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

López‐Schier, Hernán; Starr, Catherine J.; Kappler, James A.; Kollmar, Richard; Hudspeth, A. J.

doi:10.1016/j.devcel.2004.07.018

Cited by 156 publications

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“…During development, neuromasts acquire two equally populated groups of hair cells whose hair bundles are oriented along a single axis but in opposite directions (14). For example, the first neuromast of the posterior lateral line, conventionally named L1, has an axis of planar cell polarity that is oriented parallel to the animal's anteroposterior body axis: each hair bundle directs its kinocilium toward either the head or the tail (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…These mitotic cells were observed regularly at the dorsal and ventral poles of developing or regenerating neuromasts such as L1, whose axis of planar cell polarity is oriented anteroposteriorally. In a neuromast whose axis of polarization is instead directed dorsoventrally (14), the positions of the progenitors were also rotated by 90°, that is, at the anterior and posterior extremes of the organ. The progenitors were encountered rarely in quiescent, nonproliferating neuromasts (data not shown), which may explain why they heretofore have escaped identification.…”

Section: Pairs Of Hair Cellsmentioning

confidence: 99%

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A two-step mechanism underlies the planar polarization of regenerating sensory hair cells

López‐Schier

Hudspeth²

2006

Proc. Natl. Acad. Sci. U.S.A.

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162

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The restoration of planar cell polarity is an essential but poorly understood step toward physiological recovery during sensoryorgan regeneration. Investigating this issue in the lateral line of the zebrafish, we found that hair cells regenerate in pairs along a single axis established by the restricted localization and oriented division of their progenitors. By analyzing mutants lacking the planar-polarity determinant Vangl2, we ascertained that the uniaxial production of hair cells and the subsequent orientation of their hair bundles are controlled by distinct pathways, whose combination underlies the establishment of hair-cell orientation during development and regeneration. This mechanism may represent a general principle governing the long-term maintenance of planar cell polarity in remodeling epithelia.auditory system ͉ balance ͉ hearing ͉ lateral line ͉ vestibular system E pithelial cells are polarized along the apicobasal axis and often also perpendicularly to this axis, within the plane of the epithelium. The latter type of cellular organization, termed planar cell polarity, has been studied extensively during development in Drosophila (1, 2). Because the epithelia of adult fruit flies harden and, consequently, cannot undergo repair after mechanical damage or cell death, they are not amenable to studies of the postembryonic recovery of planar cell polarity. In vertebrates, the orientation of the hair bundle that projects from the apical surface of a sensory hair cell represents a striking example of planar cell polarity (3, 4). Because the hair bundle's axis of morphological polarization defines the cell's axis of responsiveness to mechanical stimuli, the senses of hearing and equilibrium rely on the coordinated orientation of hair cells across the sensory epithelium (5, 6).The loss of cochlear hair cells in mammals is irreversible. However, other vertebrates can regenerate hair cells (7-9). In birds, for example, regenerated hair cells appear normal and regain their proper orientation (10-12). The mechanisms that underlie the establishment of hair-cell orientation during development remain poorly understood, however, and those active during hair-cell regeneration are unknown. Direct and continuous observation of hair-cell development and regeneration has not yet been achieved, for live imaging of the ear's mechanosensory epithelium is hampered by the inaccessibility of the cochlea within the skull. Furthermore, the long periods needed by some animals to regenerate hair cells pose severe limitations to analyzing the process continuously. Attempts to monitor cellular behavior in neuromasts after hair-cell ablation in salamanders suffered from the absence of cellular and molecular markers (13), which prevented the unambiguous identification of cellular types and the analysis of the recovery of epithelial architecture upon regeneration. In this study, we used the lateral-line system of the zebrafish to circumvent these limitations and to acquire time-lapse sequences of hair-cell formation and regeneration....

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Section: Resultsmentioning

confidence: 99%

Section: Pairs Of Hair Cellsmentioning

confidence: 99%

A two-step mechanism underlies the planar polarization of regenerating sensory hair cells

López‐Schier

Hudspeth²

2006

Proc. Natl. Acad. Sci. U.S.A.

