Visualizing the metazoan proliferation-quiescence decision in vivo

Cell proliferation and quiescence are intimately coordinated during metazoan development. Here, we adapt a cyclin-dependent kinase (CDK) sensor to uncouple these key events of the cell cycle in Caenorhabditis elegans and zebrafish through live-cell imaging. The CDK sensor consists of a fluorescently...

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Main Authors: Rebecca C Adikes, Abraham Q Kohrman, Michael A Q Martinez, Nicholas J Palmisano, Jayson J Smith, Taylor N Medwig-Kinney, Mingwei Min, Maria D Sallee, Ononnah B Ahmed, Nuri Kim, Simeiyun Liu, Robert D Morabito, Nicholas Weeks, Qinyun Zhao, Wan Zhang, Jessica L Feldman, Michalis Barkoulas, Ariel M Pani, Sabrina L Spencer, Benjamin L Martin, David Q Matus
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/63265
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spelling doaj-ef13a2875ea8461db4c27f46e2101a882021-05-05T21:53:13ZengeLife Sciences Publications LtdeLife2050-084X2020-12-01910.7554/eLife.63265Visualizing the metazoan proliferation-quiescence decision in vivoRebecca C Adikes0https://orcid.org/0000-0002-7526-8701Abraham Q Kohrman1https://orcid.org/0000-0002-3726-1090Michael A Q Martinez2https://orcid.org/0000-0003-1178-7139Nicholas J Palmisano3https://orcid.org/0000-0002-7992-4462Jayson J Smith4https://orcid.org/0000-0001-8525-7873Taylor N Medwig-Kinney5https://orcid.org/0000-0001-7989-3291Mingwei Min6https://orcid.org/0000-0002-9050-5330Maria D Sallee7Ononnah B Ahmed8Nuri Kim9Simeiyun Liu10Robert D Morabito11Nicholas Weeks12Qinyun Zhao13Wan Zhang14Jessica L Feldman15https://orcid.org/0000-0002-5210-5045Michalis Barkoulas16https://orcid.org/0000-0003-1974-7668Ariel M Pani17Sabrina L Spencer18https://orcid.org/0000-0002-5798-3007Benjamin L Martin19https://orcid.org/0000-0001-5474-4492David Q Matus20https://orcid.org/0000-0002-1570-5025Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and BioFrontiers Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Biology, Stanford University, Stanford, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biology, Stanford University, Stanford, United StatesDepartment of Life Sciences, Imperial College, London, United KingdomDepartment of Biology, University of Virginia, Charlottesville, United StatesDepartment of Biochemistry and BioFrontiers Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesDepartment of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, United StatesCell proliferation and quiescence are intimately coordinated during metazoan development. Here, we adapt a cyclin-dependent kinase (CDK) sensor to uncouple these key events of the cell cycle in Caenorhabditis elegans and zebrafish through live-cell imaging. The CDK sensor consists of a fluorescently tagged CDK substrate that steadily translocates from the nucleus to the cytoplasm in response to increasing CDK activity and consequent sensor phosphorylation. We show that the CDK sensor can distinguish cycling cells in G1 from quiescent cells in G0, revealing a possible commitment point and a cryptic stochasticity in an otherwise invariant C. elegans cell lineage. Finally, we derive a predictive model of future proliferation behavior in C. elegans based on a snapshot of CDK activity in newly born cells. Thus, we introduce a live-cell imaging tool to facilitate in vivo studies of cell-cycle control in a wide-range of developmental contexts.https://elifesciences.org/articles/63265cell cyclequiescencecell proliferationG1/G0CDK sensor
collection DOAJ
language English
format Article
sources DOAJ
author Rebecca C Adikes
Abraham Q Kohrman
Michael A Q Martinez
Nicholas J Palmisano
Jayson J Smith
Taylor N Medwig-Kinney
Mingwei Min
Maria D Sallee
Ononnah B Ahmed
Nuri Kim
Simeiyun Liu
Robert D Morabito
Nicholas Weeks
Qinyun Zhao
Wan Zhang
Jessica L Feldman
Michalis Barkoulas
Ariel M Pani
Sabrina L Spencer
Benjamin L Martin
David Q Matus
spellingShingle Rebecca C Adikes
Abraham Q Kohrman
Michael A Q Martinez
Nicholas J Palmisano
Jayson J Smith
Taylor N Medwig-Kinney
Mingwei Min
Maria D Sallee
Ononnah B Ahmed
Nuri Kim
Simeiyun Liu
Robert D Morabito
Nicholas Weeks
Qinyun Zhao
Wan Zhang
Jessica L Feldman
Michalis Barkoulas
Ariel M Pani
Sabrina L Spencer
Benjamin L Martin
David Q Matus
Visualizing the metazoan proliferation-quiescence decision in vivo
eLife
cell cycle
quiescence
cell proliferation
G1/G0
CDK sensor
author_facet Rebecca C Adikes
Abraham Q Kohrman
Michael A Q Martinez
Nicholas J Palmisano
Jayson J Smith
Taylor N Medwig-Kinney
Mingwei Min
Maria D Sallee
Ononnah B Ahmed
Nuri Kim
Simeiyun Liu
Robert D Morabito
Nicholas Weeks
Qinyun Zhao
Wan Zhang
Jessica L Feldman
Michalis Barkoulas
Ariel M Pani
Sabrina L Spencer
Benjamin L Martin
David Q Matus
author_sort Rebecca C Adikes
title Visualizing the metazoan proliferation-quiescence decision in vivo
title_short Visualizing the metazoan proliferation-quiescence decision in vivo
title_full Visualizing the metazoan proliferation-quiescence decision in vivo
title_fullStr Visualizing the metazoan proliferation-quiescence decision in vivo
title_full_unstemmed Visualizing the metazoan proliferation-quiescence decision in vivo
title_sort visualizing the metazoan proliferation-quiescence decision in vivo
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-12-01
description Cell proliferation and quiescence are intimately coordinated during metazoan development. Here, we adapt a cyclin-dependent kinase (CDK) sensor to uncouple these key events of the cell cycle in Caenorhabditis elegans and zebrafish through live-cell imaging. The CDK sensor consists of a fluorescently tagged CDK substrate that steadily translocates from the nucleus to the cytoplasm in response to increasing CDK activity and consequent sensor phosphorylation. We show that the CDK sensor can distinguish cycling cells in G1 from quiescent cells in G0, revealing a possible commitment point and a cryptic stochasticity in an otherwise invariant C. elegans cell lineage. Finally, we derive a predictive model of future proliferation behavior in C. elegans based on a snapshot of CDK activity in newly born cells. Thus, we introduce a live-cell imaging tool to facilitate in vivo studies of cell-cycle control in a wide-range of developmental contexts.
topic cell cycle
quiescence
cell proliferation
G1/G0
CDK sensor
url https://elifesciences.org/articles/63265
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