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Principles of Early Vertebrate Forebrain Formation

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Organogenetic Gene Networks

Abstract

The formation of the vertebrate central nervous system begins at the onset of gastrulation with the specification of the neuroectoderm or neural plate. This flat sheet of neuroepithelial cells is further patterned along its main axes as it undergoes a complex morphogenetic reorganisation to give rise to the priomordia of the brain and the spinal cord. In this chapter, we provide a basic overview of the regulatory networks that couple patterning and morphogenesis of the forebrain primordium, which arises from the most anterior part of the neural plate and comprises the telencephalic, retinal, hypothalamic and diencephalic fields. We will describe that, as it occurs in other regions of the developing embryo, morphogenesis and specification of the forebrain primordium is coordinated by a constantly evolving combination of a reduced number of signalling pathways and transcription factors , which together form highly interconnected gene regulatory networks. We will also discuss the still fragmentary information showing that the expression levels of the components of these networks is fine-tuned by different species of non-translated RNAs, which further contribute to originate forebrain complexity from a limited number of key genes.

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References

  • Acampora, D., Mazan, S., Lallemand, Y., Avantaggiato, V., Maury, M., Simeone, A., et al. (1995). Forebrain and midbrain regions are deleted in Otx2−/− mutants due to a defective anterior neuroectoderm specification during gastrulation. Development, 121, 3279–3290.

    CAS  PubMed  Google Scholar 

  • Adijanto, J., Castorino, J. J., Wang, Z. X., Maminishkis, A., Grunwald, G. B., & Philp, N. J. (2012). Microphthalmia-associated transcription factor (MITF) promotes differentiation of human retinal pigment epithelium (RPE) by regulating microRNAs-204/211 expression. The Journal of Biological Chemistry, 287, 20491–20503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andoniadou, C. L., & Martinez-Barbera, J. P. (2013). Developmental mechanisms directing early anterior forebrain specification in vertebrates. Cellular and Molecular Life Sciences: CMLS, 70, 3739–3752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araya, C., Tawk, M., Girdler, G. C., Costa, M., Carmona-Fontaine, C., & Clarke, J. D. (2014). Mesoderm is required for coordinated cell movements within zebrafish neural plate in vivo. Neural Development, 9, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beccari, L., Conte, I., Cisneros, E., & Bovolenta, P. (2012). Sox2-mediated differential activation of Six3.2 contributes to forebrain patterning. Development, 139, 151–164.

    Article  CAS  PubMed  Google Scholar 

  • Beccari, L., Marco-Ferreres, R., & Bovolenta, P. (2013). The logic of gene regulatory networks in early vertebrate forebrain patterning. Mechanisms of Development, 130, 95–111.

    Article  CAS  PubMed  Google Scholar 

  • Beccari, L., Marco-Ferreres, R., Tabanera, N., Manfredi, A., Souren, M., Wittbrodt, B., et al. (2015). A trans-regulatory code for the forebrain expression of Six3.2 in the medaka fish. The Journal of Biological Chemistry.

    Google Scholar 

  • Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., et al. (2003). Dicer is essential for mouse development. Nature Genetics, 35, 215–217.

    Article  CAS  PubMed  Google Scholar 

  • Bhinge, A., Poschmann, J., Namboori, S. C., Tian, X., Jia Hui Loh, S., Traczyk, A., et al. (2014). MiR-135b is a direct PAX6 target and specifies human neuroectoderm by inhibiting TGF-beta/BMP signaling. The EMBO Journal, 33, 1271–1283.

    Google Scholar 

  • Bielen, H., & Houart, C. (2012). BMP signaling protects telencephalic fate by repressing eye identity and its Cxcr4-dependent morphogenesis. Developmental Cell, 23, 812–822.

