Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration

issue regeneration requires the activation of a set of specific growth signaling pathways. The identity of these cascades and their biological roles are known; however, the molecular mechanisms regulating the interplay between these pathways remain poorly understood. Here, we define a new role for S...

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Autores: Nakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698ab, García-Fernández-de-Barrena, M. (Maite)|||/items/cfa77580-40b9-43a4-b237-b234ef7fb6cb, Ortiz-Ruiz, M.C. (Maria C.)|||/items/09b93e00-0da7-4e32-9886-c38de07ab5f6, Almada, L.L. (Luciana L.)|||/items/29677c79-da0b-4a29-bd71-e9decae1754c, Hu, C. (Chunling)|||/items/04d72539-99e2-4a40-9d9a-fe4332595efe, Elsawa, S.F. (Sherine F.)|||/items/02d1ebd6-836d-4779-bf7f-1e1ec8d3eca4, Mills, L.D. (Lisa D.)|||/items/b81b93df-bff2-442f-b492-56f24ed207e2, Romecin, P.A. (Paola A.)|||/items/33e6aef0-baf2-4fff-8713-a939bc5b5208, Gulaid, K.H. (Kadra H.)|||/items/3ef3f71a-343d-497d-bdfb-289f38c7ad06, Moser, C.D. (Catherine D.)|||/items/3d8e33b8-8262-427a-93ab-539c1e4a0ee6, Han, J.J. (Jing-Jing)|||/items/5e8b3ed8-ecf1-48c1-95ce-0211edb115d3, Vrabel, A. (Anne)|||/items/03e9ec35-008f-48ed-888d-1d25b4b38612, Hanse, E.A. (Eric A.)|||/items/9870e4ef-6d80-42f5-8c8c-2a8b921b211b, Akogyeram, N.A. (Nicholas A.)|||/items/7279c976-f97e-489f-95b1-b12703773889, Albrecht, J.H. (Jeffrey H.)|||/items/f9b39250-7c51-4c1f-891f-7fa16145edbc, Monga, S.P. (Satdarshan P.)|||/items/068189ef-613a-48f4-9e6d-fc7ae6b5a6da, Sanderson, S.O. (Schuyler O.)|||/items/d012fcf9-0953-422c-acf1-2157ecf9152b, Prieto, J. (Jesús)|||/items/0d9c3dec-4a09-400d-8c83-23ece1096c71, Roberts, L.R. (Lewis R.)|||/items/53e58801-8eb8-49f9-9fd2-46b93d01e35b, Fernandez-Zapico, M.E. (Martín E.)|||/items/4c4f76f4-afec-47be-91c9-c67d0d54ac41
Formato: artículo
Fecha de publicación:2013
País:España
Recursos:Universidad de Navarra
Repositorio:Dadun. Depósito Académico Digital de la Universidad de Navarra
Idioma:inglés
OAI Identifier:oai:dadun.unav.edu:10171/121014
Acesso em linha:https://hdl.handle.net/10171/121014
Access Level:acceso abierto
Palavra-chave:Gene Knockout
Liver
Regeneration
Transcription Factors
Wnt Signaling
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spelling Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regenerationNakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698abGarcía-Fernández-de-Barrena, M. (Maite)|||/items/cfa77580-40b9-43a4-b237-b234ef7fb6cbOrtiz-Ruiz, M.C. (Maria C.)|||/items/09b93e00-0da7-4e32-9886-c38de07ab5f6Almada, L.L. (Luciana L.)|||/items/29677c79-da0b-4a29-bd71-e9decae1754cHu, C. (Chunling)|||/items/04d72539-99e2-4a40-9d9a-fe4332595efeElsawa, S.F. (Sherine F.)|||/items/02d1ebd6-836d-4779-bf7f-1e1ec8d3eca4Mills, L.D. (Lisa D.)|||/items/b81b93df-bff2-442f-b492-56f24ed207e2Romecin, P.A. (Paola A.)|||/items/33e6aef0-baf2-4fff-8713-a939bc5b5208Gulaid, K.H. (Kadra H.)|||/items/3ef3f71a-343d-497d-bdfb-289f38c7ad06Moser, C.D. (Catherine D.)|||/items/3d8e33b8-8262-427a-93ab-539c1e4a0ee6Han, J.J. (Jing-Jing)|||/items/5e8b3ed8-ecf1-48c1-95ce-0211edb115d3Vrabel, A. (Anne)|||/items/03e9ec35-008f-48ed-888d-1d25b4b38612Hanse, E.A. (Eric A.)