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Choanoflagellates and the ancestry of neurosecretory vesicles

Neurosecretory vesicles are highly specialized trafficking organelles that store neurotransmitters that are released at presynaptic nerve endings and are, therefore, important for animal cell–cell signalling. Despite considerable anatomical and functional diversity of neurons in animals, the protein...

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Autores principales: Göhde, Ronja, Naumann, Benjamin, Laundon, Davis, Imig, Cordelia, McDonald, Kent, Cooper, Benjamin H., Varoqueaux, Frédérique, Fasshauer, Dirk, Burkhardt, Pawel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934909/
https://www.ncbi.nlm.nih.gov/pubmed/33550951
http://dx.doi.org/10.1098/rstb.2019.0759
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author Göhde, Ronja
Naumann, Benjamin
Laundon, Davis
Imig, Cordelia
McDonald, Kent
Cooper, Benjamin H.
Varoqueaux, Frédérique
Fasshauer, Dirk
Burkhardt, Pawel
author_facet Göhde, Ronja
Naumann, Benjamin
Laundon, Davis
Imig, Cordelia
McDonald, Kent
Cooper, Benjamin H.
Varoqueaux, Frédérique
Fasshauer, Dirk
Burkhardt, Pawel
author_sort Göhde, Ronja
collection PubMed
description Neurosecretory vesicles are highly specialized trafficking organelles that store neurotransmitters that are released at presynaptic nerve endings and are, therefore, important for animal cell–cell signalling. Despite considerable anatomical and functional diversity of neurons in animals, the protein composition of neurosecretory vesicles in bilaterians appears to be similar. This similarity points towards a common evolutionary origin. Moreover, many putative homologues of key neurosecretory vesicle proteins predate the origin of the first neurons, and some even the origin of the first animals. However, little is known about the molecular toolkit of these vesicles in non-bilaterian animals and their closest unicellular relatives, making inferences about the evolutionary origin of neurosecretory vesicles extremely difficult. By comparing 28 proteins of the core neurosecretory vesicle proteome in 13 different species, we demonstrate that most of the proteins are present in unicellular organisms. Surprisingly, we find that the vesicular membrane-associated soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein synaptobrevin is localized to the vesicle-rich apical and basal pole in the choanoflagellate Salpingoeca rosetta. Our 3D vesicle reconstructions reveal that the choanoflagellates S. rosetta and Monosiga brevicollis exhibit a polarized and diverse vesicular landscape reminiscent of the polarized organization of chemical synapses that secrete the content of neurosecretory vesicles into the synaptic cleft. This study sheds light on the ancestral molecular machinery of neurosecretory vesicles and provides a framework to understand the origin and evolution of secretory cells, synapses and neurons. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.
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spelling pubmed-79349092021-03-24 Choanoflagellates and the ancestry of neurosecretory vesicles Göhde, Ronja Naumann, Benjamin Laundon, Davis Imig, Cordelia McDonald, Kent Cooper, Benjamin H. Varoqueaux, Frédérique Fasshauer, Dirk Burkhardt, Pawel Philos Trans R Soc Lond B Biol Sci Part II: The Transition to Nervous Systems Neurosecretory vesicles are highly specialized trafficking organelles that store neurotransmitters that are released at presynaptic nerve endings and are, therefore, important for animal cell–cell signalling. Despite considerable anatomical and functional diversity of neurons in animals, the protein composition of neurosecretory vesicles in bilaterians appears to be similar. This similarity points towards a common evolutionary origin. Moreover, many putative homologues of key neurosecretory vesicle proteins predate the origin of the first neurons, and some even the origin of the first animals. However, little is known about the molecular toolkit of these vesicles in non-bilaterian animals and their closest unicellular relatives, making inferences about the evolutionary origin of neurosecretory vesicles extremely difficult. By comparing 28 proteins of the core neurosecretory vesicle proteome in 13 different species, we demonstrate that most of the proteins are present in unicellular organisms. Surprisingly, we find that the vesicular membrane-associated soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein synaptobrevin is localized to the vesicle-rich apical and basal pole in the choanoflagellate Salpingoeca rosetta. Our 3D vesicle reconstructions reveal that the choanoflagellates S. rosetta and Monosiga brevicollis exhibit a polarized and diverse vesicular landscape reminiscent of the polarized organization of chemical synapses that secrete the content of neurosecretory vesicles into the synaptic cleft. This study sheds light on the ancestral molecular machinery of neurosecretory vesicles and provides a framework to understand the origin and evolution of secretory cells, synapses and neurons. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’. The Royal Society 2021-03-29 2021-02-08 /pmc/articles/PMC7934909/ /pubmed/33550951 http://dx.doi.org/10.1098/rstb.2019.0759 Text en © 2021 The Authors. http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/http://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Part II: The Transition to Nervous Systems
Göhde, Ronja
Naumann, Benjamin
Laundon, Davis
Imig, Cordelia
McDonald, Kent
Cooper, Benjamin H.
Varoqueaux, Frédérique
Fasshauer, Dirk
Burkhardt, Pawel
Choanoflagellates and the ancestry of neurosecretory vesicles
title Choanoflagellates and the ancestry of neurosecretory vesicles
title_full Choanoflagellates and the ancestry of neurosecretory vesicles
title_fullStr Choanoflagellates and the ancestry of neurosecretory vesicles
title_full_unstemmed Choanoflagellates and the ancestry of neurosecretory vesicles
title_short Choanoflagellates and the ancestry of neurosecretory vesicles
title_sort choanoflagellates and the ancestry of neurosecretory vesicles
topic Part II: The Transition to Nervous Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934909/
https://www.ncbi.nlm.nih.gov/pubmed/33550951
http://dx.doi.org/10.1098/rstb.2019.0759
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