Postnatal development of the hamster cochlea. II. Growth and differentiation of stereocilia bundles

Abstract

The postnatal development of stereocilia was studied in the Syrian golden hamster. The purpose was to describe the morphological changes underlying the differentiation of stereocilia bundles and to define the time course of their growth in different regions of the cochlea. Differentiation of the hair bundle occurred by progressive changes in stereocilia number, dimensions, and spatial relationships. The overall transformation of the bundle is interpreted as a four-stage process involving the initial production of stereocilia (stage I), differentiation into tall and short populations (stage II), formation of distinct ranks (stage III), and resorption of excess stereocilia (stage IV). The orientation and arrangement of stereocilia during stage II began to occur before the tectorial membrane grew over the hair cell field. Growth in the dimensions of stereocilia occurred continuously throughout these four stages with increases in length and width occurring simultaneously. The time frame of the growth process depended both on location along the organ of Corti and on the type of hair cell. Hair bundles in the basal turn began growing and reached maturity a few days earlier than those in the apical turn. Stereocilia of outer hair cells matured earlier than those of inner hair cells. Outer hair cell stereocilia reached their adult lengths by 14 days after birth, those of inner hair cells between 16 and 18 days after birth. A kinocilium was present on almost all hair cells on the day of birth, but most were eliminated by 14 days after birth. Tip links were observed as early as 4 days after birth, and their growth appeared to be synchronous with the growth of stereocilia. The spatial gradient of stereocilia length, which increased toward the apex in the adult, was nearly the reverse of that seen at birth. The gradient for inner hair cells was associated with a gradient in the rate of stereocilia growth. The data further expand the foundation for interpreting mechanisms underlying the morphogenesis of stereocilia bundles in mammals and for understanding structure-function relationships during development.

Progressive hearing loss and gradual deterioration of sensory hair bundles in the ears of mice lacking the actin-binding protein Eps8L2

“…In contrast, mice lacking Eps8 are profoundly deaf from the onset of hearing (16). The normal development and maintenance of hair bundles requires differential regulation of actin filaments in stereocilia of different length within one bundle and between hair bundles on adjacent hair cells (2,24,25). The mechanical properties of stereocilia are also a function of combinations of actin-binding proteins (26).…”

Espins and the actin cytoskeleton of hair cell stereocilia and sensory cell microvilli

“…The overall length of the stereociliary bundle, commonly scored by measuring the length of the tallest stereocilia within a bundle, varies in a reproducible way according to hair cell type or position. For example, the length of the tallest stereocilia increases 3-fold from base to apex along the cochlear spiral in rodents (or along the proximal-distal axis in the chicken) [13,17,18,22,23], and inner hair cells have longer stereocilia than outer hair cells ( fig. 2B), except at the extreme base [13,22,23].…”

“…For example, the length of the tallest stereocilia increases 3-fold from base to apex along the cochlear spiral in rodents (or along the proximal-distal axis in the chicken) [13,17,18,22,23], and inner hair cells have longer stereocilia than outer hair cells ( fig. 2B), except at the extreme base [13,22,23]. There can also be regular, placespecific variations in the slope of the stereociliary bundle [24].…”

Class III myosins shape the auditory hair bundles by limiting microvilli and stereocilia growth

“…increase of the spacing between stereocilia accompanies their continuous widening and functional maturation during this phase (Kaltenbach et al, 1994).…”

“…The kinocilium, a genuine cilium (Flock and Duvall, 1965), controls the initial positioning and polarity of the developing hair bundle (Jones and Chen, 2008;Deans, 2013). Its migration to the lateral side of the apical surface between E14.5 and E17.5 (Lepelletier et al, 2013) initiates a first phase of growth during which the microvilli-like precursors of the stereocilia that are closest to the kinocilium elongate and widen first, forming the tallest stereocilia row, followed by growth of the other rows (Tilney et al, 1992;Kaltenbach et al, 1994). The kinocilium marks the vertex of the hair bundle (Cotanche and Corwin, 1991;Denman-Johnson and Forge, 1999), whose shape and positioning are constrained by the compartmentalization of the asymmetric cell division proteins Par-6 and Gαi 3 at the apical surface of the hair cell (Ezan et al, 2013;Tarchini et al, 2013;see also Fig.…”