Fold-change detection and scale invariance of cell–cell signaling in social amoeba
Cell–cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively giv...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 21; pp. E4149 - E4157 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
23.05.2017
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| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Cell–cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3′,5′-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change–dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism. |
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| AbstractList | Cell–cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3′,5′-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change–dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism. Recent works have hinted at an ability of cells to respond in the exact same manner to a fold change in the input stimulus. The property is thought to allow cells to function properly regardless of changes in the absolute concentrations of signaling molecules. Despite its general importance, however, evidence has remained scarce. The present work demonstrated that, in the social amoeba Dictyostelium , a response to cell–cell communication molecules is fold-change dependent and that this property is tightly linked to the condition that allows them to oscillate collectively, and thus to organize into a multicellular form. Such properties may be of importance for robustness of other developmental systems where oscillatory signaling plays a pivotal role in defining multicellular organization. Cell–cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3′,5′-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change–dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism. Cell-cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3',5'-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change-dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism.Cell-cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae Dictyostelium discoideum collectively give rise to oscillations and waves of cyclic adenosine 3',5'-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change-dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism. Cell-cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute concentrations of the extracellular signaling molecules. To direct cell aggregation, the social amoebae collectively give rise to oscillations and waves of cyclic adenosine 3',5'-monophosphate (cAMP) under a wide range of cell density. To date, the systems-level mechanism underlying the robustness is unclear. By using quantitative live-cell imaging, here we show that the magnitude of the cAMP relay response of individual cells is determined by fold change in the extracellular cAMP concentrations. The range of cell density and exogenous cAMP concentrations that support oscillations at the population level agrees well with conditions that support a large fold-change-dependent response at the single-cell level. Mathematical analysis suggests that invariance of the oscillations to density transformation is a natural outcome of combining secrete-and-sense systems with a fold-change detection mechanism. |
| Author | Kamino, Keita Kaneko, Kunihiko Kondo, Yohei Honda-Kitahara, Mai Sawai, Satoshi Nakajima, Akihiko |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28495969$$D View this record in MEDLINE/PubMed |
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| Copyright | Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences May 23, 2017 |
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| Keywords | robustness fold-change detection Dictyostelium oscillations collective behavior |
| Language | English |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 ObjectType-Undefined-3 Edited by Peter N. Devreotes, The Johns Hopkins University School of Medicine, Baltimore, MD, and approved April 9, 2017 (received for review February 9, 2017) Author contributions: K. Kamino, Y.K., K. Kaneko, and S.S. designed research; K. Kamino, Y.K., A.N., and S.S. performed research; M.H.-K. and S.S. contributed new reagents; K. Kamino and A.N. acquired and analyzed live cell image data; K. Kamino and Y.K. performed theoretical and computational analysis; and K. Kamino, Y.K., and S.S. wrote the paper. |
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| Snippet | Cell–cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute... Recent works have hinted at an ability of cells to respond in the exact same manner to a fold change in the input stimulus. The property is thought to allow... Cell-cell signaling is subject to variability in the extracellular volume, cell number, and dilution that potentially increase uncertainty in the absolute... |
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| SubjectTerms | Agglomeration Amoeba Biological Sciences Cell aggregation Cell density Cell number Cells Change detection Cyclic AMP Density Dilution Genetic transformation Invariance Mathematical analysis Molecules Oscillations Physical Sciences PNAS Plus Robustness (mathematics) Scale invariance Transformations (mathematics) |
| Title | Fold-change detection and scale invariance of cell–cell signaling in social amoeba |
| URI | https://www.jstor.org/stable/26483325 https://www.ncbi.nlm.nih.gov/pubmed/28495969 https://www.proquest.com/docview/1905687097 https://www.proquest.com/docview/1899111126 https://pubmed.ncbi.nlm.nih.gov/PMC5448168 |
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