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Maintenance of cell type-specific connectivity and circuit function requires Tao kinase

Sensory circuits are typically established during early development, yet how circuit specificity and function are maintained during organismal growth has not been elucidated. To gain insight we quantitatively investigated synaptic growth and connectivity in the Drosophila nociceptive network during...

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Autores principales: Tenedini, Federico Marcello, Sáez González, Maria, Hu, Chun, Pedersen, Lisa Hedegaard, Petruzzi, Mabel Matamala, Spitzweck, Bettina, Wang, Denan, Richter, Melanie, Petersen, Meike, Szpotowicz, Emanuela, Schweizer, Michaela, Sigrist, Stephan J., Calderon de Anda, Froylan, Soba, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6683158/
https://www.ncbi.nlm.nih.gov/pubmed/31383864
http://dx.doi.org/10.1038/s41467-019-11408-1
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author Tenedini, Federico Marcello
Sáez González, Maria
Hu, Chun
Pedersen, Lisa Hedegaard
Petruzzi, Mabel Matamala
Spitzweck, Bettina
Wang, Denan
Richter, Melanie
Petersen, Meike
Szpotowicz, Emanuela
Schweizer, Michaela
Sigrist, Stephan J.
Calderon de Anda, Froylan
Soba, Peter
author_facet Tenedini, Federico Marcello
Sáez González, Maria
Hu, Chun
Pedersen, Lisa Hedegaard
Petruzzi, Mabel Matamala
Spitzweck, Bettina
Wang, Denan
Richter, Melanie
Petersen, Meike
Szpotowicz, Emanuela
Schweizer, Michaela
Sigrist, Stephan J.
Calderon de Anda, Froylan
Soba, Peter
author_sort Tenedini, Federico Marcello
collection PubMed
description Sensory circuits are typically established during early development, yet how circuit specificity and function are maintained during organismal growth has not been elucidated. To gain insight we quantitatively investigated synaptic growth and connectivity in the Drosophila nociceptive network during larval development. We show that connectivity between primary nociceptors and their downstream neurons scales with animal size. We further identified the conserved Ste20-like kinase Tao as a negative regulator of synaptic growth required for maintenance of circuit specificity and connectivity. Loss of Tao kinase resulted in exuberant postsynaptic specializations and aberrant connectivity during larval growth. Using functional imaging and behavioral analysis we show that loss of Tao-induced ectopic synapses with inappropriate partner neurons are functional and alter behavioral responses in a connection-specific manner. Our data show that fine-tuning of synaptic growth by Tao kinase is required for maintaining specificity and behavioral output of the neuronal network during animal growth.
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spelling pubmed-66831582019-08-07 Maintenance of cell type-specific connectivity and circuit function requires Tao kinase Tenedini, Federico Marcello Sáez González, Maria Hu, Chun Pedersen, Lisa Hedegaard Petruzzi, Mabel Matamala Spitzweck, Bettina Wang, Denan Richter, Melanie Petersen, Meike Szpotowicz, Emanuela Schweizer, Michaela Sigrist, Stephan J. Calderon de Anda, Froylan Soba, Peter Nat Commun Article Sensory circuits are typically established during early development, yet how circuit specificity and function are maintained during organismal growth has not been elucidated. To gain insight we quantitatively investigated synaptic growth and connectivity in the Drosophila nociceptive network during larval development. We show that connectivity between primary nociceptors and their downstream neurons scales with animal size. We further identified the conserved Ste20-like kinase Tao as a negative regulator of synaptic growth required for maintenance of circuit specificity and connectivity. Loss of Tao kinase resulted in exuberant postsynaptic specializations and aberrant connectivity during larval growth. Using functional imaging and behavioral analysis we show that loss of Tao-induced ectopic synapses with inappropriate partner neurons are functional and alter behavioral responses in a connection-specific manner. Our data show that fine-tuning of synaptic growth by Tao kinase is required for maintaining specificity and behavioral output of the neuronal network during animal growth. Nature Publishing Group UK 2019-08-05 /pmc/articles/PMC6683158/ /pubmed/31383864 http://dx.doi.org/10.1038/s41467-019-11408-1 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Tenedini, Federico Marcello
Sáez González, Maria
Hu, Chun
Pedersen, Lisa Hedegaard
Petruzzi, Mabel Matamala
Spitzweck, Bettina
Wang, Denan
Richter, Melanie
Petersen, Meike
Szpotowicz, Emanuela
Schweizer, Michaela
Sigrist, Stephan J.
Calderon de Anda, Froylan
Soba, Peter
Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title_full Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title_fullStr Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title_full_unstemmed Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title_short Maintenance of cell type-specific connectivity and circuit function requires Tao kinase
title_sort maintenance of cell type-specific connectivity and circuit function requires tao kinase
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6683158/
https://www.ncbi.nlm.nih.gov/pubmed/31383864
http://dx.doi.org/10.1038/s41467-019-11408-1
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