Hair cells in non-vertebrate models: Lower chordates and molluscs

Burighel, Paolo; Caicci, Federico; Manni, Lucia

doi:10.1016/j.heares.2010.03.087

Cited by 50 publications

(70 citation statements)

References 54 publications

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“…In fact, the facial motoneurons have been implied to be among the earliest chordate motoneurons [Dufour et al, 2006], consistent with the finding of efferent terminals on sensory cells in chordates that have certain features in common with hair cells [Burighel et al, 2011]. In contrast to these suggestive outgroup data, hagfish, a basal group of jawless vertebrates, lacked the evidence for the existence of ear efferents that had been found in lampreys [Köppl, 2011].…”

Section: Evolutionary Origin Of Efferent Innervation To Hair Cellsmentioning

confidence: 60%

“…Furthermore, efferent neurons were labeled from the ear, but not the lateral line system, in both hagfish and lampreys [Fritzsch, 1999;Köppl, 2011]. Given that facial motoneurons may already exist in chordates [Dufour et al, 2006], which also have hair-cell precursors that receive efferent innervation [Burighel et al, 2011], it is thus possible that facial motoneuron input to hair cell precursors predates ear formation.…”

Section: Evolutionary Origin Of Efferent Innervation To Hair Cellsmentioning

confidence: 99%

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Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Sienknecht¹,

Köppl²,

Fritzsch

2014

Brain Behav Evol

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The function of the inner ear critically depends on mechanoelectrically transducing hair cells and their afferent and efferent innervation. The first part of this review presents data on the evolution and development of polarized vertebrate hair cells that generate a sensitive axis for mechanical stimulation, an essential part of the function of hair cells. Beyond the cellular level, a coordinated alignment of polarized hair cells across a sensory epithelium, a phenomenon called planar cell polarity (PCP), is essential for the organ's function. The coordinated alignment of hair cells leads to hair cell orientation patterns that are characteristic of the different sensory epithelia of the vertebrate inner ear. Here, we review the developmental mechanisms that potentially generate molecular and morphological asymmetries necessary for the control of PCP. In the second part, this review concentrates on the evolution, development and function of the enigmatic efferent neurons terminating on hair cells. We present evidence suggestive of efferents being derived from motoneurons and synapsing predominantly onto a unique but ancient cholinergic receptor. A review of functional data shows that the plesiomorphic role of the efferent system likely was to globally shut down and protect the peripheral sensors, be they vestibular, lateral line or auditory hair cells, from desensitization and damage during situations of self-induced sensory overload. The addition of a dedicated auditory papilla in land vertebrates appears to have favored the separation of vestibular and auditory efferents and specializations for more sophisticated and more diverse functions.

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Section: Evolutionary Origin Of Efferent Innervation To Hair Cellsmentioning

confidence: 60%

Section: Evolutionary Origin Of Efferent Innervation To Hair Cellsmentioning

confidence: 99%

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Sienknecht¹,

Köppl²,

Fritzsch

2014

Brain Behav Evol

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“…Stereocilia are graded in length across the hair bundle (Hudspeth, 1985). In ascidians, sensory hair cells of the coronal organ feature hair bundles consisting of actin-based stereocilia that are graded in length across the hair bundle (Burighel et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Repair of traumatized mammalian hair cells via sea anemone repair proteins

Tang

Smith

Watson

2016

Journal of Experimental Biology

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Mammalian hair cells possess only a limited ability to repair damage after trauma. In contrast, sea anemones show a marked capability to repair damaged hair bundles by means of secreted repair proteins (RPs). Previously, it was found that recovery of traumatized hair cells in blind cavefish was enhanced by anemone-derived RPs; therefore, the ability of anemone RPs to assist recovery of damaged hair cells in mammals was tested here. After a 1 h incubation in RP-enriched culture media, uptake of FM1-43 by experimentally traumatized murine cochlear hair cells was restored to levels comparable to those exhibited by healthy controls. In addition, RP-treated explants had significantly more normally structured hair bundles than timematched traumatized control explants. Collectively, these results indicate that anemone-derived RPs assist in restoring normal function and structure of experimentally traumatized hair cells of the mouse cochlea.

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“…Most vertebrate vestibular hair cells are topped with a bundle of stereocilia of increasing length and extended kinocilium and a bipolarity with maximum activation when deflected toward the kinocilium. Squid statocyst hair cells, by contrast, have a bundle of cilia of the same length inclined toward the cell surface (Burighel et al, 2011). In the octopus, hair cells are maximally activated when the cilia are deflected away from the incline (Budelmann and Williamson, 1994).…”

Section: Introductionmentioning

confidence: 99%

“…Invertebrate hair cells are typically primary sensory cells with an action-potential-propagating axon. Unlike the simpler marine invertebrate vestibular systems like that of nautilus, squid statocysts contain both primary and secondary sensory cells (Williamson, 1990;Burighel et al, 2011). This offers a unique opportunity to study and compare, at the cellular level, two types of mechanosensation in the same sensory epithelium.…”

Section: Introductionmentioning

confidence: 99%

Aminoglycoside-Induced Damage in the Statocyst of the Longfin Inshore Squid, Doryteuthis pealeii

Scharr

Mooney

Schweizer

et al. 2014

The Biological Bulletin

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Abstract. Squid are a significant component of the marine biomass and are a long-established model organism in experimental neurophysiology. The squid statocyst senses linear and angular acceleration and is the best candidate for mediating squid auditory responses, but its physiology and morphology are rarely studied. The statocyst contains mechano-sensitive hair cells that resemble hair cells in the vestibular and auditory systems of other animals. We examined whether squid statocyst hair cells are sensitive to aminoglycosides, a group of antibiotics that are ototoxic in fish, birds, and mammals. To assess aminoglycoside-induced damage, we used immunofluorescent methods to image the major cell types in the statocyst of longfin squid (Doryteuthis pealeii). Statocysts of live, anesthetized squid were injected with either a buffered saline solution or neomycin at concentrations ranging from 0.05 to 3.0 mmol l Ϫ1 . The statocyst hair cells of the macula statica princeps were examined 5 h post-treatment. Anti-acetylated tubulin staining showed no morphological differences between the hair cells of saline-injected and non-injected statocysts. The hair cell bundles of the macula statica princeps in aminoglycoside-injected statocysts were either missing or damaged, with the amount of damage being dose-dependent. The proportion of missing hair cells did not increase at the same rate as damaged cells, suggesting that neomycin treatment affects hair cells in a nonlethal manner. These experiments provide a reliable method for imaging squid hair cells. Further, aminoglycosides can be used to induce hair cell damage in a primary sensory area of the statocyst of squid. Such results support further studies on loss of hearing and balance in squid.

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Hair cells in non-vertebrate models: Lower chordates and molluscs

Cited by 50 publications

References 54 publications

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Repair of traumatized mammalian hair cells via sea anemone repair proteins

Aminoglycoside-Induced Damage in the Statocyst of the Longfin Inshore Squid, Doryteuthis pealeii

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