    Article  CAS  PubMed  Google Scholar 

  • Blaess, S., Szabo, N., Haddad-Tovolli, R., Zhou, X., & Alvarez-Bolado, G. (2014). Sonic hedgehog signaling in the development of the mouse hypothalamus. Frontiers in Neuroanatomy, 8, 156.

    PubMed  Google Scholar 

  • Bovolenta, P., Esteve, P., Ruiz, J. M., Cisneros, E., & Lopez-Rios, J. (2008). Beyond Wnt inhibition: New functions of secreted Frizzled-related proteins in development and disease. Journal of Cell Science, 121, 737–746.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Brown, K. E., Keller, P. J., Ramialison, M., Rembold, M., Stelzer, E. H., Loosli, F., & Wittbrodt, J. (2010). Nlcam modulates midline convergence during anterior neural plate morphogenesis. Developmental Biology, 339, 14–25.

    Article  CAS  PubMed  Google Scholar 

  • Buckley, C., & Clarke, J. (2014). Establishing the plane of symmetry for lumen formation and bilateral brain formation in the zebrafish neural rod. Seminars in Cell & Developmental Biology, 31, 100–105.

    Article  Google Scholar 

  • Cavodeassi, F. (2014). Integration of anterior neural plate patterning and morphogenesis by the Wnt signaling pathway. Developmental Neurobiology, 74, 759–771.

    Article  PubMed  Google Scholar 

  • Cavodeassi, F., Carreira-Barbosa, F., Young, R. M., Concha, M. L., Allende, M. L., Houart, C., et al. (2005). Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron, 47, 43–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavodeassi, F., & Houart, C. (2012). Brain regionalization: Of signaling centers and boundaries. Developmental Neurobiology, 72, 218–233.

    Article  PubMed  Google Scholar 

  • Cavodeassi, F., Ivanovitch, K., & Wilson, S. W. (2013). Eph/Ephrin signalling maintains eye field segregation from adjacent neural plate territories during forebrain morphogenesis. Development, 140, 4193–4202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciruna, B., Jenny, A., Lee, D., Mlodzik, M., & Schier, A. F. (2006). Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature, 439, 220–224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke, J. (2009). Role of polarized cell divisions in zebrafish neural tube formation. Current Opinion in Neurobiology, 19, 134–138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conte, I., Banfi, S., & Bovolenta, P. (2013). Non-coding RNAs in the development of sensory organs and related diseases. Cellular and Molecular Life Sciences: CMLS, 70, 4141–4155.

    Article  CAS  PubMed  Google Scholar 

  • Conte, I., Carrella, S., Avellino, R., Karali, M., Marco-Ferreres, R., Bovolenta, P., et al. (2010). miR-204 is required for lens and retinal development via Meis2 targeting. Proceedings of the National Academy of Sciences USA, 107, 15491–15496.

    Article  CAS  Google Scholar 

  • Conte, I., Merella, S., Garcia-Manteiga, J. M., Migliore, C., Lazarevic, D., Carrella, S., et al. (2014). The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucleic Acids Research, 42, 7793–7806.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz, N. F., Cruz-Resendiz, M. S., Flores-Herrera, H., Garcia-Lopez, G., & Molina-Hernandez, A. (2014). MicroRNAs in central nervous system development. Reviews in the Neurosciences, 25, 675–686.

    CAS  PubMed  Google Scholar 

  • Du, Z. W., Ma, L. X., Phillips, C., & Zhang, S. C. (2013). miR-200 and miR-96 families repress neural induction from human embryonic stem cells. Development, 140, 2611–2618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., et al. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature, 472, 51–56.

    Article  CAS  PubMed  Google Scholar 

  • Erwin, D. H., & Davidson, E. H. (2009). The evolution of hierarchical gene regulatory networks. Nature Reviews Genetics, 10, 141–148.

    Article  CAS  PubMed  Google Scholar 

  • Esteve, P., & Bovolenta, P. (2006). Secreted inducers in vertebrate eye development: More functions for old morphogens. Current Opinion in Neurobiology, 16, 13–19.

