Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation

Autores
Gambini, Andres; Stein, Paula; Savy, Virginia; Grow, Edward J.; Papas, Brian N.; Zhang, Yingpei; Kenan, Anna C.; Padilla Banks, Elizabeth; Cairns, Bradley R.; Williams, Carmen J.
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Embryonic genome activation (EGA) is orchestrated by an intrinsic developmental program initiated during oocyte maturation with translation of stored maternal mRNAs. Here, we show that tankyrase, a poly(ADP-ribosyl) polymerase that regulates β-catenin levels, undergoes programmed translation during oocyte maturation and serves an essential role in mouse EGA. Newly translated TNKS triggers proteasomal degradation of axin, reducing targeted destruction of β-catenin and promoting β-catenin-mediated transcription of target genes, including Myc. MYC mediates ribosomal RNA transcription in 2-cell embryos, supporting global protein synthesis. Suppression of tankyrase activity using knockdown or chemical inhibition causes loss of nuclear β-catenin and global reductions in transcription and histone H3 acetylation. Chromatin and transcriptional profiling indicate that development arrests prior to the mid-2-cell stage, mediated in part by reductions in β-catenin and MYC. These findings indicate that post-transcriptional regulation of tankyrase serves as a ligand-independent developmental mechanism for post-translational β-catenin activation and is required to complete EGA.
Fil: Gambini, Andres. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario; Argentina
Fil: Stein, Paula. National Institutes of Health; Estados Unidos
Fil: Savy, Virginia. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Grow, Edward J.. University of Utah; Estados Unidos
Fil: Papas, Brian N.. National Institutes of Health; Estados Unidos
Fil: Zhang, Yingpei. National Institutes of Health; Estados Unidos
Fil: Kenan, Anna C.. National Institutes of Health; Estados Unidos
Fil: Padilla Banks, Elizabeth. National Institutes of Health; Estados Unidos
Fil: Cairns, Bradley R.. University of Utah; Estados Unidos
Fil: Williams, Carmen J.. National Institutes of Health; Estados Unidos
Materia
EMBRYO
OOCYTE
TANKYRASE
MATURATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/112291
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/112291
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome ActivationGambini, AndresStein, PaulaSavy, VirginiaGrow, Edward J.Papas, Brian N.Zhang, YingpeiKenan, Anna C.Padilla Banks, ElizabethCairns, Bradley R.Williams, Carmen J.EMBRYOOOCYTETANKYRASEMATURATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Embryonic genome activation (EGA) is orchestrated by an intrinsic developmental program initiated during oocyte maturation with translation of stored maternal mRNAs. Here, we show that tankyrase, a poly(ADP-ribosyl) polymerase that regulates β-catenin levels, undergoes programmed translation during oocyte maturation and serves an essential role in mouse EGA. Newly translated TNKS triggers proteasomal degradation of axin, reducing targeted destruction of β-catenin and promoting β-catenin-mediated transcription of target genes, including Myc. MYC mediates ribosomal RNA transcription in 2-cell embryos, supporting global protein synthesis. Suppression of tankyrase activity using knockdown or chemical inhibition causes loss of nuclear β-catenin and global reductions in transcription and histone H3 acetylation. Chromatin and transcriptional profiling indicate that development arrests prior to the mid-2-cell stage, mediated in part by reductions in β-catenin and MYC. These findings indicate that post-transcriptional regulation of tankyrase serves as a ligand-independent developmental mechanism for post-translational β-catenin activation and is required to complete EGA.Fil: Gambini, Andres. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario; ArgentinaFil: Stein, Paula. National Institutes of Health; Estados UnidosFil: Savy, Virginia. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Grow, Edward J.. University of Utah; Estados UnidosFil: Papas, Brian N.. National Institutes of Health; Estados UnidosFil: Zhang, Yingpei. National Institutes of Health; Estados UnidosFil: Kenan, Anna C.. National Institutes of Health; Estados UnidosFil: Padilla Banks, Elizabeth. National Institutes of Health; Estados UnidosFil: Cairns, Bradley R.. University of Utah; Estados UnidosFil: Williams, Carmen J.. National Institutes of Health; Estados UnidosCell Press2020-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/112291Gambini, Andres; Stein, Paula; Savy, Virginia; Grow, Edward J.; Papas, Brian N.; et al.; Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation; Cell Press; Developmental Cell; 53; 5; 6-2020; 545-5601534-5807CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/abs/pii/S1534580720303506info:eu-repo/semantics/altIdentifier/doi/10.1016/j.devcel.2020.04.018info:eu-repo/semantics/altIdentifier/url/https://www.cell.com/developmental-cell/fulltext/S1534-5807(20)30350-6info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:46:03Zoai:ri.conicet.gov.ar:11336/112291instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:46:03.867CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
title Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
spellingShingle Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
Gambini, Andres
EMBRYO
OOCYTE
TANKYRASE
MATURATION
title_short Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
title_full Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
title_fullStr Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
title_full_unstemmed Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
title_sort Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation
dc.creator.none.fl_str_mv Gambini, Andres
Stein, Paula
Savy, Virginia
Grow, Edward J.
