Innervation is required for sense organ development in the lateral line system of adult zebrafish

Wada, Hironori; Dambly‐Chaudière, Christine; Kawakami, Koichi; Ghysen, Alain

doi:10.1073/pnas.1214004110

Cited by 39 publications

(54 citation statements)

References 38 publications

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“…Next we examined the dynamics of neuromast reinnervation throughout adulthood (1,3,6, and 15 mpf) by following the extent of neuromast reinnervation every day after a nerve cut. We observed that the speed of regeneration, represented as the slope of the reinnervation curve, did not change significantly between 1 and 6 mpf, with complete or almost complete regeneration within 5 d after the onset of reinnervation, but was significantly reduced in 15-mpf fish, in which only 25% of neuromasts were reinnervated during the same period ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…This pattern is established around 1 mo postfertilization (mpf) and remains essentially unchanged throughout adulthood, except that each juvenile neuromast gives rise to a number of "accessory" neuromasts through a budding process (4,5) that depends on innervation (6). Bud-neuromasts remain closely associated and form dorsoventrally arranged linear clusters, or "stitches" (7).…”

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Dynamics of axonal regeneration in adult and aging zebrafish reveal the promoting effect of a first lesion

Graciarena

Dambly‐Chaudière

Ghysen

2014

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

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Axonal regeneration is a major issue in the maintenance of adult nervous systems, both after nerve injuries and in neurodegenerative diseases. However, studying this process in vivo is difficult or even impossible in most vertebrates. Here we show that the posterior lateral line (PLL) of zebrafish is a suitable system to study axonal regeneration in vivo because of both the superficial location and reproducible spatial arrangement of neurons and targets, and the possibility of following reinnervation in live fish on a daily basis. Axonal regeneration after nerve cut has been demonstrated in this system during the first few days of life, leading to complete regeneration within 24 h. However, the potential for PLL nerve regeneration has not been tested yet beyond the early larval stage. We explore the regeneration potential and dynamics of the PLL nerve in adult zebrafish and report that regeneration occurs throughout adulthood. We observed that irregularities in the original branching pattern are faithfully reproduced after regeneration, suggesting that regenerating axons follow the path laid down by the original nerve branches. We quantified the extent of target reinnervation after a nerve cut and found that the latency before the nerve regenerates increases with age. This latency is reduced after a second nerve cut at all ages, suggesting that a regeneration-promoting factor induced by the first cut facilitates regeneration on a second cut. We provide evidence that this factor remains present at the site of the first lesion for several days and is intrinsic to the neurons.Schwann cells | axonogenesis | neuromast | sensory system T he potential of adult neurons to regenerate their axons and to reinnervate target organs after injury is not as well understood as early axonogenesis. Whether and how this capability is modified on aging is an even less explored area. In all vertebrates studied so far, neurons of the peripheral nervous system retain the ability to reextend peripheral axons and reestablish functional connections. This ability is thought to involve intrinsic mechanisms of repair as well as extrinsic signals from the local environment, mostly coming from Schwann cells and macrophages (1).The posterior lateral line (PLL) of fish is a convenient yet unexplored sensory system to address the issue of axonal regeneration throughout adulthood. The PLL comprises a set of superficial mechanosensory organs called neuromasts, which are distributed over the body and tail. Neuromasts are composed of a core of mechanosensory hair cells providing information about the local water flow, surrounded by accessory cells. The afferent neurons innervating neuromasts are clustered in a ganglion posterior to the otic vesicle, and their peripheral axons extend toward the tail, right under the skin. This sensory system is involved in a large repertoire of behaviors (2).The juvenile PLL of zebrafish comprises four lines of neuromasts that extend at different dorsoventral levels, totaling about 50 organs (3). This pattern is estab...

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Dynamics of axonal regeneration in adult and aging zebrafish reveal the promoting effect of a first lesion

Graciarena

Dambly‐Chaudière

Ghysen

2014

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

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“…MCs also give rise to postembryonic NMs suggesting that MCs are multipotent progenitors (Wada et al, 2013a). We were surprised that MCs do not react to neo-induced hair cell death.…”

Section: Discussionmentioning

confidence: 99%

Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways

et al. 2015

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Summary In vertebrates, mechano-electrical transduction of sound is accomplished by sensory hair cells. While mammalian hair cells are not replaced when lost, in fish they constantly renew and regenerate after injury. In vivo tracking and cell fate analyses of all dividing cells during lateral line hair cell regeneration revealed that support and hair cell progenitors localize to distinct tissue compartments. Importantly, we find that the balance between self-renewal and differentiation in these compartments is controlled by spatially restricted Notch signaling and its inhibition of Wnt-induced proliferation. The ability to simultaneously study and manipulate individual cell behaviors and multiple pathways in vivo, transforms the lateral line into a powerful paradigm to mechanistically dissect sensory organ regeneration. The striking similarities to other vertebrate stem cell compartments uniquely place zebrafish to help elucidate why mammals possess such low capacity to regenerate hair cells.

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“…However, hair cell regeneration is normal in larval zebrafish that lack a posterior lateral line nerve and associated Schwann cells (Hernandez et al, 2007;Lopez-Schier and Hudspeth, 2006). Interestingly, posterior lateral line neuromasts do not survive in adult zebrafish in the absence of axonal innervation or Schwann cells (Honjo et al, 2011;Lush and Piotrowski, 2014;Wada et al, 2013a). This suggests that the long-term survival or maintenance of neuromast stem cells may depend on signals from axons or Schwann cells.…”

Section: Developmental Dynamicsmentioning

confidence: 99%

Sensory hair cell regeneration in the zebrafish lateral line

Lush

Piotrowski

2014

Developmental Dynamics

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Damage or destruction of sensory hair cells in the inner ear leads to hearing or balance deficits that can be debilitating, especially in older adults. Unfortunately, the damage is permanent, as regeneration of the inner ear sensory epithelia does not occur in mammals. Zebrafish and other non-mammalian vertebrates have the remarkable ability to regenerate sensory hair cells and understanding the molecular and cellular basis for this regenerative ability will hopefully aid us in designing therapies to induce regeneration in mammals. Zebrafish not only possess hair cells in the ear but also in the sensory lateral line system. Hair cells in both organs are functionally analogous to hair cells in the inner ear of mammals. The lateral line is a mechanosensory system found in most aquatic vertebrates that detects water motion and aids in predator avoidance, prey capture, schooling and mating. Although hair cell regeneration occurs in both the ear and lateral line, most research to date has focused on the lateral line due to its relatively simple structure and accessibility. Here we review the recent discoveries made during the characterization of hair cell regeneration in zebrafish.

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Innervation is required for sense organ development in the lateral line system of adult zebrafish

Cited by 39 publications

References 38 publications

Dynamics of axonal regeneration in adult and aging zebrafish reveal the promoting effect of a first lesion

Dynamics of axonal regeneration in adult and aging zebrafish reveal the promoting effect of a first lesion

Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways

Sensory hair cell regeneration in the zebrafish lateral line

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