Developmental origin of shark electrosensory organs

Freitas, Renata; Zhang, Guangjun; Albert, James S.; Evans, David H.; Cohn, Martin J.

doi:10.1111/j.1525-142x.2006.05076.x

Cited by 47 publications

(56 citation statements)

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“…Beyond cochlear mechanics, our findings have important implications for all sensory systems, which (with the exception of a few species of lizards) all contain accessory gelatinous structures overlying hair cells. Gels, such as the cupulae and otolithic membranes found in the vestibular system and those covering electrosensory hair cells on the skin of aquatic vertebrates, play a key role in hair cell stimulation (58)(59)(60). Much like the TM, these gels are poised to undergo deformations in response to transduction currents.…”

Section: Resultsmentioning

confidence: 99%

Electrokinetic properties of the mammalian tectorial membrane

Ghaffari

Page

Farrahi

et al. 2013

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

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The tectorial membrane (TM) clearly plays a mechanical role in stimulating cochlear sensory receptors, but the presence of fixed charge in TM constituents suggests that electromechanical properties also may be important. Here, we measure the fixed charge density of the TM and show that this density of fixed charge is sufficient to affect mechanical properties and to generate electrokinetic motions. In particular, alternating currents applied to the middle and marginal zones of isolated TM segments evoke motions at audio frequencies (1-1,000 Hz). Electrically evoked motions are nanometer scaled (∼5-900 nm), decrease with increasing stimulus frequency, and scale linearly over a broad range of electric field amplitudes (0.05-20 kV/m). These findings show that the mammalian TM is highly charged and suggest the importance of a unique TM electrokinetic mechanism.cochlear amplification | cochlear mechanics | mechanoelectrical transduction | motility T he mammalian cochlea is a remarkable sensor capable of detecting and analyzing sounds that generate subatomic vibrations (1). This extraordinary sensing property depends on mechanoelectrical transduction (MET) of cochlear hair cells (2, 3), which are functionally classified as inner and outer hair cells (OHCs). Both types of hair cells project stereociliary hair bundles from their apical surface toward an overlying extracellular matrix called the tectorial membrane (TM). Because of its strategic position above the hair bundles, the TM is believed to play a critical role in bundle deflection. Recently, genetic studies confirmed the importance of the TM in hair cell stimulation by highlighting how mutations of TM proteins cause severe hearing deficits, even when the TM and its structural attachments appear to be normal under electron microscopy (4-8).Despite significant evidence establishing the importance of the TM in normal cochlear function, relatively little is known about the TM's basic physicochemical properties and mechanistic role. Historically, models of cochlear function have represented the TM as a stiff lever with a compliant hinge, as a resonant mass-spring system, or as an inertial body (9-16). However, these models exclude important phenomena, such as longitudinal coupling (17)(18)(19)(20), and assume that only mechanical properties of the TM are important. It now is clear that the TM is a biphasic poroelastic tissue (21), which manifests longitudinal coupling in the form of traveling waves (18)(19)(20).Furthermore, TM macromolecules comprise not only mechanical constituents (21-26) such as collagen fibrils, but also charged constituents such as glycosaminoglycans (GAGs), which might affect mechanical properties (Fig. 1) (27-35). GAGs in the TM carry sulfate (SO 3 − ) and carboxyl (COO − ) charge groups, which are fully ionized at physiological pH and neutralized at acidic pH values (pKs between 2 and 4) (27). In contrast, the net charge on TM collagen constituents is small at physiological pH because the net charge of amino (NH 3 + ) and carboxyl groups is z...

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Section: Resultsmentioning

confidence: 99%

Electrokinetic properties of the mammalian tectorial membrane

Ghaffari

Page

Farrahi

et al. 2013

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

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“…In the shark Scyliorhinus canicula, electrosensory hair cells were proposed to be neural crest-derived owing to their expression of Sox8 and the carbohydrate epitope recognized by the HNK1 antibody (Freitas et al, 2006). However, neither of these proposed markers of the neural crest lineage is neural crest-specific (indeed, HNK1 was reported not to label neural crest cells in embryos of a related shark species, S. torazame; Kuratani and Horigome, 2000), and gene expression alone does not indicate lineage.…”

