Development of synapses and expression of a voltage-gated potassium channel in chick embryonic auditory nuclei

Feng, Jean; Morest, D. Kent

doi:10.1016/j.heares.2006.01.012

Cited by 14 publications

(14 citation statements)

References 55 publications

(81 reference statements)

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“…However, protein analysis showed that only Kv3.1, Kv3.2 and Kv3.4 subunit proteins were present at this early developmental stage. Previous studies showed that Kv3.1 subunit is expressed at detectable levels before birth in the murine and avian brain (Perney et al 1992;Kuenzel et al 2009;Feng and Morest 2006). However, the expression of Kv3 subunits in the embryonic central nervous system was by is drawn in all cases in which the fitting converged properly large not investigated, and the majority of the studies focused on Kv3 expression in the postnatal period and in single brain regions (Goldberg et al 2011;Liu and Kaczmarek 1998;Goldman-Wohl et al 1994;Prüss et al 2010).…”

Section: Time Course Analysis Of Kv3 Subunit Expression In Mouse Brainmentioning

confidence: 99%

“…Furthermore, the developmental profile of expression has been investigated only for the Kv3.1 (Perney et al 1992;Parameshwaran-Iyer et al 2003;Feng and Morest 2006;Bortone et al 2006;Goldberg et al 2011) and in part for the Kv3.2 subunits (Tansey et al 2002;Goldberg et al 2011). Nothing is known either about the age when the other subunits begin to be expressed or about the time course followed during development.…”

Section: Introductionmentioning

confidence: 99%

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Brain Expression of Kv3 Subunits During Development, Adulthood and Aging and in a Murine Model of Alzheimer’s Disease

et al. 2011

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In neurons, voltage-dependent Kv3 potassium channels are essential for the generation of action potentials at high frequency. A dysregulation of the Kv3.1 and Kv3.4 channel subunits has been suggested to contribute to neuronal and glial alterations in Alzheimer's disease, but a quantitative evaluation of these subunits in a mouse model of the pathology is still lacking. We analysed the profile of expression of the four Kv3 subunits by quantitative reverse transcription PCR and Western blot in the whole mouse brain and in dissected brain regions (olfactory bulb, septum, neocortex, hippocampus, brainstem and cerebellum) from 14 days after conception to 18 months after birth. In addition, we measured the levels of Kv3.1 and Kv3.4 messenger RNAs (mRNAs) and proteins in neocortex and hippocampus of APPPS1 mice, a transgenic model of Alzheimer's disease. Although all Kv3 transcripts were significantly expressed in embryonic age in whole brain extracts, only Kv3.1, Kv3.2 and Kv3.4 subunit proteins were present, suggesting a novel role for Kv3 channels at this developmental stage. With the exception of Kv3.4, during postnatal development, Kv3 transcripts and proteins showed a progressive increase in expression and reached an asymptote in adulthood, suggesting that the increase in Kv3 expression during development might contribute to the maturation of the electrical activity of neurons. During aging, Kv3 expression was rather stable. In contrast, in the neocortex of aged APPPS1 mice, Kv3.1 mRNA and protein levels were significantly lower compared to wild type, suggesting that a decrease in Kv3 currents could play a role in the cognitive symptoms of Alzheimer's disease.

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Section: Time Course Analysis Of Kv3 Subunit Expression In Mouse Brainmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Brain Expression of Kv3 Subunits During Development, Adulthood and Aging and in a Murine Model of Alzheimer’s Disease

et al. 2011

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“…This gradient was barely observed in the chicken, which might be due to the overall smaller frequency range in this bird. Furthermore, in the barn owl, the channel was concentrated in the axons of neurons of the nucleus laminaris and in their presynaptic terminals [Parameshwaran et al, 2001], whereas in the chicken, its axonal expression was restricted to the initial segment [Feng and Morest, 2006]. These data indicate cellular specializations for K v 3.1 in the barn owl and a role of this channel in reducing action potential duration within the terminal region of time encoding neurons.…”