    Article  CAS  PubMed  Google Scholar 

  • Esteve, P., Lopez-Rios, J., & Bovolenta, P. (2004). SFRP1 is required for the proper establishment of the eye field in the medaka fish. Mechanisms of Development, 121, 687–701.

    Article  CAS  PubMed  Google Scholar 

  • Esteve, P., Sandonis, A., Cardozo, M., Malapeira, J., Ibanez, C., Crespo, I., et al. (2011a). SFRPs act as negative modulators of ADAM10 to regulate retinal neurogenesis. Nature Neuroscience, 14, 562–569.

    Article  CAS  PubMed  Google Scholar 

  • Esteve, P., Sandonis, A., Ibanez, C., Shimono, A., Guerrero, I., & Bovolenta, P. (2011b). Secreted frizzled-related proteins are required for Wnt/beta-catenin signalling activation in the vertebrate optic cup. Development, 138, 4179–4184.

    Article  CAS  PubMed  Google Scholar 

  • Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., et al. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science, 308, 833–838.

    Article  CAS  PubMed  Google Scholar 

  • Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C., & Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature, 391, 357–362.

    Article  CAS  PubMed  Google Scholar 

  • Hammond, S. M., Bernstein, E., Beach, D., & Hannon, G. J. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature, 404, 293–296.

    Article  CAS  PubMed  Google Scholar 

  • Hirata, T., Nakazawa, M., Muraoka, O., Nakayama, R., Suda, Y., & Hibi, M. (2006). Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development, 133, 3993–4004.

    Article  CAS  PubMed  Google Scholar 

  • Houart, C., Caneparo, L., Heisenberg, C., Barth, K., Take-Uchi, M., & Wilson, S. (2002). Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling. Neuron, 35, 255–265.

    Article  CAS  PubMed  Google Scholar 

  • Hutvagner, G., McLachlan, J., Pasquinelli, A. E., Balint, E., Tuschl, T., & Zamore, P. D. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science, 293, 834–838.

    Article  CAS  PubMed  Google Scholar 

  • Ivanovitch, K., Cavodeassi, F., & Wilson, S. W. (2013). Precocious acquisition of neuroepithelial character in the eye field underlies the onset of eye morphogenesis. Developmental Cell, 27, 293–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong, J. Y., Einhorn, Z., Mathur, P., Chen, L., Lee, S., Kawakami, K., et al. (2007). Patterning the zebrafish diencephalon by the conserved zinc-finger protein Fezl. Development, 134, 127–136.

    Article  CAS  PubMed  Google Scholar 

  • Kapsimali, M., Kloosterman, W. P., de Bruijn, E., Rosa, F., Plasterk, R. H., & Wilson, S. W. (2007). MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biology, 8, R173.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaspi, H., Chapnik, E., Levy, M., Beck, G., Hornstein, E., & Soen, Y. (2013). Brief report: miR-290-295 regulate embryonic stem cell differentiation propensities by repressing Pax6. Stem Cells, 31, 2266–2272.

    Article  CAS  PubMed  Google Scholar 

  • Kawase-Koga, Y., Otaegi, G., & Sun, T. (2009). Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 238, 2800–2812.

    Article  Google Scholar 

  • Kiecker, C., & Lumsden, A. (2012). The role of organizers in patterning the nervous system. Annual Review of Neuroscience, 35, 347–367.

    Article  CAS  PubMed  Google Scholar 

  • Kim, N. H., Kim, H. S., Kim, N. G., Lee, I., Choi, H. S., Li, X. Y., et al. (2011). p53 and microRNA-34 are suppressors of canonical Wnt signaling. Science Signaling, 4, ra71.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Kobayashi, K., Luo, M., Zhang, Y., Wilkes, D. C., Ge, G., Grieskamp, T., et al. (2009). Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction. Nature Cell Biology, 11, 46–55.

