The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.

The assembly of neuronal circuits involves the migrations of neurons from their place of birth to their final location in the nervous system, as well as the coordinated growth and patterning of axons and dendrites. In screens for genes required for patterning of the nervous system, we identified the...

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Autores principales:	Leo T H Tang, Meera Trivedi, Jenna Freund, Christopher J Salazar, Maisha Rahman, Nelson J Ramirez-Suarez, Garrett Lee, Yu Wang, Barth D Grant, Hannes E Bülow
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/540ad2045ac0405191519c82dd7f4017
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spelling	oai:doaj.org-article:540ad2045ac0405191519c82dd7f40172021-12-02T20:03:04ZThe CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.1553-73901553-740410.1371/journal.pgen.1009475https://doaj.org/article/540ad2045ac0405191519c82dd7f40172021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009475https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404The assembly of neuronal circuits involves the migrations of neurons from their place of birth to their final location in the nervous system, as well as the coordinated growth and patterning of axons and dendrites. In screens for genes required for patterning of the nervous system, we identified the catp-8/P5A-ATPase as an important regulator of neural patterning. P5A-ATPases are part of the P-type ATPases, a family of proteins known to serve a conserved function as transporters of ions, lipids and polyamines in unicellular eukaryotes, plants, and humans. While the function of many P-type ATPases is relatively well understood, the function of P5A-ATPases in metazoans remained elusive. We show here, that the Caenorhabditis elegans ortholog catp-8/P5A-ATPase is required for defined aspects of nervous system development. Specifically, the catp-8/P5A-ATPase serves functions in shaping the elaborately sculpted dendritic trees of somatosensory PVD neurons. Moreover, catp-8/P5A-ATPase is required for axonal guidance and repulsion at the midline, as well as embryonic and postembryonic neuronal migrations. Interestingly, not all axons at the midline require catp-8/P5A-ATPase, although the axons run in the same fascicles and navigate the same space. Similarly, not all neuronal migrations require catp-8/P5A-ATPase. A CATP-8/P5A-ATPase reporter is localized to the ER in most, if not all, tissues and catp-8/P5A-ATPase can function both cell-autonomously and non-autonomously to regulate neuronal development. Genetic analyses establish that catp-8/P5A-ATPase can function in multiple pathways, including the Menorin pathway, previously shown to control dendritic patterning in PVD, and Wnt signaling, which functions to control neuronal migrations. Lastly, we show that catp-8/P5A-ATPase is required for localizing select transmembrane proteins necessary for dendrite morphogenesis. Collectively, our studies suggest that catp-8/P5A-ATPase serves diverse, yet specific, roles in different genetic pathways and may be involved in the regulation or localization of transmembrane and secreted proteins to specific subcellular compartments.Leo T H TangMeera TrivediJenna FreundChristopher J SalazarMaisha RahmanNelson J Ramirez-SuarezGarrett LeeYu WangBarth D GrantHannes E BülowPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009475 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Leo T H Tang Meera Trivedi Jenna Freund Christopher J Salazar Maisha Rahman Nelson J Ramirez-Suarez Garrett Lee Yu Wang Barth D Grant Hannes E Bülow The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
description	The assembly of neuronal circuits involves the migrations of neurons from their place of birth to their final location in the nervous system, as well as the coordinated growth and patterning of axons and dendrites. In screens for genes required for patterning of the nervous system, we identified the catp-8/P5A-ATPase as an important regulator of neural patterning. P5A-ATPases are part of the P-type ATPases, a family of proteins known to serve a conserved function as transporters of ions, lipids and polyamines in unicellular eukaryotes, plants, and humans. While the function of many P-type ATPases is relatively well understood, the function of P5A-ATPases in metazoans remained elusive. We show here, that the Caenorhabditis elegans ortholog catp-8/P5A-ATPase is required for defined aspects of nervous system development. Specifically, the catp-8/P5A-ATPase serves functions in shaping the elaborately sculpted dendritic trees of somatosensory PVD neurons. Moreover, catp-8/P5A-ATPase is required for axonal guidance and repulsion at the midline, as well as embryonic and postembryonic neuronal migrations. Interestingly, not all axons at the midline require catp-8/P5A-ATPase, although the axons run in the same fascicles and navigate the same space. Similarly, not all neuronal migrations require catp-8/P5A-ATPase. A CATP-8/P5A-ATPase reporter is localized to the ER in most, if not all, tissues and catp-8/P5A-ATPase can function both cell-autonomously and non-autonomously to regulate neuronal development. Genetic analyses establish that catp-8/P5A-ATPase can function in multiple pathways, including the Menorin pathway, previously shown to control dendritic patterning in PVD, and Wnt signaling, which functions to control neuronal migrations. Lastly, we show that catp-8/P5A-ATPase is required for localizing select transmembrane proteins necessary for dendrite morphogenesis. Collectively, our studies suggest that catp-8/P5A-ATPase serves diverse, yet specific, roles in different genetic pathways and may be involved in the regulation or localization of transmembrane and secreted proteins to specific subcellular compartments.
format	article
author	Leo T H Tang Meera Trivedi Jenna Freund Christopher J Salazar Maisha Rahman Nelson J Ramirez-Suarez Garrett Lee Yu Wang Barth D Grant Hannes E Bülow
author_facet	Leo T H Tang Meera Trivedi Jenna Freund Christopher J Salazar Maisha Rahman Nelson J Ramirez-Suarez Garrett Lee Yu Wang Barth D Grant Hannes E Bülow
author_sort	Leo T H Tang
title	The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
title_short	The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
title_full	The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
title_fullStr	The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
title_full_unstemmed	The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.
title_sort	catp-8/p5a-type atpase functions in multiple pathways during neuronal patterning.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/540ad2045ac0405191519c82dd7f4017
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The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning.

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