|||/items/9870e4ef-6d80-42f5-8c8c-2a8b921b211bAkogyeram, N.A. (Nicholas A.)|||/items/7279c976-f97e-489f-95b1-b12703773889Albrecht, J.H. (Jeffrey H.)|||/items/f9b39250-7c51-4c1f-891f-7fa16145edbcMonga, S.P. (Satdarshan P.)|||/items/068189ef-613a-48f4-9e6d-fc7ae6b5a6daSanderson, S.O. (Schuyler O.)|||/items/d012fcf9-0953-422c-acf1-2157ecf9152bPrieto, J. (Jesús)|||/items/0d9c3dec-4a09-400d-8c83-23ece1096c71Roberts, L.R. (Lewis R.)|||/items/53e58801-8eb8-49f9-9fd2-46b93d01e35bFernandez-Zapico, M.E. (Martín E.)|||/items/4c4f76f4-afec-47be-91c9-c67d0d54ac41Gene KnockoutLiverRegenerationTranscription FactorsWnt Signalingissue regeneration requires the activation of a set of specific growth signaling pathways. The identity of these cascades and their biological roles are known; however, the molecular mechanisms regulating the interplay between these pathways remain poorly understood. Here, we define a new role for SULFATASE 2 (SULF2) in regulating tissue regeneration and define the WNT-GLI1 axis as a novel downstream effector for this sulfatase in a liver model of tissue regeneration. SULF2 is a heparan sulfate 6-O-endosulfatase, which releases growth factors from extracellular storage sites turning active multiple signaling pathways. We demonstrate that SULF2-KO mice display delayed regeneration after partial hepatectomy (PH). Mechanistic analysis of the SULF2-KO phenotype showed a decrease in WNT signaling pathway activity in vivo. In isolated hepatocytes, SULF2 deficiency blocked WNT-induced β-CATENIN nuclear translocation, TCF activation, and proliferation. Furthermore, we identified the transcription factor GLI1 as a novel target of the SULF2-WNT cascade. WNT induces GLI1 expression in a SULF2- and β-CATENIN-dependent manner. GLI1-KO mice phenocopied the SULF2-KO, showing delayed regeneration and decreased hepatocyte proliferation. Moreover, we identified CYCLIN D1, a key mediator of cell growth during tissue regeneration, as a GLI1 transcriptional target. GLI1 binds to the cyclin d1 promoter and regulates its activity and expression. Finally, restoring GLI1 expression in the liver of SULF2-KO mice after PH rescues CYCLIN D1 expression and hepatocyte proliferation to wild-type levels. Thus, together these findings define a novel pathway in which SULF2 regulates tissue regeneration in part via the activation of a novel WNT-GLI1-CYCLIN D1 pathway.ElsevierDadun. Depósito Académico Digital Universidad de Navarra20132013-01-0120132013-01-01journal articlehttp://purl.org/coar/resource_type/c_6501info:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/10171/121014reponame:Dadun. Depósito Académico Digital de la Universidad de Navarrainstname:Universidad de NavarraInglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:dadun.unav.edu:10171/1210142026-06-21T12:47:57Z
dc.title.none.fl_str_mv Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
title Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
spellingShingle Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
Nakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698ab
Gene Knockout
Liver
Regeneration
Transcription Factors
Wnt Signaling
title_short Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
