Diversity of thalamic progenitor cells and postmitotic neurons

European Journal of Neuroscience

Volumn 35, Issue 10, 2012, Pages 1554-1562

  Nakagawa, Yasushi ^a   Shimogori, Tomomi ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Fgf8; Nucleogenesis; Patterning; Shh; Thalamus; Transcription factor; Wnt; ZLI

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR ASC11; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR OLIG3; BETA CATENIN; FIBROBLAST GROWTH FACTOR 8; NEUROGENIN 1; NEUROGENIN 2; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DBX1; TRANSCRIPTION FACTOR GBX2; TRANSCRIPTION FACTOR GSX1; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR ORTHODENTICLE HOMOLOG; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR TAL1; TRANSCRIPTION FACTOR TAL2; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; BRAIN DEVELOPMENT; CELL LINEAGE; CELL STRUCTURE; GENE EXPRESSION; MOLECULAR BIOLOGY; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; POSTMITOTIC NEURON; PRINCIPAL SENSORY NUCLEUS; PRIORITY JOURNAL; PROTEIN DOMAIN; THALAMIC PROGENITOR CELL; THALAMUS; THALAMUS NUCLEUS; TRANSGENE; WNT SIGNALING PATHWAY;

ANIMALS; BODY PATTERNING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; NEURONS; SIGNAL TRANSDUCTION; STEM CELLS; THALAMUS; TRANSCRIPTION FACTORS;

EID: 84862074798     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08089.x     Document Type: Article

References (91)

