Vesicular Glutamate Transporter 3 Is Required for Synaptic Transmission in Zebrafish Hair Cells

Obholzer, Nikolaus; Wolfson, Sean N.; Trapani, Josef G.; Mo, Weike; Nechiporuk, Alex; Busch-Nentwich, Elisabeth M; Seiler, Christoph; Sidi, Samuel; Söllner, Christian; Duncan, Robert N.; Boehland, Andrea; Nicolson, Teresa

doi:10.1523/jneurosci.5230-07.2008

Cited by 300 publications

(370 citation statements)

References 29 publications

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“…The Tol2 trap vector is inserted into the first exon of the deltaA gene; a detailed analysis of this mutant line will be reported elsewhere. The Tg(neurod:EGFP) (Obholzer et al, 2008) and Tg(cldnB:lynGFP) (Haas and Gilmour, 2006) fish strains were obtained from Dr. Nechiporuk (Oregon Health and Science University, Portland, OR) and Dr. Gilmour (European Molecular Biology Laboratory, Heidelberg, Germany), respectively. Males and females of these strains were mated to generate embryos.…”

Section: Methodsmentioning

confidence: 99%

“…Although the vertebrate preplacodal marker six1b (Schlosser, 2006) is expressed broadly in the preplacodal ectoderm until the early somite stage (around 11 hpf), its expression is later confined to sensory placodes, including the zebrafish pLL placode (Bessarab et al, 2004). Since pLLG neurons can first be detected by neurod expression around 10 ss (14 hpf), we next examined the position of neuronal precursors relative to the six1b-positive prepLL domain by double staining for six1b and neurod using Tg(neurod:EGFP) embryos (Obholzer et al, 2008).…”

Section: Delta-mediated Notch Signaling Is Involved In Pllg Formationmentioning

confidence: 99%

“…4 A). We used a Tg(neurod:EGFP); Tg(cldnB:lynGFP) double transgenic line to visualize the pLLG and pLLP (Haas and Gilmour, 2006;Obholzer et al, 2008). We also used PATagRFP, a photoactivatable red fluorescence protein, to label cells locally (Subach et al, 2010).…”

Section: Delta-mediated Notch Signaling Is Involved In Pllg Formationmentioning

confidence: 99%

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Neuron and Sensory Epithelial Cell Fate Is Sequentially Determined by Notch Signaling in Zebrafish Lateral Line Development

Mizoguchi

Togawa²,

Kawakami

et al. 2011

J. Neurosci.

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Sensory systems are specialized to recognize environmental changes. Sensory organs are complex structures composed of different cell types, including neurons and sensory receptor cells, and how these organs are generated is an important question in developmental neurobiology.The posterior lateral line (pLL) is a simple sensory system in fish and amphibians that detects changes in water motion. It consists of neurons and sensory receptor hair cells, both of which are derived from the cranial ectoderm preplacodal region. However, it is not clearly understood how neurons and the sensory epithelium develop separately from the same preplacodal progenitors.We found that the numbers of posterior lateral line ganglion (pLLG) neurons, which are marked by neurod expression, increased in embryos with reduced Notch activity, but the forced activation of Notch reduced their number, suggesting that Notch-mediated lateral inhibition regulates the pLLG cell fate in zebrafish. By fate-mapping analysis, we found that cells adjacent to the pLLG neurons in the pre-pLL placodal region gave rise to the anterior part of the pLL primordium (i.e., sensory epithelial progenitor cells), and that the choice of cell fate between pLLG neuron or pLL primordium was regulated by Notch signaling. Since Notch signaling also affects hair cell fate determination at a later stage, our study suggests that Notch signaling has dual, time-dependent roles in specifying multiple cell types during pLL development.