    Article  CAS  PubMed  Google Scholar 

  • Kudoh, T., Concha, M. L., Houart, C., Dawid, I. B., & Wilson, S. W. (2004). Combinatorial Fgf and Bmp signalling patterns the gastrula ectoderm into prospective neural and epidermal domains. Development, 131, 3581–3592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutejova, E., Briscoe, J., & Kicheva, A. (2009). Temporal dynamics of patterning by morphogen gradients. Current Opinion in Genetics & Development, 19, 315–322.

    Article  CAS  Google Scholar 

  • Lagutin, O. V., Zhu, C. C., Kobayashi, D., Topczewski, J., Shimamura, K., Puelles, L., et al. (2003). Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes & Development, 17, 368–379.

    Article  CAS  Google Scholar 

  • Lee, H. X., Ambrosio, A. L., Reversade, B., & De Robertis, E. M. (2006). Embryonic dorsal-ventral signaling: Secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell, 124, 147–159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature, 425, 415–419.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y., Jeon, K., Lee, J. T., Kim, S., & Kim, V. N. (2002). MicroRNA maturation: Stepwise processing and subcellular localization. The EMBO Journal, 21, 4663–4670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., & Bally-Cuif, L. (2008). MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nature Neuroscience, 11, 641–648.

    Article  CAS  PubMed  Google Scholar 

  • Li, J. Y., Lao, Z., & Joyner, A. L. (2005). New regulatory interactions and cellular responses in the isthmic organizer region revealed by altering Gbx2 expression. Development, 132, 1971–1981.

    Article  CAS  PubMed  Google Scholar 

  • Linker, C., & Stern, C. D. (2004). Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development, 131, 5671–5681.

    Article  CAS  PubMed  Google Scholar 

  • Liu, K., Liu, Y., Mo, W., Qiu, R., Wang, X., Wu, J. Y., et al. (2011). MiR-124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. Nucleic Acids Research, 39, 2869–2879.

    Article  CAS  PubMed  Google Scholar 

  • Liu, W., Lagutin, O., Swindell, E., Jamrich, M., & Oliver, G. (2010). Neuroretina specification in mouse embryos requires Six3-mediated suppression of Wnt8b in the anterior neural plate. The Journal of Clinical Investigation, 120, 3568–3577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longabaugh, W. J., Davidson, E. H., & Bolouri, H. (2005). Computational representation of developmental genetic regulatory networks. Developmental Biology, 283, 1–16.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Rios, J., Esteve, P., Ruiz, J. M., & Bovolenta, P. (2008). The Netrin-related domain of Sfrp1 interacts with Wnt ligands and antagonizes their activity in the anterior neural plate. Neural Development, 3, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lowery, L. A., & Sive, H. (2004). Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mechanisms of Development, 121, 1189–1197.

    Article  CAS  PubMed  Google Scholar 

  • Makeyev, E. V., Zhang, J., Carrasco, M. A., & Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell, 27, 435–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marti, E., & Bovolenta, P. (2002). Sonic hedgehog in CNS development: One signal, multiple outputs. Trends in Neurosciences, 25, 89–96.

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Barbera, J. P., Signore, M., Boyl, P. P., Puelles, E., Acampora, D., Gogoi, R., et al. (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.

    CAS  PubMed  Google Scholar 

  • Martinez-Morales, J. R. (2015). Toward understanding the evolution of vertebrate gene regulatory networks: Comparative genomics and epigenomic approaches. Briefings in Functional Genomics.

    Google Scholar 

  • Matsumoto, K., Nishihara, S., Kamimura, M., Shiraishi, T., Otoguro, T., Uehara, M., et al. (2004). The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nature Neuroscience, 7, 605–612.

    Article  CAS  PubMed  Google Scholar 

  • Matsuo, I., Kuratani, S., Kimura, C., Takeda, N., & Aizawa, S. (1995). Mouse Otx2 functions in the formation and patterning of rostral head. Genes & Development, 9, 2646–2658.