Section: Introductionmentioning

confidence: 83%

“…3). Previous analysis in the chicken had revealed expression both in neurons and astrocytes [Feng and Morest, 2006]. Since neural subtype-specific cell lines are not yet available from the barn owl, we could not address whether neuronal and glial expression of Kcnc1 is also true for the barn owl.…”

Section: Expression Analysis Of Kcnc1mentioning

confidence: 93%

Evolutionary Conservation of Kv3.1 in the Barn Owl Tyto alba

Kullmann

Schlüter²,

Wagner³

et al. 2013

Brain Behav Evol

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For prey capture in the dark, the barn owl Tyto alba has evolved into an auditory specialist with an exquisite capability of sound localization. Adaptations include asymmetrical ears, enlarged auditory processing centers, the utilization of minute interaural time differences, and phase locking along the entire hearing range up to 10 kHz. Adaptations on the molecular level have not yet been investigated. Here, we tested the hypothesis that divergence in the amino acid sequence of the voltage-gated K⁺ channel K_v3.1 contributes to the accuracy and high firing rates of auditory neurons in the barn owl. We therefore cloned both splice variants of Kcnc1, the gene encoding K_v3.1. Both splice variants, Kcnc1a and Kcnc1b, encode amino acids identical to those of the chicken, an auditory generalist. Expression analyses confirmed neural-restricted expression of the channel. In summary, our data reveal strong evolutionary conservation of Kcnc1 in the barn owl and point to other genes involved in auditory specializations of this animal. The data also demonstrate the feasibility to address neuroethological questions in organisms with no reference genome by molecular approaches. This will open new avenues for neuroethologists working in these organisms.

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“…Glial cell bodies are restricted to the margins outside the NL neuropil during embryonic development [27], [28], [29], [30], [31], and GFAP-positive astrocytes extend processes within the dendritic neuropil at the age when dendritic arborization patterns are changing [26]. Several studies have provided evidence to support a role for Bergmann glia in establishing the dendritic arbors of Purkinje cells in the development of the cerebellum [32], [33].…”

Section: Introductionmentioning

confidence: 99%

Astrocyte-Secreted Factors Modulate a Gradient of Primary Dendritic Arbors in Nucleus Laminaris of the Avian Auditory Brainstem

2011

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Neurons in nucleus laminaris (NL) receive binaural, tonotopically matched input from nucleus magnocelluaris (NM) onto bitufted dendrites that display a gradient of dendritic arbor size. These features improve computation of interaural time differences, which are used to determine the locations of sound sources. The dendritic gradient emerges following a period of significant reorganization at embryonic day 15 (E15), which coincides with the emergence of astrocytes that express glial fibrillary acidic protein (GFAP) in the auditory brainstem. The major changes include a loss of total dendritic length, a systematic loss of primary dendrites along the tonotopic axis, and lengthening of primary dendrites on caudolateral NL neurons. Here we have tested whether astrocyte-derived molecules contribute to these changes in dendritic morphology. We used an organotypic brainstem slice preparation to perform repeated imaging of individual dye-filled NL neurons to determine the effects of astrocyte-conditioned medium (ACM) on dendritic morphology. We found that treatment with ACM induced a decrease in the number of primary dendrites in a tonotopically graded manner similar to that observed during normal development. Our data introduce a new interaction between astrocytes and neurons in the auditory brainstem and suggest that these astrocytes influence multiple aspects of auditory brainstem maturation.

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Development of synapses and expression of a voltage-gated potassium channel in chick embryonic auditory nuclei

Cited by 14 publications

References 55 publications

Brain Expression of Kv3 Subunits During Development, Adulthood and Aging and in a Murine Model of Alzheimer’s Disease

Brain Expression of Kv3 Subunits During Development, Adulthood and Aging and in a Murine Model of Alzheimer’s Disease

Evolutionary Conservation of K<sub>v</sub>3.1 in the Barn Owl <b><i>Tyto alba</i></b>

Astrocyte-Secreted Factors Modulate a Gradient of Primary Dendritic Arbors in Nucleus Laminaris of the Avian Auditory Brainstem

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