The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration

Senescence is a form of cell cycle arrest induced by stress such as DNA damage and oncogenes. However, while arrested, senescent cells secrete a variety of proteins collectively known as the senescence-associated secretory phenotype (SASP), which can reinforce the arrest and induce senescence in a p...

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Autores: Ritschka, Birgit, 1985-, Storer, Mekayla, 1981-, Mas Malavila, Alba, Heinzmann, Florian, Ortells Campos, Mª Carmen, 1984-, Morton, Jennifer P., Sansom, Owen J., Zender, Lars, Keyes, William M., 1973-
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Recursos:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/68900
Acesso em linha:http://hdl.handle.net/10230/68900
http://dx.doi.org/10.1101/gad.290635.116
Access Level:acceso abierto
Palavra-chave:Senescence
Plasticity
Stem cells
Papilloma
CD34
SASP
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spelling The senescence-associated secretory phenotype induces cellular plasticity and tissue regenerationRitschka, Birgit, 1985-Storer, Mekayla, 1981-Mas Malavila, AlbaHeinzmann, FlorianOrtells Campos, Mª Carmen, 1984-Morton, Jennifer P.Sansom, Owen J.Zender, LarsKeyes, William M., 1973-SenescencePlasticityStem cellsPapillomaCD34SASPSenescence is a form of cell cycle arrest induced by stress such as DNA damage and oncogenes. However, while arrested, senescent cells secrete a variety of proteins collectively known as the senescence-associated secretory phenotype (SASP), which can reinforce the arrest and induce senescence in a paracrine manner. However, the SASP has also been shown to favor embryonic development, wound healing, and even tumor growth, suggesting more complex physiological roles than currently understood. Here we uncover timely new functions of the SASP in promoting a proregenerative response through the induction of cell plasticity and stemness. We show that primary mouse keratinocytes transiently exposed to the SASP exhibit increased expression of stem cell markers and regenerative capacity in vivo. However, prolonged exposure to the SASP causes a subsequent cell-intrinsic senescence arrest to counter the continued regenerative stimuli. Finally, by inducing senescence in single cells in vivo in the liver, we demonstrate that this activates tissue-specific expression of stem cell markers. Together, this work uncovers a primary and beneficial role for the SASP in promoting cell plasticity and tissue regeneration and introduces the concept that transient therapeutic delivery of senescent cells could be harnessed to drive tissue regeneration.We thank Ryan Driskell and Fiona Watt for technical advice, Guillaume Filion and Panagiotis Papasaikas for advice on statistics, Pura Muñoz-Cánoves for β-actin GFP mice, the Centre for Genomic Regulation Bioinformatics unit for assistance, and Pura Muñoz-Cánoves and Juan Valcarcel for critical reading of the manuscript. M.S. and B.R. were supported with fellowships from the “La Caixa” foundation. This work was funded by grants SAF2010-18829 and SAF2013-49082-P (to W.M.K.) from the Spanish Ministry for Economy and Competitiveness, the Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR) from the Generalitat de Catalunya, and Centre for Genomic Regulation core funding.Cold Spring Harbor Laboratory Press (CSHL Press)202420242017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/68900http://dx.doi.org/10.1101/gad.290635.116reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésGenes & Development. 2017 Jan 15;31(2):172-83info:eu-repo/grantAgreement/ES/3PN/SAF2010-18829info:eu-repo/grantAgreement/ES/1PE/SAF2013-49082-P© 2017 Ritschka et al.; Published by Cold Spring Harbor Laboratory Press. This article, published in Genes & Development, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.http://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/689002026-06-12T07:21:37Z
dc.title.none.fl_str_mv The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
title The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
spellingShingle The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
Ritschka, Birgit, 1985-
Senescence
Plasticity
Stem cells
Papilloma
CD34
SASP
title_short The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
title_full The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
title_fullStr The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
title_full_unstemmed The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
title_sort The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration
dc.creator.none.fl_str_mv Ritschka, Birgit, 1985-
Storer, Mekayla, 1981-
Mas Malavila, Alba
Heinzmann, Florian
Ortells Campos, Mª Carmen, 1984-
Morton, Jennifer P.
Sansom, Owen J.
Zender, Lars
Keyes, William M., 1973-
author Ritschka, Birgit, 1985-
author_facet Ritschka, Birgit, 1985-
Storer, Mekayla, 1981-
Mas Malavila, Alba
Heinzmann, Florian
Ortells Campos, Mª Carmen, 1984-
Morton, Jennifer P.
Sansom, Owen J.
Zender, Lars
Keyes, William M., 1973-
author_role author
author2 Storer, Mekayla, 1981-
Mas Malavila, Alba
Heinzmann, Florian
Ortells Campos, Mª Carmen, 1984-
Morton, Jennifer P.
Sansom, Owen J.
Zender, Lars
Keyes, William M., 1973-
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Senescence
Plasticity
Stem cells
Papilloma
CD34
SASP
topic Senescence
Plasticity
Stem cells
Papilloma
CD34
SASP
description Senescence is a form of cell cycle arrest induced by stress such as DNA damage and oncogenes. However, while arrested, senescent cells secrete a variety of proteins collectively known as the senescence-associated secretory phenotype (SASP), which can reinforce the arrest and induce senescence in a paracrine manner. However, the SASP has also been shown to favor embryonic development, wound healing, and even tumor growth, suggesting more complex physiological roles than currently understood. Here we uncover timely new functions of the SASP in promoting a proregenerative response through the induction of cell plasticity and stemness. We show that primary mouse keratinocytes transiently exposed to the SASP exhibit increased expression of stem cell markers and regenerative capacity in vivo. However, prolonged exposure to the SASP causes a subsequent cell-intrinsic senescence arrest to counter the continued regenerative stimuli. Finally, by inducing senescence in single cells in vivo in the liver, we demonstrate that this activates tissue-specific expression of stem cell markers. Together, this work uncovers a primary and beneficial role for the SASP in promoting cell plasticity and tissue regeneration and introduces the concept that transient therapeutic delivery of senescent cells could be harnessed to drive tissue regeneration.
publishDate 2017
dc.date.none.fl_str_mv 2017
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/68900
http://dx.doi.org/10.1101/gad.290635.116
url http://hdl.handle.net/10230/68900
http://dx.doi.org/10.1101/gad.290635.116
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Genes & Development. 2017 Jan 15;31(2):172-83
info:eu-repo/grantAgreement/ES/3PN/SAF2010-18829
info:eu-repo/grantAgreement/ES/1PE/SAF2013-49082-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Cold Spring Harbor Laboratory Press (CSHL Press)
publisher.none.fl_str_mv Cold Spring Harbor Laboratory Press (CSHL Press)
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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