Section: Sox3 Is Expressed Throughout the Development Of Both Mechanomentioning

confidence: 99%

“…Only five molecular markers for vertebrate ampullary organs have previously been reported: in axolotl, Dlx3 and Msx2 (Metscher et al, 1997), and in sharks, Eya4 (O'Neill et al, 2007), Sox8, and ephrinB2 (Freitas et al, 2006). Hence, Sox3 is a novel molecular marker for vertebrate ampullary organs and also the first published molecular marker for actinopterygian ampullary organs.…”

Section: Sox3 Is Expressed Throughout the Development Of Both Mechanomentioning

confidence: 99%

“…Electrosensory hair cells, which are innervated by lateral line placode-derived neurons, are collected together with supporting cells in ''ampullary organs'' connected to the surface by canals filled with electrically conductive jelly (reviewed in Jørgensen, 2005). Shark electrosensory hair cells were recently proposed, on the basis of gene expression alone, to be derived from the neural crest (Freitas et al, 2006). However, in a tetrapod, the axolotl Ambystoma mexicanum (a urodele amphibian), fate-mapping and ablation studies showed that ampullary organs and the electrosensory hair cells within them arise from lateral line placodes (Northcutt et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Molecular analysis of neurogenic placode development in a basal ray‐finned fish

Modrell

Buckley

Baker

2011

Genesis

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Summary: Neurogenic placodes are transient, thickened patches of embryonic vertebrate head ectoderm that give rise to the paired peripheral sense organs and most neurons in cranial sensory ganglia. We present the first analysis of gene expression during neurogenic placode development in a basal actinopterygian (rayfinned fish), the North American paddlefish (Polyodon spathula). Pax3 expression in the profundal placode confirms its homology with the ophthalmic trigeminal placode of amniotes. We report the conservation of expression of Pax2 and Pax8 in the otic and/or epibranchial placodes, Phox2b in epibranchial placode-derived neurons, Sox3 during epibranchial and lateral line placode development, and NeuroD in developing cranial sensory ganglia. We identify Sox3 as a novel marker for developing fields of electrosensory ampullary organs and for ampullary organs themselves. Sox3 is also the first molecular marker for actinopterygian ampullary organs. This is consistent with, though does not prove, a lateral line placode origin for actinopterygian ampullary organs. genesis 49:278-294, 2011. V V C 2011 Wiley-Liss, Inc.

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“…However, cell-lineage studies have shown that mechanoreceptor development in amphibians and teleosts also involves neural-crest cells (Collazo et al, 1994). Recently, Freitas et al (2006) reported that the electroreceptors of sharks may have a dual origin: from an epithelial condensation and from the cranial neural-crest-derived mesenchyme. The similar development of JOO in rats could suggest that this plays a role as sensory receptor.…”

Section: Juxta-oral Organ In Rat Embryomentioning

confidence: 99%

Development of the Juxta‐Oral Organ in Rat Embryo

Velasco

2012

The Anatomical Record

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The aim of this work is to clarify the development and morphology of the juxta-oral organ (JOO) in rat embryos from Day (E)14 to 19. Furthermore, in the region of the JOO, an analysis was made of the expression of the monoclonal antibody HNK-1, which recognizes cranial neural-crest cells. In this study, we report that JOO develops from an epithelial condensation at the end of the transverse groove of the primitive mouth at E14. During E15, it invaginates and is disconnected from the oral epithelium. At E16, the JOO forms an solid epithelial cord with three parts (anterior, middle, and posterior) and is related to the masseter, temporal, medial pterygoid, and tensor veli palatini muscles. During E17-19, no significant changes were detected in their position. Both the mesenchyme caudal to the anlage of the JOO at E14, as well as the mesenchyme that surrounds the bud of the JOO at E15, expressed positivity for HNK-1. Our results suggest that the mesenchyme surrounding the JOO at E15 could emit some inductive signal for the JOO to reach its position at E16. This work shows for the first time that the cranial neural-crest-derived mesenchyme participates in the development of the JOO. Anat Rec,

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Developmental origin of shark electrosensory organs

Cited by 47 publications

References 47 publications

Electrokinetic properties of the mammalian tectorial membrane

Electrokinetic properties of the mammalian tectorial membrane

Molecular analysis of neurogenic placode development in a basal ray‐finned fish

Development of the Juxta‐Oral Organ in Rat Embryo

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