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Review
. 2013 Mar:297:91-8.
doi: 10.1016/j.heares.2012.11.010. Epub 2012 Nov 20.

Changes in the adult vertebrate auditory sensory epithelium after trauma

Elizabeth C Oesterle  1
Affiliations
Review

Changes in the adult vertebrate auditory sensory epithelium after trauma

Elizabeth C Oesterle. Hear Res. 2013 Mar.

Abstract

Auditory hair cells transduce sound vibrations into membrane potential changes, ultimately leading to changes in neuronal firing and sound perception. This review provides an overview of the characteristics and repair capabilities of traumatized auditory sensory epithelium in the adult vertebrate ear. Injured mammalian auditory epithelium repairs itself by forming permanent scars but is unable to regenerate replacement hair cells. In contrast, injured non-mammalian vertebrate ear generates replacement hair cells to restore hearing functions. Non-sensory support cells within the auditory epithelium play key roles in the repair processes.

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Figures

Figure 1
Figure 1. Schematic diagrams of auditory hair cell epithelia in adult vertebrate inner ear
(A) Reptilian (alligator lizard) basilar papilla. (B) Bird basilar papilla. (C) Mammalian organ of Corti. All vertebrate auditory epithelia contain mechanosensitive sensory receptor cells, hair cells (red, HC), and support cells (yellow, SC). Hair cells are distributed along the lumenal surface of the epithelium; their cell bodies do not make contact with the basilar membrane (BM). A bundle of hair-like stereocilia (stc) protruding from the apical surface of the hair cell extends into the lumen. In the reptilian basilar papilla (A), a single long cilium called the kinocilium (kc) is present in the mature bundle. Support cells (with the exception of the tectal cells in the organ of Corti) extend the entire depth of the epithelium, from the lumen to the basilar membrane, and their nuclei reside primarily within the basal half of the epithelium. (B) The bird basilar papilla containing tall and short hair cells (HC) is flanked by non-sensory clear cells (C) and hyaline cells (H). (C) The mammalian organ of Corti is a highly patterned, complex tissue that contains a single row of inner hair cells (IHC), 3 rows of outer hair cells (OHC), and support cells with a variety of specialized morphologies. In contrast to non-mammalian vertebrates, support cells in the organ of Corti are structurally and functionally diversified and are subtyped as Hensen’s (H), Tectal (T), Deiters’ (D), inner pillar (IP), outer pillar (OP), inner phalangeal (P), and border (B) cells. Non-sensory inner sulcus cells (IS), Boettcher’s cells (BT), and Claudius cells (C) border the sensory epithelium. Inner phalangeal and border cells are closely associated with inner hair cells, and inner pillar and Deiters’ cells are associated with outer hair cells. Pillar and Deiters’ cells provide rigidity and structure to the epithelium. The tunnel of Corti (TC) and support cell specializations may be adaptations necessary for higher frequency hearing (Dallos and Harris, 1978; Hudspeth, 1985). Excellent descriptions of the normal architecture of the organ of Corti, including descriptions of support cell subtypes, can be found in Spicer and Schulte (1994), Slepecky (1996), and Taylor et al. (2012). Nerve fibers and endings are not depicted in the figure.
Figure 2
Figure 2. Lesion pathologies in severely damaged organ of Corti
Schematic diagrams of the normal organ of Corti (A) and two lesion pathologies seen in severely damaged organ of Corti, the repaired columnar epithelium (B) and the flat epithelium (C). Hair cells (red) are absent in both lesion pathologies. Differentiated support cells (yellow) remain in the repaired columnar epithelium, in contrast to the flat epithelium where non-sensory cells flanking the epithelium (light brown) may migrate into the region formerly occupied by the organ of Corti. Deiters’ cells can spread into the tunnel of Corti area in the repaired columnar epithelium (Taylor et al., 2012). Both damaged epithelial types may constitute the substrate for potential future therapy in clinical cases, and understanding the characteristics of the cells that remain after hair cell loss will be crucial to identifying feasible regenerative procedures. (D–G) Adult C57BL/6 mouse organ of Corti damaged by an aminoglycoside-diuretic combination described previously (single high-dose injection of kanamycin coupled with a single injection of furosemide, Oesterle et al., 2008; Oesterle and Campbell, 2009). Tissues were collected two months after the injections, prepared as whole mounts, immunolabeled for acetylated tubulin (green), and nuclei were counterstained with DAPI (blue) as described previously (Oesterle and Campbell, 2009). All images in D–G are taken from whole-mount preparations of the middle turn. Shown are brightest point projections from confocal Z-series spanning the full depth of the sensory epithelium. (D–E) Repaired columnar epithelium. Some support cells retained in the repaired columnar epithelium continue to express acetylated tubulin (region indicated by the white brackets), a component of differentiated pillar and Deiters’ cells that is associated with the intracellular microtubule bundles present within these support cell subtypes. Acetylated tubulin labeling is also present in the Claudius cell region (C). (F–G) A small stretch of flat epithelium (white arrow) is flanked by regions of repaired columnar epithelium. Note the abrupt transition between the regions and the decreased nuclear density and absence of acetylated tubulin labeling in the flat epithelium. Scale bar in D = 20 µm and applies to panels D–F.
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