    Article  CAS  Google Scholar 

  • Maurus, D., Heligon, C., Burger-Schwarzler, A., Brandli, A. W., & Kuhl, M. (2005). Noncanonical Wnt-4 signaling and EAF2 are required for eye development in Xenopus laevis. The EMBO Journal, 24, 1181–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., et al. (2012). Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell, 10, 771–785.

    Article  CAS  PubMed  Google Scholar 

  • Nishimura, T., Honda, H., & Takeichi, M. (2012). Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell, 149, 1084–1097.

    Article  CAS  PubMed  Google Scholar 

  • Nord, A. S., Pattabiraman, K., Visel, A., & Rubenstein, J. L. (2015). Genomic perspectives of transcriptional regulation in forebrain development. Neuron, 85, 27–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohana, R., Weiman-Kelman, B., Raviv, S., Tamm, E. R., Pasmanik-Chor, M., Rinon, A., et al. (2015). MicroRNAs are essential for differentiation of the retinal pigmented epithelium and maturation of adjacent photoreceptors. Development, 142, 2487–2498.

    Article  CAS  PubMed  Google Scholar 

  • Okuda, Y., Ogura, E., Kondoh, H., & Kamachi, Y. (2010). B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLoS Genetics, 6, e1000936.

    Article  PubMed  PubMed Central  Google Scholar 

  • Okuda, Y., Yoda, H., Uchikawa, M., Furutani-Seiki, M., Takeda, H., Kondoh, H., et al. (2006). Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 235, 811–825.

    Article  CAS  Google Scholar 

  • Ozair, M. Z., Kintner, C., & Brivanlou, A. H. (2013). Neural induction and early patterning in vertebrates. Wiley Interdisciplinary Reviews. Developmental Biology, 2, 479–498.

    Article  CAS  PubMed  Google Scholar 

  • Pera, E. M., Ikeda, A., Eivers, E., & De Robertis, E. M. (2003). Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes & Development, 17, 3023–3028.

    Article  CAS  Google Scholar 

  • Rao, S., Chun, C., Fan, J., Kofron, J. M., Yang, M. B., Hegde, R. S., et al. (2013). A direct and melanopsin-dependent fetal light response regulates mouse eye development. Nature, 494, 243–246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rembold, M., Loosli, F., Adams, R. J., & Wittbrodt, J. (2006). Individual cell migration serves as the driving force for optic vesicle evagination. Science, 313, 1130–1134.

    Article  CAS  PubMed  Google Scholar 

  • Rhinn, M., Lun, K., Ahrendt, R., Geffarth, M., & Brand, M. (2009). Zebrafish gbx1 refines the midbrain-hindbrain boundary border and mediates the Wnt8 posteriorization signal. Neural Development, 4, 12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Seguel, E., Alarcon, P., & Gomez-Skarmeta, J. L. (2009). The Xenopus Irx genes are essential for neural patterning and define the border between prethalamus and thalamus through mutual antagonism with the anterior repressors Fezf and Arx. Developmental Biology, 329, 258–268.

    Article  CAS  PubMed  Google Scholar 

  • Rubenstein, J. L., Shimamura, K., Martinez, S., & Puelles, L. (1998). Regionalization of the prosencephalic neural plate. Annual Review of Neuroscience, 21, 445–477.

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Arrones, L., Ferran, J. L., Rodriguez-Gallardo, L., & Puelles, L. (2009). Incipient forebrain boundaries traced by differential gene expression and fate mapping in the chick neural plate. Developmental Biology, 335, 43–65.

    Article  CAS  PubMed  Google Scholar 

  • Sanuki, R., Onishi, A., Koike, C., Muramatsu, R., Watanabe, S., Muranishi, Y., et al. (2011). miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nature Neuroscience, 14, 1125–1134.

