Striated organelle, a cytoskeletal structure positioned to modulate hair-cell transduction

Abstract

The striated organelle (SO), a cytoskeletal structure located in the apical region of cochlear and vestibular hair cells, consists of alternating, cross-linked, thick and thin filamentous bundles. In the vestibular periphery, the SO is well developed in both type I and type II hair cells. We studied the 3D structure of the SO with intermediate-voltage electron microscopy and electron microscope tomography. We also used antibodies to α-2 spectrin, one protein component, to trace development of the SO in vestibular hair cells over the first postnatal week. In type I cells, the SO forms an inverted open-ended cone attached to the cell membrane along both its upper and lower circumferences and separated from the cuticular plate by a dense cluster of exceptionally large mitochondria. In addition to contacts with the membrane and adjacent mitochondria, the SO is connected both directly and indirectly, via microtubules, to some stereociliary rootlets. The overall architecture of the apical region in type I hair cells-a striated structure restricting a cluster of large mitochondria between its filaments, the cuticular plate, and plasma membrane-suggests that the SO might serve two functions: to maintain hair-cell shape and to alter transduction by changing the geometry and mechanical properties of hair bundles.actin | cytoskeleton | stereocilia | ultrastructure | sensory receptors H air-cell stereocilia are important for mechanotransduction. Much is known about their structure, their mechanical properties, and their geometric arrangement (1-3). These cells are embedded in the cuticular plate, a dense structure composed of an actin gel (4) located at the apical end of the hair cell, which is thought to act as a rigid platform, helping stereocilia return to their resting positions after stimulus-evoked displacements (5, 6). What has never been investigated is how the cuticular plate might be stabilized by structures underneath it. Do these structures provide a foundation for the cuticular plate and the hair bundle?One such structure is the striated organelle (SO), also known as a laminated (or Friedman's) body, which is a cytoskeletal lattice underlying the apicolateral hair-cell membrane and consisting of alternating thick and thin filament bundles. When first described in vestibular hair cells in the 1960s, this structure was thought to be a pathological feature (7,8). It was later found to be a normal component of mammalian vestibular and cochlear inner, but not outer, hair cells (9-11). A striated structure, similar in position but differing in morphological details, has been described in other vertebrates (12)(13)(14).Slepecky et al. provided a description of the SO (10, 15, 16), including the periodicity of its filaments, their radial direction, attachment to the plasma membrane, and association with microtubules. Previous studies, even those based on conventional transmission electron microscopy (TEM) and deep-etch freeze fracture (9,10,15,17,18), did not provide a picture of the 3D structure of the organelle. Elec...

Remodeling of the Inner Hair Cell Microtubule Meshwork in a Mouse Model of Auditory Neuropathy AUNA1

“…In this scenario, the excess actin would expand the cuticular plate and lead to a swollen appearance under electron microscopy. Because of the dense and packed structure of the cuticular plate, the remodeling of the actin network would drag together the other components of the cuticular plate, such as spectrin (Drenckhahn et al, 1991; Furness et al, 2008; Vranceanu et al, 2012). However, under this hypothesis, the increase in actin volume would be homogeneous within the cuticular plate of the hair cells.…”

“…How can these two events be related to each other? Because the rootlets emanating from the stereocilia are embedded within the cuticular plate (DeRosier and Tilney, 1989; Furness et al, 2008; Vranceanu et al, 2012), loss of the anchoring structure might impede the stability of the stereocilia and lead to their collapse (Liberman, 1987; Kitajiri et al, 2010). Another cause of the severed stereocilia can be due to the dense microtubule matrix at the base of the stereocilia, which could interfere with key components of trafficking and delivery toward the stereocilia (Schneider et al, 2002; Zhang et al, 2012; Drummond et al, 2015).…”

LMO7 deficiency reveals the significance of the cuticular plate for hearing function

“…This gap in knowledge is in part attributable to the lack of molecular tools to manipulate the cuticular plate specifically. Molecular studies have uncovered a few resident proteins such as spectrin, tropomyosin, supervillin [23][24][25][26][27] , but loss-of-function studies for these proteins have not been undertaken to date. In this study, we report the discovery of a novel component of the cuticular plate, a hair cell-enriched protein called LIM only protein 7 (LMO7).…”

The cuticular plate: A riddle, wrapped in a mystery, inside a hair cell

“…Interestingly, electron‐microscopic tomography studies of vestibular hair cells have found that some rootlets bend within the cuticular plate, at an angle of up to 110°, and contact the plasma membrane opposite the kinocillium (Vranceanu et al, ). Some stereociliary rootlets have also been observed to fully traverse through the cuticular plate into the cytoplasm below (Takasaka et al, ; Furness et al, ; Vranceanu et al, ). This may provide additional anchoring for the rootlets.…”