Developmental time rather than local environment regulates the schedule of epithelial polarization in the zebrafish neur

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Girdler et al. Neural Development 2013, 8:5 http://www.neuraldevelopment.com/content/8/1/5

RESEARCH ARTICLE

Open Access

Developmental time rather than local environment regulates the schedule of epithelial polarization in the zebrafish neural rod Gemma C Girdler1,2, Claudio Araya1,3, Xiaoyun Ren1,4 and Jonathan DW Clarke1*

Abstract Background: Morphogenesis requires developmental processes to occur both at the right time and in the right place. During neural tube formation in the zebrafish embryo, the generation of the apical specializations of the lumen must occur in the center of the neural rod after the neural cells have undergone convergence, invagination and interdigitation across the midline. How this coordination is achieved is uncertain. One possibility is that environmental signaling at the midline of the neural rod controls the schedule of apical polarization. Alternatively, polarization could be regulated by a timing mechanism and then independent morphogenetic processes ensure the cells are in the correct spatial location. Results: Ectopic transplantation demonstrates the local environment of the neural midline is not required for neural cell polarization. Neural cells can self-organize into epithelial cysts in ectopic locations in the embryo and also in three-dimensional gel cultures. Heterochronic transplants demonstrate that the schedule of polarization and the specialized cell divisions characteristic of the neural rod are more strongly regulated by time than local environmental signals. The cells’ schedule for polarization is set prior to gastrulation, is stable through several rounds of cell division and appears independent of the morphogenetic movements of gastrulation and neurulation. Conclusions: Time rather than local environment regulates the schedule of epithelial polarization in zebrafish neural rod. Keywords: Intrinsic program, Lumen, Neuroepithelial polarity, Neural tube, Zebrafish

Background Morphogenesis is the process by which an organism takes its shape and it requires coordinated movements and shape changes of many cells and tissues. Furthermore, movement and shaping events must be coordinated with other fundamental processes of embryogenesis, such as proliferation, differentiation, and spatial patterning. Coordination through time ensures these processes occur in the correct sequence. Cells in different stages of development are likely to have different morphogenetic capabilities because processes such as differentiation of cells and tissues may limit the range of morphogenetic potential available to a cell. For example, mesenchymal cells will have a greater range of potential movements and rearrangements than epithelial cells, but epithelialization * Correspondence: [email protected] 1 MRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London SE1 1UL, UK Full list of author information is available at the end of the article

confers other possibilities for shaping tissues, such as folding. Although the mechanisms that regulate the sequence and