Origin of Inner Ear Hair Cells: Morphological and Functional Differentiation from Ciliary Cells into Hair Cells in Zebrafish Inner Ear

Tanimoto, Masashi; Ota, Yukiko; Inoue, Maya; Oda, Yoichi

doi:10.1523/jneurosci.5554-10.2011

Cited by 56 publications

(52 citation statements)

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“…8A). Tether cilia are present on tether cells, and readily bind otolith precursor particles (Riley et al, 1997;Tanimoto et al, 2011) (Fig. 8B,C).…”

Section: Discussionmentioning

confidence: 99%

“…The otolith becomes biomineralised and must also become embedded in the otolithic membrane, a gelatinous matrix that mechanically couples the otolith to the sensory epithelium beneath (reviewed by Gauldie and Nelson, 1990;Hughes et al, 2006). Little is known about the otolithic membrane in zebrafish; it is not present prior to 27 hpf (Tanimoto et al, 2011), but has been visualised as a fibrous network by scanning electron microscopy at 4 days post fertilisation (Hughes et al, 2004). It is likely to contain the collagen-like protein Otolin 1 (Murayama et al, 2005), a known component of the otolithic membrane in fish, and the otoconial membrane in mammals (Deans et al, 2010).…”

Section: An Otolith Precursor-binding Factor?mentioning

confidence: 99%

“…Otolith precursor particles become tethered to the tips of the kinocilia on the first sensory hair cells that form in the ear; these cells are thus also known as tether cells, and their kinocilia as tether cilia (Fig. 1A) (Haddon and Lewis, 1996;Riley et al, 1997;Tanimoto et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle

et al. 2012

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SUMMARYOtoliths are biomineralised structures required for the sensation of gravity, linear acceleration and sound in the zebrafish ear. Otolith precursor particles, initially distributed throughout the otic vesicle lumen, become tethered to the tips of hair cell kinocilia (tether cilia) at the otic vesicle poles, forming two otoliths. We have used high-speed video microscopy to investigate the role of cilia and ciliary motility in otolith formation. In wild-type ears, groups of motile cilia are present at the otic vesicle poles, surrounding the immotile tether cilia. A few motile cilia are also found on the medial wall, but most cilia (92-98%) in the otic vesicle are immotile. In mutants with defective cilia (iguana) or ciliary motility (lrrc50), otoliths are frequently ectopic, untethered or fused. Nevertheless, neither cilia nor ciliary motility are absolutely required for otolith tethering: a mutant that lacks cilia completely (MZovl) is still capable of tethering otoliths at the otic vesicle poles. In embryos with attenuated Notch signalling [mindbomb mutant or Su(H) morphant], supernumerary hair cells develop and otolith precursor particles bind to the tips of all kinocilia, or bind directly to the hair cells' apical surface if cilia are absent [MZovl injected with a Su(H)1+2 morpholino]. However, if the first hair cells are missing (atoh1b morphant), otolith formation is severely disrupted and delayed. Our data support a model in which hair cells produce an otolith precursor-binding factor, normally localised to tether cell kinocilia. We also show that embryonic movement plays a minor role in the formation of normal otoliths.

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“…8A). Tether cilia are present on tether cells, and readily bind otolith precursor particles (Riley et al, 1997;Tanimoto et al, 2011) (Fig. 8B,C).…”

Section: Discussionmentioning

confidence: 99%

Section: An Otolith Precursor-binding Factor?mentioning

confidence: 99%

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The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle

et al. 2012

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“…This suggests that neither signaling pathway is epistatic to the other, and that neither anterior nor posterior fate is a 'default' identity. However, these otocysts that are deficient in both FGF and Hh signaling do initially show a symmetric polarity -for example, at both poles of the otocyst they develop small otoliths (see Glossary, Box 1) and groups of ciliated tether cells, which are thought to be precocious sensory hair cells (Riley et al, 1997;Tanimoto et al, 2011) -but they never go on to manifest clear AP patterning.…”

