Directional Cell Migration Establishes the Axes of Planar Polarity in the Posterior Lateral-Line Organ of the Zebrafish

Laboratory of Sensory Neuroscience, The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
Developmental Cell (Impact Factor: 9.71). 10/2004; 7(3):401-12. DOI: 10.1016/j.devcel.2004.07.018
Source: PubMed


The proper orientation of mechanosensory hair cells along the lateral-line organ of a fish or amphibian is essential for the animal's ability to sense directional water movements. Within the sensory epithelium, hair cells are polarized in a stereotyped manner, but the mechanisms that control their alignment relative to the body axes are unknown. We have found, however, that neuromasts can be oriented either parallel or perpendicular to the anteroposterior body axis. By characterizing the strauss mutant zebrafish line and by tracking labeled cells, we have demonstrated that neuromasts of these two orientations originate from, respectively, the first and second primordia. Furthermore, altering the migratory pathway of a primordium reorients a neuromast's axis of planar polarity. We propose that the global orientation of hair cells relative to the body axes is established through an interaction between directional movement by primordial cells and the timing of neuromast maturation.

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Available from: James A Kappler, Nov 10, 2015
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    • "Here we detail a simple, fast and inexpensive protocol to characterize hair-cell development and regeneration by in toto high-resolution live imaging. This protocol has been optimized during over 10 years of experience using the zebrafish and high-resolution imaging (López-Schier and St. Johnston, 2001; López-Schier et al., 2004; López-Schier and Hudspeth, 2006; López-Schier, 2010; Swoger et al., 2011; Wibowo et al., 2011). It relies on the stable expression of engineered transgenes coding for fluorescent proteins in specific cellular populations of the lateral line. "
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    ABSTRACT: Direct videomicroscopic visualization of organ formation and regeneration in toto is a powerful strategy to study cellular processes that often cannot be replicated in vitro. Intravital imaging aims at quantifying changes in tissue architecture or subcellular organization over time during organ development, regeneration or degeneration. A general feature of this approach is its reliance on the optical isolation of defined cell types in the whole animals by transgenic expression of fluorescent markers. Here we describe a simple and robust method to analyze sensory hair-cell development and regeneration in the zebrafish lateral line by high-resolution intravital imaging using laser-scanning confocal microscopy (LSCM) and selective plane illumination microscopy (SPIM). The main advantage of studying hair-cell regeneration in the lateral line is that it occurs throughout the life of the animal, which allows its study in the most natural context. We detail protocols to achieve continuous videomicroscopy for up to 68 hours, enabling direct observation of cellular behavior, which can provide a sensitive assay for the quantitative classification of cellular phenotypes and cell-lineage reconstruction. Modifications to this protocol should facilitate pharmacogenetic assays to identify or validate otoprotective or reparative drugs for future clinical strategies aimed at preserving aural function in humans.
    Frontiers in Neuroanatomy 10/2013; 7:33. DOI:10.3389/fnana.2013.00033 · 3.54 Impact Factor
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    • "Therefore, the polarity of hair bundle endows hair cells with vectorial excitability. Each neuromast contains two intermingled populations of hair cells, equal in number, whose stereocilia are oriented along a single axis but in opposite directions (Figures 1B and C; Rouse and Pickles, 1991; López-Schier et al., 2004). Thus, each neuromast is mechanically bidirectional sensitive. "
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    ABSTRACT: The transmission and central representation of sensory cues through the accurate construction of neural maps is essential for animals to react to environmental stimuli. Structural diversity of sensorineural maps along a continuum between discrete- and continuous-map architectures can influence behavior. The mechanosensory lateral line of fishes and amphibians, for example, detects complex hydrodynamics occurring around the animal body. It triggers innate fast escape reactions but also modulates complex navigation behaviors that require constant knowledge about the environment. The aim of this article is to summarize recent work in the zebrafish that has shed light on the development and structure of the lateralis neural map, which is helping to understand how individual sensory modalities generate appropriate behavioral responses to the sensory context.
    Frontiers in Neural Circuits 03/2013; 7:47. DOI:10.3389/fncir.2013.00047 · 3.60 Impact Factor
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    • "At 2 dpf, hair cells are positioned in a highly stereotyped fashion within each neuromast, along a line perpendicular to the axis of mechanosensitivity (Figure 3D " ). Sister cells are paired across this line, and are fated to have opposing polarities (Figure 3D " ) (López-Schier et al., 2004). In this arrangement, when mature, all cells initially present on the left side of the neuromast will respond to posterior stimuli, and those on the right side will respond to anterior stimuli. "
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    ABSTRACT: Mechanosensitive cilia are vital to signaling and development across many species. In sensory hair cells, sound and movement are transduced by apical hair bundles. Each bundle is comprised of a single primary cilium (kinocilium) flanked by multiple rows of actin-filled projections (stereocilia). Extracellular tip links that interconnect stereocilia are thought to gate mechanosensitive channels. In contrast to stereocilia, kinocilia are not critical for hair-cell mechanotransduction. However, by sequentially imaging the structure of hair bundles and mechanosensitivity of individual lateral-line hair cells in vivo, we uncovered a central role for kinocilia in mechanosensation during development. Our data demonstrate that nascent hair cells require kinocilia and kinocilial links for mechanosensitivity. Although nascent hair bundles have correct planar polarity, the polarity of their responses to mechanical stimuli is initially reversed. Later in development, a switch to correctly polarized mechanosensitivity coincides with the formation of tip links and the onset of tip-link-dependent mechanotransduction.
    Developmental Cell 08/2012; 23(2):329-41. DOI:10.1016/j.devcel.2012.05.022 · 9.71 Impact Factor
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