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Section: Methodsmentioning

confidence: 99%

Section: Delta-mediated Notch Signaling Is Involved In Pllg Formationmentioning

confidence: 99%

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Neuron and Sensory Epithelial Cell Fate Is Sequentially Determined by Notch Signaling in Zebrafish Lateral Line Development

Mizoguchi

Togawa²,

Kawakami

et al. 2011

J. Neurosci.

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“…To record microphonic potentials, a recording micropipette was inserted into the otic vesicle (OV) (Corey et al, 2004;Obholzer et al, 2008;Prober et al, 2008). To apply imperative mechanical stimulation to the macular HCs, a piezoelectric probe or micropipette filled with extracellular solution was positioned adjacent to the otoliths.…”

Section: Methodsmentioning

confidence: 99%

Auditory Input to CNS Is Acquired Coincidentally with Development of Inner Ear after Formation of Functional Afferent Pathway in Zebrafish

Tanimoto¹,

Ota²,

Horikawa³

et al. 2009

J. Neurosci.

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“…(glutamate transporter of IHC synaptic vesicles [37][38][39] ) and otoferlin immunofluorescence throughout the cytosol and along the plasma membrane, both in Otof +/+ and Otof…”

Section: Systems Consequences Of Impaired Vesicle Replenishmentmentioning

confidence: 99%

Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells

et al. 2010

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At the first auditory synapse in mammals, one ribbon-type AZ of the IHC drives one postsynaptic spiral ganglion neuron (SGN) to spike at rates exceeding 100 Hz in silence and 1 kHz upon sound onset 1, 2 . Moreover, SGNs sustain firing rates of several hundred Hz during ongoing acoustic stimulation. In such a steady state, vesicle replenishment has to balance vesicle fusion at the IHC AZ. Accordingly, high rates of initial and sustained exocytosis have been found in hair cells [3][4][5][6][7][8] . Ribbon-type AZs of IHCs replenish readily releasable vesicles at hundreds of Hz over several seconds of stimulation, faster than ribbon synapses in the eye 9-15 and most non-ribbon-type AZs 16(but see ref. 17). This efficient vesicle re-supply maintains a large standing pool of fusion competent synaptic vesicles, which appears to be critical for reliable and temporally precise sound encoding [18][19][20] . and Otof +/+ mice ( Fig. 2a-b The observations of normal RRP size after resting the synapse for more than 30 seconds and of reduced vesicle re-supply during ongoing stimulation prompted us to explore RRP recovery from depletion in paired-pulse experiments (Fig. 3a). RRP recovery, assessed as the paired-pulse ratio for different inter-pulse intervals, was impaired in Otof Pga/Pga mice (Fig. 3b). This indicated a deficit in vesicle replenishment also in the rest period between stimuli. The ΔC m pattern elicited by trains of ten short (10 ms) depolarizations demonstrates the exocytosis phenotype found after a period of rest (30 s voltage-clamp at -84 mV): normal RRP exocytosis but subsequent failure (Fig. 3c). Studying the C m decline after exocytosis we observed normal endocytic membrane retrieval (Fig. 3d). Normal synaptic ultrastructure in Otof Pga/Pga IHCsIn order to explore whether a docking or a priming defect underlies the impairment of vesicle replenishment at Otof Pga/Pga IHC synapses, we studied their ultrastructure using electron microscopy (EM). Both, EM of single ultrathin sections (perpendicular to the 7 plasma membrane and the long axis of the ribbon; Supplementary Fig. 2) as well as EM tomography (Fig. 3e-f High-resolution EM tomography ( Fig. 3e-f) was used to measure the distance of membrane-proximal synaptic vesicles (labeled orange in Fig. 3f) from the plasma membrane under both conditions. The average membrane-membrane distance was approximately 6 nm regardless of condition and genotype (Supplementary Reduced rates but maintained size variability of EPSCsThe stark contrast between the absence of auditory neuron population responses in vivo (Fig. 1) (Fig. 4a-b). We pooled the data from recordings in 5. Fig. 4h-i; Kolmogorov-Smirnov test, p = 0.14). Moreover, we detected action potential generation by recording action currents in the loose-patch configuration (Fig. 4g). Together these results suggest that Otof Pga/Pga synapses should be capable of encoding sound into spiking activity in auditory nerve fibers, albeit at lower rates.In addition, we recorded from SGNs of Otof -/-mice of the same age a...

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Vesicular Glutamate Transporter 3 Is Required for Synaptic Transmission in Zebrafish Hair Cells

Cited by 300 publications

References 29 publications

Neuron and Sensory Epithelial Cell Fate Is Sequentially Determined by Notch Signaling in Zebrafish Lateral Line Development

Neuron and Sensory Epithelial Cell Fate Is Sequentially Determined by Notch Signaling in Zebrafish Lateral Line Development

Auditory Input to CNS Is Acquired Coincidentally with Development of Inner Ear after Formation of Functional Afferent Pathway in Zebrafish

Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells

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