Papas, Brian N.
Zhang, Yingpei
Kenan, Anna C.
Padilla Banks, Elizabeth
Cairns, Bradley R.
Williams, Carmen J.
author Gambini, Andres
author_facet Gambini, Andres
Stein, Paula
Savy, Virginia
Grow, Edward J.
Papas, Brian N.
Zhang, Yingpei
Kenan, Anna C.
Padilla Banks, Elizabeth
Cairns, Bradley R.
Williams, Carmen J.
author_role author
author2 Stein, Paula
Savy, Virginia
Grow, Edward J.
Papas, Brian N.
Zhang, Yingpei
Kenan, Anna C.
Padilla Banks, Elizabeth
Cairns, Bradley R.
Williams, Carmen J.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv EMBRYO
OOCYTE
TANKYRASE
MATURATION
topic EMBRYO
OOCYTE
TANKYRASE
MATURATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Embryonic genome activation (EGA) is orchestrated by an intrinsic developmental program initiated during oocyte maturation with translation of stored maternal mRNAs. Here, we show that tankyrase, a poly(ADP-ribosyl) polymerase that regulates β-catenin levels, undergoes programmed translation during oocyte maturation and serves an essential role in mouse EGA. Newly translated TNKS triggers proteasomal degradation of axin, reducing targeted destruction of β-catenin and promoting β-catenin-mediated transcription of target genes, including Myc. MYC mediates ribosomal RNA transcription in 2-cell embryos, supporting global protein synthesis. Suppression of tankyrase activity using knockdown or chemical inhibition causes loss of nuclear β-catenin and global reductions in transcription and histone H3 acetylation. Chromatin and transcriptional profiling indicate that development arrests prior to the mid-2-cell stage, mediated in part by reductions in β-catenin and MYC. These findings indicate that post-transcriptional regulation of tankyrase serves as a ligand-independent developmental mechanism for post-translational β-catenin activation and is required to complete EGA.
Fil: Gambini, Andres. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario; Argentina
Fil: Stein, Paula. National Institutes of Health; Estados Unidos
Fil: Savy, Virginia. National Institutes of Health; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Grow, Edward J.. University of Utah; Estados Unidos
Fil: Papas, Brian N.. National Institutes of Health; Estados Unidos
Fil: Zhang, Yingpei. National Institutes of Health; Estados Unidos
Fil: Kenan, Anna C.. National Institutes of Health; Estados Unidos
Fil: Padilla Banks, Elizabeth. National Institutes of Health; Estados Unidos
Fil: Cairns, Bradley R.. University of Utah; Estados Unidos
Fil: Williams, Carmen J.. National Institutes of Health; Estados Unidos
description Embryonic genome activation (EGA) is orchestrated by an intrinsic developmental program initiated during oocyte maturation with translation of stored maternal mRNAs. Here, we show that tankyrase, a poly(ADP-ribosyl) polymerase that regulates β-catenin levels, undergoes programmed translation during oocyte maturation and serves an essential role in mouse EGA. Newly translated TNKS triggers proteasomal degradation of axin, reducing targeted destruction of β-catenin and promoting β-catenin-mediated transcription of target genes, including Myc. MYC mediates ribosomal RNA transcription in 2-cell embryos, supporting global protein synthesis. Suppression of tankyrase activity using knockdown or chemical inhibition causes loss of nuclear β-catenin and global reductions in transcription and histone H3 acetylation. Chromatin and transcriptional profiling indicate that development arrests prior to the mid-2-cell stage, mediated in part by reductions in β-catenin and MYC. These findings indicate that post-transcriptional regulation of tankyrase serves as a ligand-independent developmental mechanism for post-translational β-catenin activation and is required to complete EGA.
publishDate 2020
dc.date.none.fl_str_mv 2020-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/112291
Gambini, Andres; Stein, Paula; Savy, Virginia; Grow, Edward J.; Papas, Brian N.; et al.; Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation; Cell Press; Developmental Cell; 53; 5; 6-2020; 545-560
1534-5807
CONICET Digital
CONICET
url http://hdl.handle.net/11336/112291
identifier_str_mv Gambini, Andres; Stein, Paula; Savy, Virginia; Grow, Edward J.; Papas, Brian N.; et al.; Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation; Cell Press; Developmental Cell; 53; 5; 6-2020; 545-560
1534-5807
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/abs/pii/S1534580720303506
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.devcel.2020.04.018
info:eu-repo/semantics/altIdentifier/url/https://www.cell.com/developmental-cell/fulltext/S1534-5807(20)30350-6
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Cell Press
publisher.none.fl_str_mv Cell Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.13397

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