Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability

Detection of chemical stimuli is crucial for living systems and also contributes to quality of life in humans. Since loss of olfaction becomes more prevalent with aging, longer life expectancies have fueled interest in understanding the molecular mechanisms behind the development and maintenance of...

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Autores principales:	Eugene Matthew P. Almazan, Joseph F. Ryan, Labib Rouhana
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	planarian Girardia dorotocephala regeneration stem cells neoblast chemotaxis Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/c23a70a7377a4916b9967247b00e80d9
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spelling	oai:doaj.org-article:c23a70a7377a4916b9967247b00e80d92021-12-01T07:36:15ZRegeneration of Planarian Auricles and Reestablishment of Chemotactic Ability2296-634X10.3389/fcell.2021.777951https://doaj.org/article/c23a70a7377a4916b9967247b00e80d92021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fcell.2021.777951/fullhttps://doaj.org/toc/2296-634XDetection of chemical stimuli is crucial for living systems and also contributes to quality of life in humans. Since loss of olfaction becomes more prevalent with aging, longer life expectancies have fueled interest in understanding the molecular mechanisms behind the development and maintenance of chemical sensing. Planarian flatworms possess an unsurpassed ability for stem cell-driven regeneration that allows them to restore any damaged or removed part of their bodies. This includes anteriorly-positioned lateral flaps known as auricles, which have long been thought to play a central role in chemotaxis. The contribution of auricles to the detection of positive chemical stimuli was tested in this study using Girardia dorotocephala, a North American planarian species known for its morphologically prominent auricles. Behavioral experiments staged under laboratory conditions revealed that removal of auricles by amputation leads to a significant decrease in the ability of planarians to find food. However, full chemotactic capacity is observed as early as 2 days post-amputation, which is days prior from restoration of auricle morphology, but correlative with accumulation of ciliated cells in the position of auricle regeneration. Planarians subjected to x-ray irradiation prior to auricle amputation were unable to restore auricle morphology, but were still able to restore chemotactic capacity. These results indicate that although regeneration of auricle morphology requires stem cells, some restoration of chemotactic ability can still be achieved in the absence of normal auricle morphology, corroborating with the initial observation that chemotactic success is reestablished 2-days post-amputation in our assays. Transcriptome profiles of excised auricles were obtained to facilitate molecular characterization of these structures, as well as the identification of genes that contribute to chemotaxis and auricle development. A significant overlap was found between genes with preferential expression in auricles of G. dorotocephala and genes with reduced expression upon SoxB1 knockdown in Schmidtea mediterranea, suggesting that SoxB1 has a conserved role in regulating auricle development and function. Models that distinguish between possible contributions to chemotactic behavior obtained from cellular composition, as compared to anatomical morphology of the auricles, are discussed.Eugene Matthew P. AlmazanJoseph F. RyanJoseph F. RyanLabib RouhanaFrontiers Media S.A.articleplanarianGirardia dorotocephalaregenerationstem cellsneoblastchemotaxisBiology (General)QH301-705.5ENFrontiers in Cell and Developmental Biology, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	planarian Girardia dorotocephala regeneration stem cells neoblast chemotaxis Biology (General) QH301-705.5
spellingShingle	planarian Girardia dorotocephala regeneration stem cells neoblast chemotaxis Biology (General) QH301-705.5 Eugene Matthew P. Almazan Joseph F. Ryan Joseph F. Ryan Labib Rouhana Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
description	Detection of chemical stimuli is crucial for living systems and also contributes to quality of life in humans. Since loss of olfaction becomes more prevalent with aging, longer life expectancies have fueled interest in understanding the molecular mechanisms behind the development and maintenance of chemical sensing. Planarian flatworms possess an unsurpassed ability for stem cell-driven regeneration that allows them to restore any damaged or removed part of their bodies. This includes anteriorly-positioned lateral flaps known as auricles, which have long been thought to play a central role in chemotaxis. The contribution of auricles to the detection of positive chemical stimuli was tested in this study using Girardia dorotocephala, a North American planarian species known for its morphologically prominent auricles. Behavioral experiments staged under laboratory conditions revealed that removal of auricles by amputation leads to a significant decrease in the ability of planarians to find food. However, full chemotactic capacity is observed as early as 2 days post-amputation, which is days prior from restoration of auricle morphology, but correlative with accumulation of ciliated cells in the position of auricle regeneration. Planarians subjected to x-ray irradiation prior to auricle amputation were unable to restore auricle morphology, but were still able to restore chemotactic capacity. These results indicate that although regeneration of auricle morphology requires stem cells, some restoration of chemotactic ability can still be achieved in the absence of normal auricle morphology, corroborating with the initial observation that chemotactic success is reestablished 2-days post-amputation in our assays. Transcriptome profiles of excised auricles were obtained to facilitate molecular characterization of these structures, as well as the identification of genes that contribute to chemotaxis and auricle development. A significant overlap was found between genes with preferential expression in auricles of G. dorotocephala and genes with reduced expression upon SoxB1 knockdown in Schmidtea mediterranea, suggesting that SoxB1 has a conserved role in regulating auricle development and function. Models that distinguish between possible contributions to chemotactic behavior obtained from cellular composition, as compared to anatomical morphology of the auricles, are discussed.
format	article
author	Eugene Matthew P. Almazan Joseph F. Ryan Joseph F. Ryan Labib Rouhana
author_facet	Eugene Matthew P. Almazan Joseph F. Ryan Joseph F. Ryan Labib Rouhana
author_sort	Eugene Matthew P. Almazan
title	Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
title_short	Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
title_full	Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
title_fullStr	Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
title_full_unstemmed	Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability
title_sort	regeneration of planarian auricles and reestablishment of chemotactic ability
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/c23a70a7377a4916b9967247b00e80d9
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_version_	1718405439430852608

Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability

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