1. Altman, J. & Bayer, S.A. (1979) Development of the diencephalon in the rat. VI. Reevaluation of the embryonic development of the thalamus on the basis of thymidine-radiographic datings. J. Comp. Neurol., 188, 501-524.
2. Altman, J. & Bayer, S.A. (1988a) Development of the rat thalamus: I. Mosaic organization of the thalamic neuroepithelium. J. Comp. Neurol., 275, 346-377.
3. Altman, J. & Bayer, S.A. (1988b) Development of the rat thalamus: II. Time and site of origin and settling pattern of neurons derived from the anterior lobule of the thalamic neuroepithelium. J. Comp. Neurol., 275, 378-405.
4. Altman, J. & Bayer, S.A. (1988c) Development of the rat thalamus: III. Time and site of origin and settling pattern of neurons of the reticular nucleus. J. Comp. Neurol., 275, 406-428.
5. Altman, J. & Bayer, S.A. (1989a) Development of the rat thalamus: IV. The intermediate lobule of the thalamic neuroepithelium, and the time and site of origin and settling pattern of neurons of the ventral nuclear complex. J. Comp. Neurol., 284, 534-566.
6. Altman, J. & Bayer, S.A. (1989b) Development of the rat thalamus: V. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the medial geniculate body. J. Comp. Neurol., 284, 567-580.
7. Altman, J. & Bayer, S.A. (1989c) Development of the rat thalamus: VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. J. Comp. Neurol., 284, 581-601.
8. Angelucci, A., Clasca, F., Bricolo, E., Cramer, K.S. & Sur, M. (1997) Experimentally induced retinal projections to the ferret auditory thalamus: development of clustered eye-specific patterns in a novel target. J. Neurosci., 17, 2040-2055.
9. Angevine, J.B.J. (1970) Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J. Comp. Neurol., 139, 129-187.
10. Bhide, P.G. & Frost, D.O. (1992) Axon substitution in the reorganization of developing neural connections. Proc. Natl Acad. Sci. USA, 89, 11847-11851.
11. Bluske, K.K., Kawakami, Y., Koyano-Nakagawa, N. & Nakagawa, Y. (2009) Differential activity of Wnt/beta-catenin signaling in the embryonic mouse thalamus. Dev. Dyn., 238, 3297-3309.
12. Braun, M.M., Etheridge, A., Bernard, A., Robertson, C.P. & Roelink, H. (2003) Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development, 130, 5579-5587.
13. Bucher, K., Sofroniew, M.V., Pannell, R., Impey, H., Smith, A.J., Torres, E.M., Dunnett, S.B., Jin, Y., Baer, R. & Rabbitts, T.H. (2000) The T cell oncogene Tal2 is necessary for normal development of the mouse brain. Dev. Biol., 227, 533-544.
14. Chen, L., Guo, Q. & 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.
15. Crossley, P.H., Martinez, S., Ohkubo, Y. & Rubenstein, J.L. (2001) Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience, 108, 183-206.
16. Figdor, M.C. & Stern, C.D. (1993) Segmental organization of embryonic diencephalon. Nature, 363, 630-634.
17. Fode, C., Ma, Q., Casarosa, S., Ang, S.L., Anderson, D.J. & Guillemot, F. (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev., 14, 67-80.
18. Garcia-Calero, E., Garda, A.L., Marin, F. & Puelles, L. (2006) Expression of Lrrn1 marks the prospective site of the zona limitans thalami in the early embryonic chicken diencephalon. Gene Expr. Patterns, 6, 879-885.
19. Garcia-Lopez, R., Vieira, C., Echevarria, D. & 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.
20. Golden, J.A. & Cepko, C.L. (1996) Clones in the chick diencephalon contain multiple cell types and siblings are widely dispersed. Development, 122, 65-78.
21. Golden, J.A., Zitz, J.C., McFadden, K. & Cepko, C.L. (1997) Cell migration in the developing chick diencephalon. Development, 124, 3525-3533.
22. Hahm, J.O., Cramer, K.S. & Sur, M. (1999) Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: developmental segregation and the role of N-methyl-d-aspartate receptors. J. Comp. Neurol., 411, 327-345.
23. Hashimoto-Torii, K., Motoyama, J., Hui, C.C., Kuroiwa, A., Nakafuku, M. & Shimamura, K. (2003) Differential activities of Sonic hedgehog mediated by Gli transcription factors define distinct neuronal subtypes in the dorsal thalamus. Mech. Dev., 120, 1097-1111.
24. Haubensak, W., Attardo, A., Denk, W. & Huttner, W.B. (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl Acad. Sci. USA, 101, 3196-3201.
25. Hebert, J.M. & Fishell, G. (2008) The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci., 9, 678-685.
26. Ishibashi, M. & McMahon, A.P. (2002) A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development, 129, 4807-4819.
27. Jeong, Y., El-Jaick, K., Roessler, E., Muenke, M. & Epstein, D.J. (2006) A functional screen for sonic hedgehog regulatory elements across a 1Mb interval identifies long-range ventral forebrain enhancers. Development, 133, 761-772.
28. Jeong, Y., Dolson, D.K., Waclaw, R.R., Matise, M.P., Sussel, L., Campbell, K., Kaestner, K.H. & Epstein, D.J. (2011) Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development, 138, 531-541.
29. Jessell, T.M. (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet., 1, 20-29.
30. Jones, E.G. & Rubenstein, J.L. (2004) Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. J. Comp. Neurol., 477, 55-80.
