Hair cell replacement in avian vestibular epithelium: Supporting cell to Type I hair cell

Weisleder, Pedro; Tsue, Terance T.; Rubel, Edwin W.

doi:10.1016/0378-5955(94)00169-q

Cited by 58 publications

(37 citation statements)

References 29 publications

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“…It has been suggested that regenerating type II hair cells transdifferentiate into type I hair cells (Favre and Sans, 1979;Weisleder et al, 1995). Several lines of evidence support that view.…”

Section: Discussionsupporting

confidence: 48%

“…Several lines of evidence support that view. First, type II hair cells precede type I cells by several weeks and regenerate in regions in which type I cells will develop in the future (Weisleder and Rubel, 1993;Weisleder et al, 1995;Masetto and Correia, 1997a). Second, no increase in apoptosis occurred when calyceal terminals were regenerating, as would be expected if type II cells were dying to be replaced.…”

Section: Discussionmentioning

confidence: 95%

“…Mitotic division was observed in, or immediately adjacent to, the support cell layer in which presumed regenerating daughter cells (Fig. 2c, arrowhead) were differentiating into new hair cells (Weisleder et al, 1995). It should be noted that, given our level of observation, it is also possible that these few observed cells were not regenerating, but instead were either dying or damaged hair cells.…”

Section: Ototoxic Lesionmentioning

confidence: 98%

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Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

Zakir

Dickman²

2006

J. Neurosci.

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Regeneration of receptor cells and subsequent functional recovery after damage in the auditory and vestibular systems of many vertebrates is well known. Spontaneous regeneration of mammalian hair cells does not occur. However, recent approaches provide hope for similar restoration of hearing and balance in humans after loss. Newly regenerated hair cells receive afferent terminal contacts, yet nothing is known about how reinnervation progresses or whether regenerated afferents finally develop normal termination fields. We hypothesized that neural regeneration in the vestibular otolith system would recapitulate the topographic phenotype of afferent innervation so characteristic of normal development. We used an ototoxic agent to produce complete vestibular receptor cell loss and epithelial denervation, and then quantitatively examined afferent regeneration at discrete periods up to 1 year in otolith maculas. Here, we report that bouton, dimorph, and calyx afferents all regenerate slowly at different time epochs, through a progressive temporal sequence. Furthermore, our data suggest that both the hair cells and their innervating afferents transdifferentiate from an early form into more advanced forms during regeneration. Finally, we show that regeneration remarkably recapitulates the topographic organization of afferent macular innervation, comparable with that developed through normative morphogenesis. However, we also show that regenerated terminal morphologies were significantly less complex than normal fibers. Whether these structural fiber changes lead to alterations in afferent responsiveness is unknown. If true, adaptive plasticity in the central neural processing of motion information would be necessitated, because it is known that many vestibular-related behaviors fully recover during regeneration.

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Section: Discussionsupporting

confidence: 48%

Section: Discussionmentioning

confidence: 95%

Section: Ototoxic Lesionmentioning

confidence: 98%

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Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

Zakir

Dickman²

2006

J. Neurosci.

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“…For example, the important compensatory vestibuloocular reflex (VOR) is diminished or even abolished following administration of ototoxic agents (Carey et al 1996;Goode et al 2001;Matsui et al 2003;Wersäll and Hawkins 1962), as are the vestibulocollic (VCR, Goode et al 1999) and the visual optokinetic responses (Wersäll and Hawkins 1962). It is now well established that, in time, regeneration of vestibular hair cells, followed by their reinnervation, occurs after the cessation of ototoxic treatments in several animal classes, including birds (Boyle et al 2001;Dye et al 1999;Kevetter et al 2000;Masetto and Correia 1997a, b;Rubel 1992, 1993;Weisleder et al 1995), amphibians (Baird et al 1993), and to a lesser extent mammals Rubel et al 1995;Warchol et al 1993). The morphological regeneration in the vestibular system of birds has been shown to produce some functional recovery of behavioral responses.…”

Section: Introductionmentioning

confidence: 99%

Posture, Head Stability, and Orientation Recovery During Vestibular Regeneration In Pigeons

Dickman

Lim

2004

JARO

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Compensatory behavior such as oculomotor, gaze, and postural responses that occur during movement largely depend upon a functioning vestibular system. In the present study, the initial loss and subsequent recovery of postural and head stability in pigeons undergoing vestibular regeneration were examined. Adult pigeons were trained to manipulate a straight run chamber to peck an illuminated key for fluid reward. Six behavioral measures assessing performance, posture, and head stability were quantified. These included run latency, steps (walking), path negotiation (lane changes), gaze saccades, head bobs, and head shakes. Once normative values were obtained for four birds, complete lesion of all receptor cells and denervation of the epithelia in the vestibular endorgans were produced using a single intralabyrinthine application of streptomycin sulfate. Each bird was then tested at specific times during regeneration and the same behavioral measures examined. At 7 days post-streptomycin treatment (PST), all birds exhibited severe postural and head instability, with tremors, head shakes, staggering, and circling predominating. No normal trial runs, walking, gaze saccades, or head bobs were present. Many of these dysfunctions persisted through 3-4 weeks PST. Gradually, tremor and head shakes diminished and were replaced with an increasing number of normal head bobs during steps and gaze saccades. Beginning at 4 weeks PST, but largely inaccurate, was the observed initiation of directed steps, less staggering, and some successful path negotiation. As regeneration progressed, spatial orientation and navigation ability increased and, by 49 days PST, most trials were successful. By 70 days PST, all birds had recovered to pretreatment levels. Thus, it was observed that ataxia must subside, coincident with normalized head and postural stability prior to the recovery of spatial orientation and path navigation recovery. Parallels in recovery were drawn to hair cell regeneration and afferent responsiveness, as inferred from present results and those in other investigations.

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“…A vian vestibular receptors have been shown to continuously produce new hair cells (HCs), and to spontaneously renew HCs following injury (1)(2)(3)(4). In birds, renewal of vestibular HCs results in a return of function (5)(6)(7).…”

mentioning

confidence: 99%

Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function

Kopke

Jackson

et al. 2001

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

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The vestibules of adult guinea pigs were lesioned with gentamicin and then treated with perilymphatic infusion of either of two growth factor mixtures (i.e., GF I or GF II). GF I contained transforming growth factor ␣ (TGF␣), insulin-like growth factor type one (IGF-1), and retinoic acid (RA), whereas GF II contained those three factors and brain-derived neurotrophic factor. Treatment with GF I significantly enhanced vestibular hair cell renewal in ototoxin-damaged utricles and the maturation of stereociliary bundle morphology. The addition of brain-derived neurotrophic factor to the GF II infusion mixture resulted in the return of type 1 vestibular hair cells in ototoxin-damaged cristae, and improved vestibular function. These results suggest that growth factor therapy may be an effective treatment for balance disorders that are the result of hair cell dysfunction and͞or loss.

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Hair cell replacement in avian vestibular epithelium: Supporting cell to Type I hair cell

Cited by 58 publications

References 29 publications

Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

Posture, Head Stability, and Orientation Recovery During Vestibular Regeneration In Pigeons

Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function

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