Mapping developmental maturation of inner hair cell ribbon synapses in the apical mouse cochlea.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
26 03 2019
Historique:
pubmed: 15 3 2019
medline: 21 5 2019
entrez: 15 3 2019
Statut: ppublish

Résumé

Ribbon synapses of cochlear inner hair cells (IHCs) undergo molecular assembly and extensive functional and structural maturation before hearing onset. Here, we characterized the nanostructure of IHC synapses from late prenatal mouse embryo stages (embryonic days 14-18) into adulthood [postnatal day (P)48] using electron microscopy and tomography as well as optical nanoscopy of apical turn organs of Corti. We find that synaptic ribbon precursors arrive at presynaptic active zones (AZs) after afferent contacts have been established. These ribbon precursors contain the proteins RIBEYE and piccolino, tether synaptic vesicles and their delivery likely involves active, microtubule-based transport pathways. Synaptic contacts undergo a maturational transformation from multiple small to one single, large AZ. This maturation is characterized by the fusion of ribbon precursors with membrane-anchored ribbons that also appear to fuse with each other. Such fusion events are most frequently encountered around P12 and hence, coincide with hearing onset in mice. Thus, these events likely underlie the morphological and functional maturation of the AZ. Moreover, the postsynaptic densities appear to undergo a similar refinement alongside presynaptic maturation. Blockwise addition of ribbon material by fusion as found during AZ maturation might represent a general mechanism for modulating ribbon size.

Identifiants

pubmed: 30867284
pii: 1812029116
doi: 10.1073/pnas.1812029116
pmc: PMC6442603
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6415-6424

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

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Auteurs

Susann Michanski (S)

Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, InnerEarLab and Center for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, 37075 Göttingen, Germany.
Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.

Katharina Smaluch (K)

Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.
Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Presynaptogenesis and Intracellular Transport in Hair Cells Junior Research Group, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.

Anna Maria Steyer (AM)

Electron Microscopy Core Unit, Department of Neurogenetics, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.
Center Nanoscale Microscopy and Molecular Physiology of the Brain, University of Göttingen, 37075 Göttingen, Germany.

Rituparna Chakrabarti (R)

Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, InnerEarLab and Center for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, 37075 Göttingen, Germany.
Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.

Cristian Setz (C)

Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.
Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Presynaptogenesis and Intracellular Transport in Hair Cells Junior Research Group, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Department of Otolaryngology, Head and Neck Surgery, University Medical Center Göttingen, 37075 Göttingen, Germany.
Auditory Neuroscience Group, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.

David Oestreicher (D)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Presynaptogenesis and Intracellular Transport in Hair Cells Junior Research Group, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Department of Otolaryngology, Head and Neck Surgery, University Medical Center Göttingen, 37075 Göttingen, Germany.

Christian Fischer (C)

Johann Friedrich Blumenbach Institute for Zoology and Anthropology, Department of Animal Evolution and Biodiversity, Georg August University of Göttingen, 37073 Göttingen, Germany.

Wiebke Möbius (W)

Electron Microscopy Core Unit, Department of Neurogenetics, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.
Center Nanoscale Microscopy and Molecular Physiology of the Brain, University of Göttingen, 37075 Göttingen, Germany.

Tobias Moser (T)

Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.
Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Center Nanoscale Microscopy and Molecular Physiology of the Brain, University of Göttingen, 37075 Göttingen, Germany.
Auditory Neuroscience Group, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.
Synaptic Nanophysiology Group, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany.

Christian Vogl (C)

Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany; christian.vogl@med.uni-goettingen.de carolin.wichmann@med.uni-goettingen.de.
Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Presynaptogenesis and Intracellular Transport in Hair Cells Junior Research Group, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, 37075 Göttingen, Germany.
Auditory Neuroscience Group, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.

Carolin Wichmann (C)

Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, InnerEarLab and Center for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, 37075 Göttingen, Germany; christian.vogl@med.uni-goettingen.de carolin.wichmann@med.uni-goettingen.de.
Collaborative Research Center 889, University of Göttingen, 37075 Göttingen, Germany.
Auditory Neuroscience Group, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany.

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