31. Jones, E.G. (2007) The Thalamus. Cambridge University Press, New York.
32. Kataoka, A. & Shimogori, T. (2008) Fgf8 controls regional identity in the developing thalamus. Development, 135, 2873-2881.
33. Keyser, A. (1973) The development of the diencephalon in the Chinese hamster: an investigation into the validity of the criteria of subdivision of the brain. Acta Anat. (Basel), 86, 42-43.
34. Kiecker, C. & Lumsden, A. (2004) Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat. Neurosci., 7, 1242-1249.
35. Kim, E.J., Hori, K., Wyckoff, A., Dickel, L.K., Koundakjian, E.J., Goodrich, L.V. & Johnson, J.E. (2011) Spatiotemporal fate map of neurogenin1 (Neurog1) lineages in the mouse central nervous system. J. Comp. Neurol., 519, 1355-1370.
36. Kitamura, K., Miura, H., Yanazawa, M., Miyashita, T. & Kato, K. (1997) Expression patterns of Brx1 (Rieg gene), Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech. Dev., 67, 83-96.
37. Kobayashi, D., Kobayashi, M., Matsumoto, K., Ogura, T., Nakafuku, M. & Shimamura, K. (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development, 129, 83-93.
38. Larsen, C.W., Zeltser, L.M. & Lumsden, A. (2001) Boundary formation and compartition in the avian diencephalon. J. Neurosci., 21, 4699-4711.
39. Lee, S.M., Danielian, P.S., Fritzsch, B. & 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.
40. Lim, Y. & Golden, J.A. (2007) Patterning the developing diencephalon. Brain Res. Brain Res. Rev., 53, 17-26.
41. Liu, A., Losos, K. & Joyner, A.L. (1999) FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development, 126, 4827-4838.
42. Louvi, A., Yoshida, M. & Grove, E.A. (2007) The derivatives of the Wnt3a lineage in the central nervous system. J. Comp. Neurol., 504, 550-569.
43. Lui, J.H., Hansen, D.V. & Kriegstein, A.R. (2011) Development and evolution of the human neocortex. Cell, 146, 18-36.
44. Macchi, G., Bentivoglio, M., Minciacchi, D. & Molinari, M. (1996) Trends in the anatomical organization and functional significance of the mammalian thalamus. Ital. J. Neurol. Sci., 17, 105-129.
45. Martinez, S., Alvarado-Mallart, R.M., Martinez-de-la-Torre, M. & Puelles, L. (1991) Retinal and tectal connections of embryonic nucleus superficialis magnocellularis and its mature derivatives in the chick. Anat. Embryol. (Berl), 183, 235-243.
46. Martinez-de-la-Torre, M., Garda, A.L., Puelles, E. & Puelles, L. (2002) Gbx2 expression in the late embryonic chick dorsal thalamus. Brain Res. Bull., 57, 435-438.
47. Martinez-Ferre, A. & Martinez, S. (2009) The development of the thalamic motor learning area is regulated by Fgf8 expression. J. Neurosci., 29, 13389-13400.
48. Meyers, E.N., Lewandoski, M. & Martin, G.R. (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet., 18, 136-141.
49. Miyashita-Lin, E.M., Hevner, R., Wassarman, K.M., Martinez, S. & Rubenstein, J.L. (1999) Early neocortical regionalization in the absence of thalamic innervation. Science, 285, 906-909.
50. Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T. & Ogawa, M. (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development, 131, 3133-3145.
51. Nakagawa, Y. & O'Leary, D.D. (2001) Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. J. Neurosci., 21, 2711-2725.
52. Nakagawa, Y. & O'Leary D, D. (2003) Dynamic patterned expression of orphan nuclear receptor genes RORalpha and RORbeta in developing mouse forebrain. Dev. Neurosci., 25, 233-244.
53. Noctor, S.C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A.R. (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci., 7, 136-144.
54. Nordstrom, U., Jessell, T.M. & Edlund, T. (2002) Progressive induction of caudal neural character by graded Wnt signaling. Nat. Neurosci., 5, 525-532.
55. O'Leary, D.D., Schlaggar, B.L. & Tuttle, R. (1994) Specification of neocortical areas and thalamocortical connections. Annu. Rev. Neurosci., 17, 419-439.
56. Pearson, B.J. & Doe, C.Q. (2004) Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol., 20, 619-647.
57. Penn, A.A., Riquelme, P.A., Feller, M.B. & Shatz, C.J. (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science, 279, 2108-2112.
58. Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R.F. (2008) Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci., 30, 24-32.
59. Pratt, T., Vitalis, T., Warren, N., Edgar, J.M., Mason, J.O. & Price, D.J. (2000) A role for Pax6 in the normal development of dorsal thalamus and its cortical connections. Development, 127, 5167-5178.
60. Puelles, L. & 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.
61. Puelles, L. & Rubenstein, J.L. (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci., 26, 469-476.
62. Puelles, E., Acampora, D., Gogoi, R., Tuorto, F., Papalia, A., Guillemot, F., Ang, S.L. & Simeone, A. (2006) Otx2 controls identity and fate of glutamatergic progenitors of the thalamus by repressing GABAergic differentiation. J. Neurosci., 26, 5955-5964.
63. Puelles, L., Martinez-de-La-Torre, M., Bardet, S.M. & Rubenstein, J.L.R. (2011a) Hypothalamus. In Watson, C., Paxinos, G. & Puelles, L. (Eds), The Mouse Nervous System. Academic Press, San Diego, pp. 221-312.
