Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain

  1. Elizabeth A Williams  Is a corresponding author
  2. Csaba Verasztó
  3. Sanja Jasek
  4. Markus Conzelmann
  5. Réza Shahidi
  6. Philipp Bauknecht
  7. Olivier Mirabeau
  8. Gáspár Jékely  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Institut Curie, France

Abstract

Neurosecretory centers in animal brains use peptidergic signaling to influence physiology and behavior. Understanding neurosecretory center function requires mapping cell types, synapses, and peptidergic networks. Here we use transmission electron microscopy and gene expression mapping to analyze the synaptic and peptidergic connectome of an entire neurosecretory center. We reconstructed 78 neurosecretory neurons and mapped their synaptic connectivity in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory center expressing many neuropeptides, including hypothalamic peptide orthologs and their receptors. Analysis of peptide-receptor pairs in spatially mapped single-cell transcriptome data revealed sparsely connected networks linking specific neuronal subsets. We experimentally analyzed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signaling. Our study uncovered extensive networks of peptidergic signaling within a neurosecretory center and its connection to the synaptic brain.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Elizabeth A Williams

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    elizabeth.williams@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3067-3137
  2. Csaba Verasztó

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6295-7148
  3. Sanja Jasek

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Markus Conzelmann

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Réza Shahidi

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Philipp Bauknecht

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Olivier Mirabeau

    Cancer Genetics Unit, Inserm U830, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Gáspár Jékely

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    G.Jekely@exeter.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8496-9836

Funding

Max-Planck-Gesellschaft (N/A)

  • Elizabeth A Williams
  • Csaba Verasztó
  • Sanja Jasek
  • Markus Conzelmann
  • Philipp Bauknecht

Deutsche Forschungsgemeinschaft (JE 777/1-1)

  • Elizabeth A Williams

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: February 24, 2017
  2. Accepted: December 2, 2017
  3. Accepted Manuscript published: December 4, 2017 (version 1)
  4. Accepted Manuscript updated: December 13, 2017 (version 2)
  5. Version of Record published: December 29, 2017 (version 3)

Copyright

© 2017, Williams et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Elizabeth A Williams
  2. Csaba Verasztó
  3. Sanja Jasek
  4. Markus Conzelmann
  5. Réza Shahidi
  6. Philipp Bauknecht
  7. Olivier Mirabeau
  8. Gáspár Jékely
(2017)
Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain
eLife 6:e26349.
https://doi.org/10.7554/eLife.26349

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