Zinc finger genes Fezf1 and Fezf2 control neuronal differentiation by repressing Hes5 expression in the forebrain

Development

Volumn 137, Issue 11, 2010, Pages 1875-1885

  Shimizu, Takeshi ^a,e   Nakazawa, Masato ^a   Kani, Shuichi ^a   Bae, Young Ki ^a,d   Shimizu, Takashi ^a,c   Kageyama, Ryoichiro ^b   Hibi, Masahiko ^a,c  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d National Cancer Center   (South Korea)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Corticogenesis; Fezf1; Fezf2; Hes5; Mouse; Neurogenesis; Neurogenin 2; Zinc finger genes

Indexed keywords

NEUROGENIN 2; ZINC FINGER PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; FEXF1 GENE; FEZF2 GENE; FOREBRAIN; GENE; GENE REPRESSION; HES5 GENE; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TELENCEPHALON;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; DNA PRIMERS; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PREGNANCY; PROMOTER REGIONS, GENETIC; PROSENCEPHALON; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; TELENCEPHALON; ZINC FINGERS;

EID: 77952172670     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.047167     Document Type: Article

References (83)

1. Aboitiz, F., Montiel, J. and Garcia, R. R. (2005). Ancestry of the mammalian preplate and its derivatives: evolutionary relicts or embryonic adaptations? Rev. Neurosci. 16, 359-376. (Pubitemid 43185086)
2. Adolf, B., Chapouton, P., Lam, C. S., Topp, S., Tannhauser, B., Strahle, U., Gotz, M. and Bally-Cuif, L. (2006). Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev. Biol. 295, 278-293. (Pubitemid 44041332)
3. Alcamo, E. A., Chirivella, L., Dautzenberg, M., Dobreva, G., Farinas, I., Grosschedl, R. and McConnell, S. K. (2008). Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57, 364-377. (Pubitemid 351179160)
4. Alcantara, S., Ruiz, M., D'Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C. and Soriano, E. (1998). Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18, 7779-7799. (Pubitemid 28441019)
5. Allendoerfer, K. L. and Shatz, C. J. (1994). The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci. 17, 185-218.
6. Arimatsu, Y., Ishida, M., Kaneko, T., Ichinose, S. and Omori, A. (2003). Organization and development of corticocortical associative neurons expressing the orphan nuclear receptor Nurr1. J. Comp. Neurol. 466, 180-196. (Pubitemid 37255228)
7. Arlotta, P., Molyneaux, B. J., Jabaudon, D., Yoshida, Y. and Macklis, J. D. (2008). Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J. Neurosci. 28, 622-632.
8. Arnold, S. J., Huang, G. J., Cheung, A. F., Era, T., Nishikawa, S., Bikoff, E. K., Molnar, Z., Robertson, E. J. and Groszer, M. (2008). The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev. 22, 2479-2484.
9. Berberoglu, M. A., Dong, Z., Mueller, T. and Guo, S. (2009). fezf2 expression delineates cells with proliferative potential and expressing markers of neural stem cells in the adult zebrafish brain. Gene Expr. Patterns 9, 411-422.
10. Bicknese, A. R., Sheppard, A. M., O'Leary, D. D. and Pearlman, A. L. (1994). Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci. 14, 3500-3510.
11. Bielle, F., Griveau, A., Narboux-Neme, N., Vigneau, S., Sigrist, M., Arber, S., Wassef, M. and Pierani, A. (2005). Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat. Neurosci. 8, 1002-1012.
12. Britanova, O., de Juan Romero, C., Cheung, A., Kwan, K. Y., Schwark, M., Gyorgy, A., Vogel, T., Akopov, S., Mitkovski, M., Agoston, D. et al. (2008). Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378-392.
13. Cau, E., Gradwohl, G., Casarosa, S., Kageyama, R. and Guillemot, F. (2000). Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127, 2323-2332.
14. Chen, B., Schaevitz, L. R. and McConnell, S. K. (2005a). Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl. Acad. Sci. USA 102, 17184-17189.