64. Puelles, L., Martinez-de-La-Torre, M., Ferran, J.L. & Watson, C. (2011b) Diencephalon. In Watson, C., Paxinos, G. & Puelles, L. (Eds), The Mouse Nervous System. Academic Press, San Diego, pp. 313-336.
65. Quinlan, R., Graf, M., Mason, I., Lumsden, A. & Kiecker, C. (2009) Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev., 4, 35.
66. Redies, C., Ast, M., Nakagawa, S., Takeichi, M., Martinez-de-la-Torre, M. & Puelles, L. (2000) Morphologic fate of diencephalic prosomeres and their subdivisions revealed by mapping cadherin expression. J. Comp. Neurol., 421, 481-514.
67. Roelink, H. & Nusse, R. (1991) Expression of two members of the Wnt family during mouse development - restricted temporal and spatial patterns in the developing neural tube. Genes Dev., 5, 381-388.
68. Scholpp, S. & Lumsden, A. (2010) Building a bridal chamber: development of the thalamus. Trends Neurosci., 33, 373-380.
69. Scholpp, S., Wolf, O., Brand, M. & Lumsden, A. (2006) Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development, 133, 855-864.
70. Scholpp, S., Delogu, A., Gilthorpe, J., Peukert, D., Schindler, S. & Lumsden, A. (2009) Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc. Natl Acad. Sci. USA, 106, 19895-19900.
71. Shimamura, K., Hartigan, D.J., Martinez, S., Puelles, L. & Rubenstein, J.L. (1995) Longitudinal organization of the anterior neural plate and neural tube. Development, 121, 3923-3933.
72. Shimogori, T. & Ogawa, M. (2008) Gene application with in utero electroporation in mouse embryonic brain. Dev. Growth Differ., 50, 499-506.
73. Smart, I.H. (1972) Proliferative characteristics of the ependymal layer during the early development of the mouse diencephalon, as revealed by recording the number, location, and plane of cleavage of mitotic figures. J. Anat., 113, 109-129.
74. Stellwagen, D. & Shatz, C.J. (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron, 33, 357-367.
75. Suda, Y., Hossain, Z.M., Kobayashi, C., Hatano, O., Yoshida, M., Matsuo, I. & Aizawa, S. (2001) Emx2 directs the development of diencephalon in cooperation with Otx2. Development 128, 2433-2450
76. Sur, M., Garraghty, P.E. & Roe, A.W. (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science, 242, 1437-1441.
77. Suzuki, S.C., Inoue, T., Kimura, Y., Tanaka, T. & Takeichi, M. (1997) Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol. Cell. Neurosci., 9, 433-447.
78. Suzuki-Hirano, A., Ogawa, M., Kataoka, A., Yoshida, A.C., Itoh, D., Ueno, M., Blackshaw, S. & Shimogori, T. (2011) Dynamic spatiotemporal gene expression in embryonic mouse thalamus. J. Comp. Neurol., 519, 528-543.
79. Szabo, N.E., Zhao, T., Zhou, X. & Alvarez-Bolado, G. (2009) The role of Sonic hedgehog of neural origin in thalamic differentiation in the mouse. J. Neurosci., 29, 2453-2466.
80. Uchikawa, M., Kamachi, Y. & Kondoh, H. (1999) Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech. Dev., 84, 103-120.
81. Ulloa, F. & Marti, E. (2010) Wnt won the war: antagonistic role of Wnt over Shh controls dorsoventral patterning of the vertebrate neural tube. Dev. Dyn., 239, 69-76.
82. Vieira, C. & Martinez, S. (2006) Sonic hedgehog from the basal plate and the zona limitans intrathalamica exhibits differential activity on diencephalic molecular regionalization and nuclear structure. Neuroscience, 143, 129-140.
83. Vieira, C., Garda, A.L., Shimamura, K. & Martinez, S. (2005) Thalamic development induced by Shh in the chick embryo. Dev. Biol., 284, 351-363.
84. Vieira, C., Pombero, A., Garcia-Lopez, R., Gimeno, L., Echevarria, D. & Martinez, S. (2010) Molecular mechanisms controlling brain development: an overview of neuroepithelial secondary organizers. Int. J. Dev. Biol., 54, 7-20.
85. Vue, T.Y., Aaker, J., Taniguchi, A., Kazemzadeh, C., Skidmore, J.M., Martin, D.M., Martin, J.F., Treier, M. & Nakagawa, Y. (2007) Characterization of progenitor domains in the developing mouse thalamus. J. Comp. Neurol., 505, 73-91.
86. Vue, T.Y., Bluske, K., Alishahi, A., Yang, L.L., Koyano-Nakagawa, N., Novitch, B. & Nakagawa, Y. (2009) Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J. Neurosci., 29, 4484-4497.
87. Wang, L., Bluske, K.K., Dickel, L.K. & Nakagawa, Y. (2011) Basal progenitor cells in the embryonic mouse thalamus - their molecular characterization and the role of neurogenins and Pax6. Neural Dev., 6, 35.
88. Yoon, M.S., Puelles, L. & Redies, C. (2000) Formation of cadherin-expressing brain nuclei in diencephalic alar plate divisions. J. Comp. Neurol., 421, 461-480.
89. Yuge, K., Kataoka, A., Yoshida, A.C., Itoh, D., Aggarwal, M., Mori, S., Blackshaw, S. & Shimogori, T. (2011) Region-specific gene expression in early postnatal mouse thalamus. J. Comp. Neurol., 519, 544-561.
90. Zeltser, L.M. (2005) Shh-dependent formation of the ZLI is opposed by signals from the dorsal diencephalon. Development, 132, 2023-2033.
91. Zhou, C.J., Pinson, K.I. & Pleasure, S.J. (2004) Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J. Neurosci., 24, 7632-7639.