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162

216

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“…The hair-cell set also contains seven confirmed or candidate genes that, when mutated, cause syndromic or nonsyndromic deafness in humans or other vertebrates; these include cacna1d (13) and the genes encoding proteins similar to Otof (14), Pmca2 (15), SALL4 (16), Ush1c (17), USH1G (18), and MYO15A (19). By contrast, the supporting-cell markers claudin b (20), hes5 (21), and p27 kip1 (22) are not included in the hair-cell transcriptome. Furthermore, the probe for the ganglionic neuronal marker Hu antigen C (23) and that for the efferent-axonal marker acetylcholinesterase (24) are negative in the hair-cell data set.…”

Section: Resultsmentioning

confidence: 99%

“…Larvae were immunolabeled by conventional techniques (20). Monoclonal anti-acetylated tubulin (6 -11B-1; Sigma) was used at a dilution of 1/1,000, and Alexa Fluor 488-labeled goat anti-mouse IgG (Invitrogen) was used at 1/200.…”

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confidence: 99%

Analysis and functional evaluation of the hair-cell transcriptome

McDermott

Baucom

Hudspeth

2007

Proc. Natl. Acad. Sci. U.S.A.

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An understanding of the molecular bases of the morphogenesis, organization, and functioning of hair cells requires that the genes expressed in these cells be identified and their functions ascertained. After purifying zebrafish hair cells and detecting mRNAs with oligonucleotide microarrays, we developed a subtractive strategy that identified 1,037 hair cell-expressed genes whose cognate proteins subserve functions including membrane transport, synaptic transmission, transcriptional control, cellular adhesion and signal transduction, and cytoskeletal organization. To assess the validity of the subtracted hair-cell data set, we verified the presence of 11 transcripts in inner-ear tissue. Functional evaluation of two genes from the subtracted data set revealed their importance in hair bundles: zebrafish larvae bearing the seahorse and ift 172 mutations display specific kinociliary defects. Moreover, a search for candidate genes that underlie heritable deafness identified a human ortholog of a zebrafish hair-cell gene whose map location is bracketed by the markers of a deafness locus.auditory system ͉ balance ͉ hearing ͉ vestibular system ͉ zebrafish

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“…Finally, the zebrafish genome has been sequenced, and many human genes are conserved in zebrafish. Particularly, the zebrafish has been used as a unique vertebrate model for studying hearing and balance disorders (Nicolson et al 1998;Ernest et al 2000;Whitfield 2002;Söllner et al 2004;Kappler et al 2004;Nicolson 2005;Shen et al 2008;Gleason et al 2009;Phillips et al 2011;Yariz et al 2012), with its externally exposed hair cells of the lateral line being used for study in hair cell death and regeneration, ototoxicity, and drug screens (Chiu et al 2008;López-Schier et al 2004;Owens et al 2009;Coffin et al 2010;Buck et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Early Development of Hearing in Zebrafish

DeSmidt

2013

JARO

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The zebrafish (Danio rerio) has become a valuable vertebrate model for human hearing and balance disorders because it combines powerful genetics, excellent embryology, and exceptional in vivo visualization in one organism. In this study, we investigated auditory function of zebrafish at early developmental stages using the microphonic potential method. This is the first study to report ontogeny of response of hair cells in any fish during the first week post fertilization. The right ear of each zebrafish embedded in agarose was linearly stimulated with a glass probe that was driven by a calibrated piezoelectric actuator. Using beveled micropipettes filled with standard fish saline, extracellular microphonic potentials were recorded from hair cells in the inner ear of zebrafish embryos or larvae in response to 20, 50, 100, and 200-Hz stimulation. Saccular hair cells expressing green fluorescent protein of the transgenic zebrafish from 2 to 7 days post fertilization (dpf) were visualized and quantified using confocal microscopy. The otic vesicles' areas, otoliths' areas, and saccular hair cell count and density increased linearly with age and standard body length. Microphonic responses increased monotonically with stimulus intensity, stimulus frequency, and age of zebrafish. Microphonic threshold at 200 Hz gradually decreased with zebrafish age. The increases in microphonic response and sensitivity correlate with the increases in number and density of hair cells in the saccule. These results enhance our knowledge of early development of auditory function in zebrafish and provide the control data that can be used to evaluate hearing of young zebrafish morphants or mutants.

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

Cited by 156 publications

References 44 publications

A two-step mechanism underlies the planar polarization of regenerating sensory hair cells

A two-step mechanism underlies the planar polarization of regenerating sensory hair cells

Analysis and functional evaluation of the hair-cell transcriptome

Early Development of Hearing in Zebrafish

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