15. Chen, B., Wang, S. S., Hattox, A. M., Rayburn, H., Nelson, S. B. and McConnell, S. K. (2008). The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc. Natl. Acad. Sci. USA 105, 11382-11387.
16. Chen, J. G., Rasin, M. R., Kwan, K. Y. and Sestan, N. (2005b). Zfp312 is required for subcortical axonal projections and dendritic morphology of deeplayer pyramidal neurons of the cerebral cortex. Proc. Natl. Acad. Sci. USA 102, 17792-17797.
17. Chenn, A. and McConnell, S. K. (1995). Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641.
18. D'Arcangelo, G., Miao, G. G., Chen, S. C., Soares, H. D., Morgan, J. I. and Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719-723.
19. del Rio, J. A., Martinez, A., Fonseca, M., Auladell, C. and Soriano, E. (1995). Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb. Cortex 5, 13-21.
20. Dolbeare, F., Gratzner, H., Pallavicini, M. G. and Gray, J. W. (1983). Flow cytometric measurement of total DNA content and incorporated bromodeoxyuridine. Proc. Natl. Acad. Sci. USA 80, 5573-5577.
21. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251.
22. Fode, C., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C. and Guillemot, F. (1998). The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 20, 483-494.
23. Gaiano, N. and Fishell, G. (2002). The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471-490.
24. Gotz, M. and Huttner, W. B. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
25. Gotz, M., Stoykova, A. and Gruss, P. (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031-1044.
26. Grandel, H., Kaslin, J., Ganz, J., Wenzel, I. and Brand, M. (2006). Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 295, 263-277.
27. Guo, S., Wilson, S. W., Cooke, S., Chitnis, A. B., Driever, W. and Rosenthal, A. (1999). Mutations in the zebrafish unmask shared regulatory pathways controlling the development of catecholaminergic neurons. Dev. Biol. 208, 473-487.
28. 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. Mech. Dev. 97, 191-195.
29. Hatakeyama, J., Bessho, Y., Katoh, K., Ookawara, S., Fujioka, M., Guillemot, F. and Kageyama, R. (2004). Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131, 5539-5550.
30. Hevner, R. F., Shi, L., Justice, N., Hsueh, Y., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T. and Rubenstein, J. L. (2001). Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366.
31. Hirata, T., Suda, Y., Nakao, K., Narimatsu, M., Hirano, T. and Hibi, M. (2004). Zinc finger gene fez-like functions in the formation of subplate neurons and thalamocortical axons. Dev. Dyn. 230, 546-556.
32. Hirata, T., Nakazawa, M., Muraoka, O., Nakayama, R., Suda, Y. and Hibi, M. (2006a). Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development 133, 3993-4004.
33. Hirata, T., Nakazawa, M., Yoshihara, S., Miyachi, H., Kitamura, K., Yoshihara, Y. and Hibi, M. (2006b). Zinc-finger gene Fez in the olfactory sensory neurons regulates development of the olfactory bulb non-cell- autonomously. Development 133, 1433-1443.
34. Hoerder-Suabedissen, A., Wang, W. Z., Lee, S., Davies, K. E., Goffinet, A. M., Rakic, S., Parnavelas, J., Reim, K., Nicolic, M., Paulsen, O. et al. (2009). Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb. Cortex 19, 1738-1750.
35. Imayoshi, I., Shimogori, T., Ohtsuka, T. and Kageyama, R. (2008). Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 135, 2531-2541.
36. Inoue, K., Terashima, T., Nishikawa, T. and Takumi, T. (2004). Fez1 is layer-specifically expressed in the adult mouse neocortex. Eur. J. Neurosci. 20, 2909-2916.
37. 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.
38. Kageyama, R., Ohtsuka, T., Hatakeyama, J. and Ohsawa, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306, 343-348.
39. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251.
40. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2008a). Roles of Hes genes in neural development. Dev. Growth Differ. 50 Suppl. 1, S97-S103.
41. Kageyama, R., Ohtsuka, T., Shimojo, H. and Imayoshi, I. (2008b). Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 11, 1247-1251.
42. Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T. and Matsuzaki, F. (2008). Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101.
43. Kowalczyk, T., Pontious, A., Englund, C., Daza, R. A., Bedogni, F., Hodge, R., Attardo, A., Bell, C., Huttner, W. B. and Hevner, R. F. (2009). Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19, 2439-2450.
44. Kubbutat, M. H., Key, G., Duchrow, M., Schluter, C., Flad, H. D. and Gerdes, J. (1994). Epitope analysis of antibodies recognising the cell proliferation associated nuclear antigen previously defined by the antibody Ki-67 (Ki-67 protein). J. Clin. Pathol. 47, 524-528.
45. Lai, T., Jabaudon, D., Molyneaux, B. J., Azim, E., Arlotta, P., Menezes, J. R. and Macklis, J. D. (2008). SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57, 232-247.
46. Lee, M. K., Tuttle, J. B., Rebhun, L. I., Cleveland, D. W. and Frankfurter, A. (1990). The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton 17, 118-132.
47. Leone, D. P., Srinivasan, K., Chen, B., Alcamo, E. and McConnell, S. K. (2008). The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 18, 28-35.
48. Levkowitz, G., Zeller, J., Sirotkin, H. I., French, D., Schilbach, S., Hashimoto, H., Hibi, M., Talbot, W. S. and Rosenthal, A. (2003). Zinc finger protein too few controls the development of monoaminergic neurons. Nat. Neurosci. 6, 28-33.
49. Lo, L., Dormand, E., Greenwood, A. and Anderson, D. J. (2002). Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 129, 1553-1567.
50. Louvi, A. and Artavanis-Tsakonas, S. (2006). Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7, 93-102.
51. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F. and Gruss, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55.
52. McConnell, S. K., Ghosh, A. and Shatz, C. J. (1989). Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245, 978-982.
53. Meyer, G., Perez-Garcia, C. G., Abraham, H. and Caput, D. (2002). Expression of p73 and Reelin in the developing human cortex. J. Neurosci. 22, 4973-4986.
54. Meyer, G., Cabrera Socorro, A., Perez Garcia, C. G., Martinez Millan, L., Walker, N. and Caput, D. (2004). Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J. Neurosci. 24, 9878-9887. (Pubitemid 39463568)
55. Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. and Gaiano, N. (2007). Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351-355. (Pubitemid 47443472)
56. Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M. and Macklis, J. D. (2005). Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47, 817-831. (Pubitemid 41266949)
57. Molyneaux, B. J., Arlotta, P., Menezes, J. R. and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. (Pubitemid 46789231)
58. Morin, X., Jaouen, F. and Durbec, P. (2007). Control of planar divisions by the Gprotein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440-1448. (Pubitemid 350014675)
59. Nakagawa, Y. and O'Leary, D. D. (2003). Dynamic patterned expression of orphan nuclear receptor genes RORalpha and RORbeta in developing mouse forebrain. Dev. Neurosci. 25, 234-244. (Pubitemid 37100216)
60. Nishimura, M., Isaka, F., Ishibashi, M., Tomita, K., Tsuda, H., Nakanishi, S. and Kageyama, R. (1998). Structure, chromosomal locus, and promoter of mouse Hes2 gene, a homologue of Drosophila hairy and Enhancer of split. Genomics 49, 69-75. (Pubitemid 28194438)
