The development of links between stereocilia in hair cells of the chick basilar papilla

Pickles, James O.; Perger, M. Von; Rouse, Greg W.; Brix, Jutta

doi:10.1016/0378-5955(91)90116-q

Cited by 37 publications

(25 citation statements)

References 25 publications

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“…3 B and C). Finally, does the mechanism of tip-link regeneration differ from the mechanism of initial insertion during bundle development (11)? With the development of the tip-link regeneration assay, we can now investigate the mechanism of assembly of the transduction apparatus and address these and other questions.…”

Section: Discussionmentioning

confidence: 99%

Regeneration of broken tip links and restoration of mechanical transduction in hair cells

Zhao

Yamoah

Gillespie

1996

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

206

196

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A hair cell's tip links are thought to gate mechanoelectrical transduction channels. The susceptibility of tip links to acoustic trauma raises questions as to whether these fragile structures can be regenerated. We broke tip links with the calcium chelator 1,2-bis(O-aminophenoxy)ethane-N,N,N,N-tetraacetic acid and found that they can regenerate, albeit imperfectly, over several hours. The time course of tip-link regeneration suggests that this process may underlie recovery from temporary threshold shifts induced by noise exposure. Cycloheximide does not block tip-link regeneration, indicating that new protein synthesis is not required. The calcium ionophore ionomycin prevents regeneration, suggesting regeneration normally may be stimulated by the reduction in stereociliary Ca 2؉ when gating springs rupture and transduction channels close. Supporting the equivalence of tip links with gating springs, mechanoelectrical transduction returns over the same time period as tip links; strikingly, adaptation is substantially reduced, even 24 hr after breaking tip links.Hair cells transduce displacements of their mechanically sensitive hair bundles into electrical signals (1, 2). A hair bundle consists of about 100 stereocilia, each of which contains hundreds of crosslinked actin filaments enshrouded by plasma membrane. Stereocilia are arrayed in rows of increasing height, producing a bundle that exhibits mirror symmetry along a central axis; this axis also corresponds to the bundle's axis of highest displacement sensitivity. When a bundle is displaced along this axis, the tip of each shorter stereocilium slides along the side of its tallest neighbor. Such displacements stretch elastic mechanical elements called gating springs, which open transduction channels (3). Optimally poised to be gating springs, tip links are 5 ϫ 150 nm extracellular filaments that stretch from the tip of a stereocilium to the side of its neighbor, parallel to the plane of mirror symmetry (4). Bundle displacements that stretch tip links also open transduction channels, and displacements that slacken tip links permit channels to close. Because 1,2-bis(O-aminophenoxy)ethane-N,N,NЈ,NЈ-tetraacetic acid (BAPTA) eradicates tip links, simultaneously disrupting transduction by disengaging gating springs, tip links are thought to either be gating springs themselves or connect in series with the gating spring (5).A hair cell's transduction apparatus survives constant stimulation and occasionally experiences stimuli that can break tip links (6). If tip links indeed play an essential role in transduction, broken tip links should be replaced to maintain sensitivity to mechanical displacements. We intentionally broke tip links with BAPTA and found that they regenerate over a period of several hours. Regeneration is imperfect, as many links arise that connect stereociliary pairs not oriented along the plane of mirror symmetry. Although restoration of tip links does not require new protein synthesis, elevation of intracellular Ca 2ϩ levels effectively prev...

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Section: Discussionmentioning

confidence: 99%

Regeneration of broken tip links and restoration of mechanical transduction in hair cells

Zhao

Yamoah

Gillespie

1996

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

206

196

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“…The development of hair-bundle links has been studied in detail for the hair cells of the avian basilar papilla and in the OHCs of the mouse cochlea (Pickles et al, 1991;Goodyear et al, 2005). Abundant links are associated with the surface of immature developing hair bundles and on the basis of morphological studies alone it is not clear to which class or type these multiple links belong.…”

Section: Development Of Linksmentioning

confidence: 99%

“…Abundant links are associated with the surface of immature developing hair bundles and on the basis of morphological studies alone it is not clear to which class or type these multiple links belong. In the bird papilla, SEM studies originally suggested tip and ankle links both develop from the spokelike, radial arrays of multiple links that are found interconnecting the distal tips of the short immature stereocilia prior to their elongation (Pickles et al, 1991). Immunohistochemical studies with monoclonal antibodies indicate that proteins associated with ankle links, tip links and shaft connectors are distributed all over the surface of the developing stereocilia of immature hair bundles in the avian papilla before becoming restricted to their normal, adult-type distributions (Bartolami et al, 1991;Goodyear and Richardson, 1999;.…”

Section: Development Of Linksmentioning

confidence: 99%

“…In the bird, transducer currents and loading with the styryl dye FM1-43, a permeant blocker of the hair cell's mechanotransducer channel (Gale et al, 2001), can be first measured and detected at embryonic day 12 (Si et al, 2003). This is some three days after oblique links can be first seen extending from the stereociliary tips by SEM (at E9, coincident with the onset of phase 1 elongation) and shortly before the densities that characterise the insertion points (attachment plaques) of the tip links can be first sporadically observed by TEM (at E13) (Pickles et al, 1991). In the mouse utricle, measures of transduction currents and FM1-43 dye loading indicate transduction begins at E17 (Géléoc and Holt, 2003), some 2 days after the first appearance of potential tip links (Denman- Johnson and Forge, 1999).…”

Section: Development Of Transductionmentioning

confidence: 99%

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Development of the hair bundle and mechanotransduction

Nayak

Ratnayaka²,

Goodyear³

et al. 2007

Int. J. Dev. Biol.

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This review focuses on the cellular and molecular mechanisms underlying the development of the sensory hair bundle, an apical specialisation of the hair cell that is essential for mechanotransduction. The structure, function and development of the hair bundle is described, with an emphasis on the properties and possible roles played by the different link types that interconnect the individual elements of the hair bundle -the multiple stereocilia and the single kinocilium. Studies of mouse and zebrafish mutants have revealed that several classes of molecule are required for the genesis and maintenance of hair-bundle structure. These include cell surface molecules that are associated with the different hair-bundle links, along with myosin motors, scaffolding proteins and an actin cross-linker. Finally we consider how differences in the form and shape of hair bundles within and between different sensory organs are generated.

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“…It is already detectable at E17 in the mouse and persists throughout life (Geleoc and Holt, 2003;Goodyear et al, 2005). Pickles et al have proposed that these tip links are a specialisation of the links that join immature stereocilia laterally near their tips (Pickles et al, 1991). Indeed, a dense network of links that connect stereocilia within the growing hair bundle and show dramatic changes between its early developmental and mature stages.…”

Section: Morphogenesis Of the Hair Bundlementioning

confidence: 99%

Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells

El-Amraoui

Petit

2005

Journal of Cell Science

161

131

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The development of links between stereocilia in hair cells of the chick basilar papilla

Cited by 37 publications

References 25 publications

Regeneration of broken tip links and restoration of mechanical transduction in hair cells

Regeneration of broken tip links and restoration of mechanical transduction in hair cells

Development of the hair bundle and mechanotransduction

Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells

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