, L. (2000). Morphologic fate of diencephalic prosomeres and their subdivisions revealed by mapping cadherin expression. j. Comp. Neurol. 421, 481-514.
53. Ruiz, I., and Altaba, A. (1998). Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125, 2203-2212.
54. Salinas, P. C, and Nusse, R. (1992). Regional expression of the Wnt-3 gene in the developing mouse forebrain in relationship to diencephalic neuromeres. Meek. Dev. 39, 151-160.
55. Schambony,A.,and Wedlich,D. (2007). Wnt-5A/Ror2 regulate expression of XPAPC through an alternative non-canonical signaling pathway. Dev. Cell 12, 779-792.
56. Scholpp, S., Delogu, A., Gilthorpe, J., Peukert, D., Schindler, S., and Lums-den, A. (2009). Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc. Natl Acad. Sci. U.S.A. 106, 19895-19900.
57. Scholpp, S., Foucher, I., Staudt, N., Peukert, D., Lumsden, A., and Houart, C. (2007). Otxll, Otx2 and Irxlb establish and position the ZLI in the diencephalon. Development 134,3167-3176.
58. Scholpp, S., and Lumsden, A. (2010). Building a bridal chamber: development of the thalamus. Trends Neu-rosci. 33, 373-380.
59. Scholpp, S., Wolf, O., Brand, M., and Lumsden, A. (2006). Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development 133, 855-864.
60. Seibt, J., Schuurmans, C, Gradwhol, G., Dehay, C, Vanderhaeghen, P., Guillemot, E, and Polleux, E (2003). Neurogenin2 specifies the connectivity of thalamic neurons by controlling axon responsiveness to intermediate target cues. Neuron 39, 439-452.
61. Seth, A., Culverwell, J., Walkowicz, M., Toro, S., Rick, J. M., Neuhauss, S. C, Varga, Z. M., and Karlstrom, R. O. (2006). Belladonna/(Ihx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 133, 725-735.
62. Shimamura, K., Hartigan, D. J., Martinez, S., Puelles, L., and Ruben-stein, J. L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121,3923-3933.
63. Shimogori, T., Vansant, J., Paik, E., and Grove, E. A. (2004). Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. j. Comp. Neurol 473, 496-510.
64. Staudt, N., and Houart, C. (2007). The prethalamus is established during gastrulation and influences diencephalic region-alization. PLoS Biol. 5, e69. doi:10.1371/joumal.pbio.0050069
65. Suzuki-Hirano, A., Ogawa, M., Kataoka, A., Yoshida, A. C, Itoh, D., Ueno, M., Blackshaw, S., and Shimogori, T. (2011). Dynamic spatiotempo-ral gene expression in embryonic mouse thalamus. j. Comp. Neurol. 519,528-543.
66. Szabo, N. E., Zhao, T., Zhou, X., and Alvarez-Bolado, G. (2009). The role of Sonic hedgehog of neural origin in thalamic differentiation in the mouse. j. Neurosci. 29,2453-2466.
67. Takatori, N., Butts, T., Candiani, S., Pes-tarino, M., Ferrier, D. E., Saiga, H., and Holland, P. W. (2008). Comprehensive survey and classification of homeobox genes in the genome of amphioxus, Branchiostoma floridae. Dev. Genes Evol. 218,579-590.
68. Takeichi, M. (1977). Functional correlation between cell adhesive properties and some cell surface proteins. j. Cell Biol. 75, 464-474.
69. Vieira, C, Garda, A. L., Shimamura, K., and Martinez, S. (2005). Thalamic development induced by Shh in the chick embryo. Dev. Biol. 284, 351-363.
70. Vue, T. Y., Aaker, J., Taniguchi, A., Kazemzadeh, C, Skidmore, J. M., Martin, D. M., Martin, J. E, Treier, M., and Nakagawa, Y. (2007). Characterization of progenitor domains in the developing mouse thalamus. j. Comp. Neurol. 505, 73-91.
71. Vue, T. Y, Bluske, K., Alishahi, A., Yang, L. L., Koyano-Nakagawa, N., Novitch, B., and Nakagawa, Y (2009). Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. j. Neurosci. 29,4484-4497.
72. Wall, D. S., Mears, A. J., Mcneill, B., Mazerolle, C, Thurig, S., Wang, Y., Kageyama, R., and Wallace, V. A. (2009). Progenitor cell proliferation in the retina is dependent on Notch-independent Sonic hedgehog/Hesl activity.j. Cell Biol. 184, 101-112.
73. Walshe, J., and Mason, I. (2003). Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish fore-brain development. Development 130,4337-4349.
74. Wilson, S. W., and Houart, C. (2004). Early steps in the development of the forebrain. Dev. Cell 6,167-181.
75. Wisniewska, M. B., Misztal, K., Michowski, W, Szczot, M., Purta, E., Lesniak, W., Klejman, M. E., Dabrowski, M., Filipkowski, R. K., Nagalski, A., Mozrzymas, J. W, and Kuznicki, J. (2011). LEFl/beta-catenin complex regulates transcription of the Cav3.1 calcium channel gene (Cacnalg) in thalamic neurons of the adult brain. j. Neurosci. 30, 4957-4969.
76. Zeltser, L. M., Larsen, C. W, and Lumsden, A. (2001). A new developmental compartment in the forebrain regulated by Lunatic fringe. Nat. Neurosci. 4, 683-684.
77. Zhou, C. J., Pinson, K. I., and Pleasure, S. J. (2004). Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. j. Neurosci. 24, 7632-7639.