61. Ochiai, W., Nakatani, S., Takahara, T., Kainuma, M., Masaoka, M., Minobe, S., Namihira, M., Nakashima, K., Sakakibara, A., Ogawa, M. et al. (2009). Periventricular notch activation and asymmetric Ngn2 and Tbr2 expression in pair-generated neocortical daughter cells. Mol. Cell. Neurosci. 40, 225-233.
62. Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F. and Kageyama, R. (1999). Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18, 2196-2207. (Pubitemid 29179176)
63. Rink, E. and Guo, S. (2004). The too few mutant selectively affects subgroups of monoaminergic neurons in the zebrafish forebrain. Neuroscience 127, 147-154. (Pubitemid 38829160)
64. Ross, S. E., Greenberg, M. E. and Stiles, C. D. (2003). Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25. (Pubitemid 36830945)
65. Schwaller, B., Buchwald, P., Blumcke, I., Celio, M. R. and Hunziker, W. (1993). Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14, 639-648.
66. Sessa, A., Mao, C. A., Hadjantonakis, A. K., Klein, W. H. and Broccoli, V. (2008). Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60, 56-69.
67. Sheppard, A. M. and Pearlman, A. L. (1997). Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J. Comp. Neurol. 378, 173-179.
68. Sheppard, A. M., Hamilton, S. K. and Pearlman, A. L. (1991). Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci. 11, 3928-3942.
69. Shimizu, T. and Hibi, M. (2009). Formation and patterning of the forebrain and olfactory system by zinc-finger genes Fezf1 and Fezf2. Dev. Growth Differ. 51, 221-231.
70. Shimizu, T., Kagawa, T., Wada, T., Muroyama, Y., Takada, S. and Ikenaka, K. (2005). Wnt signaling controls the timing of oligodendrocyte development in the spinal cord. Dev. Biol. 282, 397-410.
71. Shimizu, T., Kagawa, T., Inoue, T., Nonaka, A., Takada, S., Aburatani, H. and Taga, T. (2008). Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol. Cell. Biol. 28, 7427-7441.
72. Shimojo, H., Ohtsuka, T. and Kageyama, R. (2008). Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64.
73. Takebayashi, K., Akazawa, C., Nakanishi, S. and Kageyama, R. (1995). Structure and promoter analysis of the gene encoding the mouse helix-loophelix factor HES-5. Identification of the neural precursor cell-specific promoter element. J. Biol. Chem. 270, 1342-1349.
74. Takiguchi-Hayashi, K., Sekiguchi, M., Ashigaki, S., Takamatsu, M., Hasegawa, H., Suzuki-Migishima, R., Yokoyama, M., Nakanishi, S. and Tanabe, Y. (2004). Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24, 2286-2295.
75. Turner, D. L. and Weintraub, H. (1994). Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8, 1434-1447.
76. Wang, X., Tsai, J. W., Imai, J. H., Lian, W. N., Vallee, R. B. and Shi, S. H. (2009). Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955.
77. Weng, M., Golden, K. L. and Lee, C. Y. (2010). dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 18, 126-135.
78. Yoon, K. and Gaiano, N. (2005). Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8, 709-715.
79. Yoon, K. J., Koo, B. K., Im, S. K., Jeong, H. W., Ghim, J., Kwon, M. C., Moon, J. S., Miyata, T. and Kong, Y. Y. (2008). Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519-531.
80. Yoshida, M., Assimacopoulos, S., Jones, K. R. and Grove, E. A. (2006). Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133, 537-545.
81. Zhou, C., Qiu, Y., Pereira, F. A., Crair, M. C., Tsai, S. Y. and Tsai, M. J. (1999). The nuclear orphan receptor COUP-TFI is required for differentiation of subplate neurons and guidance of thalamocortical axons. Neuron 24, 847-859.
82. Zhou, S., Fujimuro, M., Hsieh, J. J., Chen, L., Miyamoto, A., Weinmaster, G. and Hayward, S. D. (2000). SKIP, a CBF1-associated protein, interacts with the ankyrin repeat domain of NotchIC To facilitate NotchIC function. Mol. Cell. Biol. 20, 2400-2410.
83. Zupanc, G. K., Hinsch, K. and Gage, F. H. (2005). Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J. Comp. Neurol. 488, 290-319.