The Dynamics of Aerotaxis in a Simple Eukaryotic Model

In aerobic organisms, oxygen is essential for efficient energy production, and it acts as the last acceptor of the mitochondrial electron transport chain and as regulator of gene expression. However, excessive oxygen can lead to production of deleterious reactive oxygen species. Therefore, the direc...

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Autores principales:	Marta Biondo, Cristina Panuzzo, Shahzad M. Ali, Salvatore Bozzaro, Matteo Osella, Enrico Bracco, Barbara Pergolizzi
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	aerotaxis oxidative stress hydrogen peroxide collective cell migration Dictyostelium G-protein Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/1da648d9d26742279a7e89b99b0a6359
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spelling	oai:doaj.org-article:1da648d9d26742279a7e89b99b0a63592021-11-30T13:59:14ZThe Dynamics of Aerotaxis in a Simple Eukaryotic Model2296-634X10.3389/fcell.2021.720623https://doaj.org/article/1da648d9d26742279a7e89b99b0a63592021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fcell.2021.720623/fullhttps://doaj.org/toc/2296-634XIn aerobic organisms, oxygen is essential for efficient energy production, and it acts as the last acceptor of the mitochondrial electron transport chain and as regulator of gene expression. However, excessive oxygen can lead to production of deleterious reactive oxygen species. Therefore, the directed migration of single cells or cell clumps from hypoxic areas toward a region of optimal oxygen concentration, named aerotaxis, can be considered an adaptive mechanism that plays a major role in biological and pathological processes. One relevant example is the development of O2 gradients when tumors grow beyond their vascular supply, leading frequently to metastasis. In higher eukaryotic organisms, aerotaxis has only recently begun to be explored, but genetically amenable model organisms suitable to dissect this process remain an unmet need. In this regard, we sought to assess whether Dictyostelium cells, which are an established model for chemotaxis and other motility processes, could sense oxygen gradients and move directionally in their response. By assessing different physical parameters, our findings indicate that both growing and starving Dictyostelium cells under hypoxic conditions migrate directionally toward regions of higher O2 concentration. This migration is characterized by a specific pattern of cell arrangement. A thickened circular front of high cell density (corona) forms in the cell cluster and persistently moves following the oxygen gradient. Cells in the colony center, where hypoxia is more severe, are less motile and display a rounded shape. Aggregation-competent cells forming streams by chemotaxis, when confined under hypoxic conditions, undergo stream or aggregate fragmentation, giving rise to multiple small loose aggregates that coordinately move toward regions of higher O2 concentration. By testing a panel of mutants defective in chemotactic signaling, and a catalase-deficient strain, we found that the latter and the pkbR1null exhibited altered migration patterns. Our results suggest that in Dictyostelium, like in mammalian cells, an intracellular accumulation of hydrogen peroxide favors the migration toward optimal oxygen concentration. Furthermore, differently from chemotaxis, this oxygen-driven migration is a G protein-independent process.Marta BiondoCristina PanuzzoShahzad M. AliSalvatore BozzaroMatteo OsellaEnrico BraccoBarbara PergolizziFrontiers Media S.A.articleaerotaxisoxidative stresshydrogen peroxidecollective cell migrationDictyosteliumG-proteinBiology (General)QH301-705.5ENFrontiers in Cell and Developmental Biology, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	aerotaxis oxidative stress hydrogen peroxide collective cell migration Dictyostelium G-protein Biology (General) QH301-705.5
spellingShingle	aerotaxis oxidative stress hydrogen peroxide collective cell migration Dictyostelium G-protein Biology (General) QH301-705.5 Marta Biondo Cristina Panuzzo Shahzad M. Ali Salvatore Bozzaro Matteo Osella Enrico Bracco Barbara Pergolizzi The Dynamics of Aerotaxis in a Simple Eukaryotic Model
description	In aerobic organisms, oxygen is essential for efficient energy production, and it acts as the last acceptor of the mitochondrial electron transport chain and as regulator of gene expression. However, excessive oxygen can lead to production of deleterious reactive oxygen species. Therefore, the directed migration of single cells or cell clumps from hypoxic areas toward a region of optimal oxygen concentration, named aerotaxis, can be considered an adaptive mechanism that plays a major role in biological and pathological processes. One relevant example is the development of O2 gradients when tumors grow beyond their vascular supply, leading frequently to metastasis. In higher eukaryotic organisms, aerotaxis has only recently begun to be explored, but genetically amenable model organisms suitable to dissect this process remain an unmet need. In this regard, we sought to assess whether Dictyostelium cells, which are an established model for chemotaxis and other motility processes, could sense oxygen gradients and move directionally in their response. By assessing different physical parameters, our findings indicate that both growing and starving Dictyostelium cells under hypoxic conditions migrate directionally toward regions of higher O2 concentration. This migration is characterized by a specific pattern of cell arrangement. A thickened circular front of high cell density (corona) forms in the cell cluster and persistently moves following the oxygen gradient. Cells in the colony center, where hypoxia is more severe, are less motile and display a rounded shape. Aggregation-competent cells forming streams by chemotaxis, when confined under hypoxic conditions, undergo stream or aggregate fragmentation, giving rise to multiple small loose aggregates that coordinately move toward regions of higher O2 concentration. By testing a panel of mutants defective in chemotactic signaling, and a catalase-deficient strain, we found that the latter and the pkbR1null exhibited altered migration patterns. Our results suggest that in Dictyostelium, like in mammalian cells, an intracellular accumulation of hydrogen peroxide favors the migration toward optimal oxygen concentration. Furthermore, differently from chemotaxis, this oxygen-driven migration is a G protein-independent process.
format	article
author	Marta Biondo Cristina Panuzzo Shahzad M. Ali Salvatore Bozzaro Matteo Osella Enrico Bracco Barbara Pergolizzi
author_facet	Marta Biondo Cristina Panuzzo Shahzad M. Ali Salvatore Bozzaro Matteo Osella Enrico Bracco Barbara Pergolizzi
author_sort	Marta Biondo
title	The Dynamics of Aerotaxis in a Simple Eukaryotic Model
title_short	The Dynamics of Aerotaxis in a Simple Eukaryotic Model
title_full	The Dynamics of Aerotaxis in a Simple Eukaryotic Model
title_fullStr	The Dynamics of Aerotaxis in a Simple Eukaryotic Model
title_full_unstemmed	The Dynamics of Aerotaxis in a Simple Eukaryotic Model
title_sort	dynamics of aerotaxis in a simple eukaryotic model
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/1da648d9d26742279a7e89b99b0a6359
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The Dynamics of Aerotaxis in a Simple Eukaryotic Model

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