    Article  CAS  PubMed  Google Scholar 

  • Sasai, Y., Eiraku, M., & Suga, H. (2012). In vitro organogenesis in three dimensions: Self-organising stem cells. Development, 139, 4111–4121.

    Article  CAS  PubMed  Google Scholar 

  • Scholpp, S., Foucher, I., Staudt, N., Peukert, D., Lumsden, A., & Houart, C. (2007). Otx1l, Otx2 and Irx1b establish and position the ZLI in the diencephalon. Development, 134, 3167–3176.

    Article  CAS  PubMed  Google Scholar 

  • Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., & Zamore, P. D. (2003). Asymmetry in the assembly of the RNAi enzyme complex. Cell, 115, 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki, K., Yoshida, M., Nakamura, M., Aizawa, S., & Suda, Y. (2004). Emx1 and Emx2 cooperate in initial phase of archipallium development. Mechanisms of Development, 121, 475–489.

    Article  CAS  PubMed  Google Scholar 

  • Sokol, S. Y. (2015). Spatial and temporal aspects of Wnt signaling and planar cell polarity during vertebrate embryonic development. Seminars in Cell & Developmental Biology, 42, 78–85.

    Article  CAS  Google Scholar 

  • Stern, C. D. (2005). Neural induction: Old problem, new findings, yet more questions. Development, 132, 2007–2021.

    Article  CAS  PubMed  Google Scholar 

  • Tang, F., Kaneda, M., O’Carroll, D., Hajkova, P., Barton, S. C., Sun, Y. A., et al. (2007). Maternal microRNAs are essential for mouse zygotic development. Genes & Development, 21, 644–648.

    Article  CAS  Google Scholar 

  • Tawk, M., Araya, C., Lyons, D. A., Reugels, A. M., Girdler, G. C., Bayley, P. R., et al. (2007). A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature, 446, 797–800.

    Article  CAS  PubMed  Google Scholar 

  • Valencia-Sanchez, M. A., Liu, J., Hannon, G. J., & Parker, R. (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes & Development, 20, 515–524.

    Article  CAS  Google Scholar 

  • Viczian, A. S., Solessio, E. C., Lyou, Y., & Zuber, M. E. (2009). Generation of functional eyes from pluripotent cells. PLoS Biology, 7, e1000174.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. The International Journal of Developmental Biology, 54, 7–20.

    Article  CAS  PubMed  Google Scholar 

  • Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E., & Plasterk, R. H. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nature Genetics, 35, 217–218.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, S. W., & Houart, C. (2004). Early steps in the development of the forebrain. Developmental Cell, 6, 167–181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi, T. P. (2001). Heads or tails: Wnts and anterior-posterior patterning. Current Biology: CB, 11, R713–R724.

    Article  CAS  PubMed  Google Scholar 

  • Zuber, M. E., Gestri, G., Viczian, A. S., Barsacchi, G., & Harris, W. A. (2003). Specification of the vertebrate eye by a network of eye field transcription factors. Development, 130, 5155–5167.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Work in our lab is supported by grants from the Spanish Government MINECO (BFU2014-55918-P to F.C.; BFU-2013-43213-P and BFU2014-55738-REDT to P.B.), the European Commission (CIG321788 to F.C. and P.B.); the Comunidad Autonoma de Madrid (CAM; S2010/BMD-2315 to P.B.); the CIBERER, ISCIII to P.B. and by an Institutional Grant from the Fundación Ramon Areces.

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Correspondence to Paola Bovolenta .

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Cavodeassi, F., Moreno-Mármol, T., Hernandez-Bejarano, M., Bovolenta, P. (2016). Principles of Early Vertebrate Forebrain Formation. In: Castelli-Gair Hombría, J., Bovolenta, P. (eds) Organogenetic Gene Networks. Springer, Cham. https://doi.org/10.1007/978-3-319-42767-6_11

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