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Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis

BACKGROUND: In the early stages of development of the cellular slime mold Dictyostelium discoideum, chemotaxis toward cAMP plays a pivotal role in organizing discrete cells into a multicellular structure. In this process, a series of signaling molecules, such as G-protein-coupled cell surface recept...

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Autores principales: Kuwayama, Hidekazu, Kubohara, Yuzuru
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2722026/
https://www.ncbi.nlm.nih.gov/pubmed/19684855
http://dx.doi.org/10.1371/journal.pone.0006658
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author Kuwayama, Hidekazu
Kubohara, Yuzuru
author_facet Kuwayama, Hidekazu
Kubohara, Yuzuru
author_sort Kuwayama, Hidekazu
collection PubMed
description BACKGROUND: In the early stages of development of the cellular slime mold Dictyostelium discoideum, chemotaxis toward cAMP plays a pivotal role in organizing discrete cells into a multicellular structure. In this process, a series of signaling molecules, such as G-protein-coupled cell surface receptors for cAMP, phosphatidylinositol metabolites, and cyclic nucleotides, function as the signal transducers for controlling dynamics of cytoskeleton. Differentiation-inducing factor-1 and -2 (DIF-1 and DIF-2) were originally identified as the factors (chlorinated alkylphenones) that induce Dictyostelium stalk cell differentiation, but it remained unknown whether the DIFs had any other physiologic functions. METHODOLOGY/PRINCIPAL FINDINGS: To further elucidate the functions of DIFs, in the present study we investigated their effects on chemotaxis under various conditions. Quite interestingly, in shallow cAMP gradients, DIF-1 suppressed chemotaxis whereas DIF-2 promoted it greatly. Analyses with various mutants revealed that DIF-1 may inhibit chemotaxis, at least in part, via GbpB (a phosphodiesterase) and a decrease in the intracellular cGMP concentration ([cGMP](i)). DIF-2, by contrast, may enhance chemotaxis, at least in part, via RegA (another phosphodiesterase) and an increase in [cGMP](i). Using null mutants for DimA and DimB, the transcription factors that are required for DIF-dependent prestalk differentiation, we also showed that the mechanisms for the modulation of chemotaxis by DIFs differ from those for the induction of cell differentiation by DIFs, at least in part. CONCLUSIONS/SIGNIFICANCE: Our findings indicate that DIF-1 and DIF-2 function as negative and positive modulators for Dictyostelium chemotaxis, respectively. To our knowledge, this is the first report in any organism of physiologic modulators (small molecules) for chemotaxis having differentiation-inducing activity.
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spelling pubmed-27220262009-08-17 Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis Kuwayama, Hidekazu Kubohara, Yuzuru PLoS One Research Article BACKGROUND: In the early stages of development of the cellular slime mold Dictyostelium discoideum, chemotaxis toward cAMP plays a pivotal role in organizing discrete cells into a multicellular structure. In this process, a series of signaling molecules, such as G-protein-coupled cell surface receptors for cAMP, phosphatidylinositol metabolites, and cyclic nucleotides, function as the signal transducers for controlling dynamics of cytoskeleton. Differentiation-inducing factor-1 and -2 (DIF-1 and DIF-2) were originally identified as the factors (chlorinated alkylphenones) that induce Dictyostelium stalk cell differentiation, but it remained unknown whether the DIFs had any other physiologic functions. METHODOLOGY/PRINCIPAL FINDINGS: To further elucidate the functions of DIFs, in the present study we investigated their effects on chemotaxis under various conditions. Quite interestingly, in shallow cAMP gradients, DIF-1 suppressed chemotaxis whereas DIF-2 promoted it greatly. Analyses with various mutants revealed that DIF-1 may inhibit chemotaxis, at least in part, via GbpB (a phosphodiesterase) and a decrease in the intracellular cGMP concentration ([cGMP](i)). DIF-2, by contrast, may enhance chemotaxis, at least in part, via RegA (another phosphodiesterase) and an increase in [cGMP](i). Using null mutants for DimA and DimB, the transcription factors that are required for DIF-dependent prestalk differentiation, we also showed that the mechanisms for the modulation of chemotaxis by DIFs differ from those for the induction of cell differentiation by DIFs, at least in part. CONCLUSIONS/SIGNIFICANCE: Our findings indicate that DIF-1 and DIF-2 function as negative and positive modulators for Dictyostelium chemotaxis, respectively. To our knowledge, this is the first report in any organism of physiologic modulators (small molecules) for chemotaxis having differentiation-inducing activity. Public Library of Science 2009-08-17 /pmc/articles/PMC2722026/ /pubmed/19684855 http://dx.doi.org/10.1371/journal.pone.0006658 Text en Kuwayama, Kubohara. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kuwayama, Hidekazu
Kubohara, Yuzuru
Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title_full Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title_fullStr Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title_full_unstemmed Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title_short Differentiation-Inducing Factor-1 and -2 Function also as Modulators for Dictyostelium Chemotaxis
title_sort differentiation-inducing factor-1 and -2 function also as modulators for dictyostelium chemotaxis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2722026/
https://www.ncbi.nlm.nih.gov/pubmed/19684855
http://dx.doi.org/10.1371/journal.pone.0006658
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