Section: Patterning the Ap Axis Of The Earmentioning

confidence: 99%

Shaping sound in space: the regulation of inner ear patterning

2012

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There was an error in Development 139, 245-257.On p. 252, in the second paragraph of the section 'Establishing gradients and boundaries in the developing cochlea', it should read 'In adults…from high (basal) to low (apical).'The authors apologise to readers for this mistake. Development 139, 826 (2012) so is not yet available in most cases. This review will summarize recent findings on the identity of these signaling and morphogen molecules and how they are coordinated in space and time to generate the tissue and cellular architecture of the ear. From placode to ear -how graded signals turn ectoderm into the inner earThe entire inner ear and its associated sensory ganglia derive from the otic placode (see Glossary, Box 1). It is one of a series of cranial placodes that collectively give rise to all craniofacial sensory organs, the lens and a subset of cranial ganglia (Baker and Bronner-Fraser, 2001;Schlosser, 2010). The precursors of different placodes are distributed in an anterior-posterior (AP) sequence around the rostral neural plate (see Glossary, Box 1) termed the pre-placodal domain (PPD) (Schlosser, 2006;Streit, 2007). The PPD is induced by signals, such as FGFs, from both the neural plate and the underlying cranial mesoderm, and inhibition of both Wnt and BMP signaling is required to correctly position the PPD at the neural plate border and to prevent it from extending into the embryonic trunk (Kwon et al., 2010;Litsiou et al., 2005).It is now well established that FGF signals are both necessary and sufficient to induce early otic placode markers from competent pre-placodal ectoderm (Fig. 2) (Ohyama et al., 2007;Schimmang, 2007), although both the location of the FGF signals and the specific FGFs responsible for otic induction vary from species to species. The earliest markers of the future inner ear that are induced in response to FGF signaling are members of the paired homeoboxcontaining Pax2/5/8 transcription factor family -Pax8 in anamniotes and Pax2 in amniotes (Groves and Bronner-Fraser, 2000;Heller and Brandli, 1999;Ohyama and Groves, 2004;Pfeffer et al., 1998). Fate-mapping studies in mice and chick have suggested that although the Pax2-expressing domain is likely to contain all the progenitors of the inner ear, it also harbors cells that will give rise to the epibranchial placodes (see Glossary, Box 1) and epidermis (Ohyama and Groves, 2004;Ohyama et al., 2007;Streit, 2001). This Pax2-expressing progenitor domain has been termed the pre-otic field or the otic-epibranchial progenitor domain (OEPD) (Ladher et al., 2000;Freter et al., 2008).The refinement of the OEPD into distinct otic, epibranchial and epidermal territories is regulated by graded Wnt signals emanating from the midline (Fig. 2) (Ohyama et al., 2006). Examination of the cranial region of Wnt reporter mice revealed that OEPD cells closest to the neural plate, which are fated to form the otic placode, receive high levels of Wnt signaling, whereas more lateral OEPD cells, fated to form epidermis and the epibranchial placodes, receiv...

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“…Compared with mammals (see a review by Rübsamen and Lippe 1998), the zebrafish is a unique model for the study of early development of hearing and balance in vertebrates because the inner ear of zebrafish embryos is easily accessible for live imaging, physiological recording, and genetic manipulation (Waterman and Bell 1984;Haddon and Lewis 1996;Nicolson et al 1998;Bever and Fekete 2002;Whitfield 2002;Nicolson 2005;Zeddies and Fay 2005;Tanimoto et al 2011). Previous studies have reported on the development of auditory sensitivity in a few juvenile and adult teleosts using various physiological methods (Corwin 1983;Kenyon 1996;Higgs et al 2003;Sisneros and Bass 2005;Vasconcelos and Ladich 2008;Alderks and Sisneros 2011;Lechner et al 2012).…”

Section: Development Of Structure and Function Of The Inner Earmentioning

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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Origin of Inner Ear Hair Cells: Morphological and Functional Differentiation from Ciliary Cells into Hair Cells in Zebrafish Inner Ear

Abstract: Auditory and vestibular functions in vertebrates depend

Cited by 56 publications

References 64 publications

The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle

The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle

Shaping sound in space: the regulation of inner ear patterning

Early Development of Hearing in Zebrafish

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