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Robust regeneration of adult zebrafish lateral line hair cells reflects continued precursor pool maintenance.

ABSTRACT: We have examined lateral line hair cell and support cell maintenance in adult zebrafish when growth is largely complete. We demonstrate that adult zebrafish not only replenish hair cells after a single instance of hair cell damage, but also maintain hair cells and support cells after multiple rounds of damage and regeneration. We find that hair cells undergo continuous turnover in adult zebrafish in the absence of damage. We identify mitotically-distinct support cell populations and show that hair cells regenerate from underlying support cells in a region-specific manner. Our results demonstrate that there are two distinct support cell populations in the lateral line, which may help explain why zebrafish hair cell regeneration is extremely robust, retained throughout life, and potentially unlimited in regenerative capacity.

SUBMITTER: Cruz IA

PROVIDER: S-EPMC4450121 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Robust regeneration of adult zebrafish lateral line hair cells reflects continued precursor pool maintenance.

Cruz Ivan A IA Kappedal Ryan R Mackenzie Scott M SM Hailey Dale W DW Hoffman Trevor L TL Schilling Thomas F TF Raible David W DW

Developmental biology 20150411 2

We have examined lateral line hair cell and support cell maintenance in adult zebrafish when growth is largely complete. We demonstrate that adult zebrafish not only replenish hair cells after a single instance of hair cell damage, but also maintain hair cells and support cells after multiple rounds of damage and regeneration. We find that hair cells undergo continuous turnover in adult zebrafish in the absence of damage. We identify mitotically-distinct support cell populations and show that ha ...[more]

PMID: 25869855

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Project description:Key pointsWe investigated hair-cell regeneration in the zebrafish lateral line following the application of the ototoxic compound copper. In early-larval zebrafish (<10 days post-fertilisation), regenerated hair cells drive action potentials (APs) in the afferent neurons 24 h post-copper treatment (24 hpt). Full regeneration of the early-larval neuromasts, the organs containing the hair cells, requires ∼48 h due to the progressive addition of hair cells and synaptic refinement. In older larval zebrafish, regenerated hair cells are active and drive afferent APs by 48 hpt, which is comparable to larvae, but the functional recovery of their neuromasts requires >120 hpt. Afferent terminals within the regenerating neuromast appear to initially contact supporting cells, and their complete ablation prevents the timely reappearance of supporting cells and hair cells. We conclude that the regeneration of zebrafish neuromasts is slower after the initial developmental stages, and that the afferent input plays a key role in driving this process.AbstractHair cells are mechanosensory receptors responsible for transducing auditory and vestibular information into electrical signals, which are then transmitted with remarkable precision to afferent neurons. Different from mammals, the hair cells of lower vertebrates, including those present in the neuromasts of the zebrafish lateral line, regenerate following environmental or chemical insults. Here we investigate the time course of regeneration of hair cells in vivo using electrophysiology, two-photon imaging and immunostaining applied to wild-type and genetically encoded fluorescent indicator zebrafish lines. Functional hair cells drive spontaneous action potentials in the posterior lateral line afferent fibres, the frequency of which progressively increases over the first 10 days post-fertilisation (dpf). Higher firing-rate fibres are only observed from ∼6 dpf. Following copper treatment, newly formed hair cells become functional and are able to drive APs in the afferent fibres within 48 h in both early-larval (≤8 dpf) and late-larval (12-17 dpf) zebrafish. However, the complete functional regeneration of the entire neuromast is delayed in late-larval compared to early-larval zebrafish. We propose that while individual regenerating hair cells can rapidly become active, the acquisition of fully functional neuromasts progresses faster at early-larval stages, a time when hair cells are still under development. At both ages, the afferent terminals in the regenerating neuromast appear to make initial contact with supporting cells. The ablation of the lateral line afferent neurons prevents the timely regeneration of supporting cells and hair cells. These findings indicate that the afferent system is likely to facilitate or promote the neuromast regeneration process.

Project description:In humans, the absence or irreversible loss of hair cells, the sensory mechanoreceptors in the cochlea, accounts for a large majority of acquired and congenital hearing disorders. In the auditory and vestibular neuroepithelia of the inner ear, hair cells are accompanied by another cell type called supporting cells. This second cell population has been described as having stem cell-like properties, allowing efficient hair cell replacement during embryonic and larval/fetal development of all vertebrates. However, mammals lose their regenerative capacity in most inner ear neuroepithelia in postnatal life. Remarkably, reptiles, birds, amphibians, and fish are different in that they can regenerate hair cells throughout their lifespan. The lateral line in amphibians and in fish is an additional sensory organ, which is used to detect water movements and is comprised of neuroepithelial patches, called neuromasts. These are similar in ultra-structure to the inner ear's neuroepithelia and they share the expression of various molecular markers. We examined the regeneration process in hair cells of the lateral line of zebrafish larvae carrying a retroviral integration in a previously uncharacterized gene, phoenix (pho). Phoenix mutant larvae develop normally and display a morphologically intact lateral line. However, after ablation of hair cells with copper or neomycin, their regeneration in pho mutants is severely impaired. We show that proliferation in the supporting cells is strongly decreased after damage to hair cells and correlates with the reduction of newly formed hair cells in the regenerating phoenix mutant neuromasts. The retroviral integration linked to the phenotype is in a novel gene with no known homologs showing high expression in neuromast supporting cells. Whereas its role during early development of the lateral line remains to be addressed, in later larval stages phoenix defines a new class of proteins implicated in hair cell regeneration.

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Robust regeneration of adult zebrafish lateral line hair cells reflects continued precursor pool maintenance.

Publications

Robust regeneration of adult zebrafish lateral line hair cells reflects continued precursor pool maintenance.

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