title_full Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
title_fullStr Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
title_full_unstemmed Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
title_sort Activation of the transcription factor gli1 by wnt signaling underlies the role of SULFATASE 2 as a regulator of tissue regeneration
dc.creator.none.fl_str_mv Nakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698ab
García-Fernández-de-Barrena, M. (Maite)|||/items/cfa77580-40b9-43a4-b237-b234ef7fb6cb
Ortiz-Ruiz, M.C. (Maria C.)|||/items/09b93e00-0da7-4e32-9886-c38de07ab5f6
Almada, L.L. (Luciana L.)|||/items/29677c79-da0b-4a29-bd71-e9decae1754c
Hu, C. (Chunling)|||/items/04d72539-99e2-4a40-9d9a-fe4332595efe
Elsawa, S.F. (Sherine F.)|||/items/02d1ebd6-836d-4779-bf7f-1e1ec8d3eca4
Mills, L.D. (Lisa D.)|||/items/b81b93df-bff2-442f-b492-56f24ed207e2
Romecin, P.A. (Paola A.)|||/items/33e6aef0-baf2-4fff-8713-a939bc5b5208
Gulaid, K.H. (Kadra H.)|||/items/3ef3f71a-343d-497d-bdfb-289f38c7ad06
Moser, C.D. (Catherine D.)|||/items/3d8e33b8-8262-427a-93ab-539c1e4a0ee6
Han, J.J. (Jing-Jing)|||/items/5e8b3ed8-ecf1-48c1-95ce-0211edb115d3
Vrabel, A. (Anne)|||/items/03e9ec35-008f-48ed-888d-1d25b4b38612
Hanse, E.A. (Eric A.)|||/items/9870e4ef-6d80-42f5-8c8c-2a8b921b211b
Akogyeram, N.A. (Nicholas A.)|||/items/7279c976-f97e-489f-95b1-b12703773889
Albrecht, J.H. (Jeffrey H.)|||/items/f9b39250-7c51-4c1f-891f-7fa16145edbc
Monga, S.P. (Satdarshan P.)|||/items/068189ef-613a-48f4-9e6d-fc7ae6b5a6da
Sanderson, S.O. (Schuyler O.)|||/items/d012fcf9-0953-422c-acf1-2157ecf9152b
Prieto, J. (Jesús)|||/items/0d9c3dec-4a09-400d-8c83-23ece1096c71
Roberts, L.R. (Lewis R.)|||/items/53e58801-8eb8-49f9-9fd2-46b93d01e35b
Fernandez-Zapico, M.E. (Martín E.)|||/items/4c4f76f4-afec-47be-91c9-c67d0d54ac41
author Nakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698ab
author_facet Nakamura, I. (Ikuo)|||/items/17bbe2f0-037c-4f6d-b43c-f10e173698ab
García-Fernández-de-Barrena, M. (Maite)|||/items/cfa77580-40b9-43a4-b237-b234ef7fb6cb
Ortiz-Ruiz, M.C. (Maria C.)|||/items/09b93e00-0da7-4e32-9886-c38de07ab5f6
Almada, L.L. (Luciana L.)|||/items/29677c79-da0b-4a29-bd71-e9decae1754c
Hu, C. (Chunling)|||/items/04d72539-99e2-4a40-9d9a-fe4332595efe
Elsawa, S.F. (Sherine F.)|||/items/02d1ebd6-836d-4779-bf7f-1e1ec8d3eca4
Mills, L.D. (Lisa D.)|||/items/b81b93df-bff2-442f-b492-56f24ed207e2
Romecin, P.A. (Paola A.)|||/items/33e6aef0-baf2-4fff-8713-a939bc5b5208
Gulaid, K.H. (Kadra H.)|||/items/3ef3f71a-343d-497d-bdfb-289f38c7ad06
Moser, C.D. (Catherine D.)|||/items/3d8e33b8-8262-427a-93ab-539c1e4a0ee6
Han, J.J. (Jing-Jing)|||/items/5e8b3ed8-ecf1-48c1-95ce-0211edb115d3
Vrabel, A. (Anne)|||/items/03e9ec35-008f-48ed-888d-1d25b4b38612
Hanse, E.A. (Eric A.)|||/items/9870e4ef-6d80-42f5-8c8c-2a8b921b211b
Akogyeram, N.A. (Nicholas A.)|||/items/7279c976-f97e-489f-95b1-b12703773889
Albrecht, J.H. (Jeffrey H.)|||/items/f9b39250-7c51-4c1f-891f-7fa16145edbc
Monga, S.P. (Satdarshan P.)|||/items/068189ef-613a-48f4-9e6d-fc7ae6b5a6da
Sanderson, S.O. (Schuyler O.)|||/items/d012fcf9-0953-422c-acf1-2157ecf9152b
Prieto, J. (Jesús)|||/items/0d9c3dec-4a09-400d-8c83-23ece1096c71
Roberts, L.R. (Lewis R.)|||/items/53e58801-8eb8-49f9-9fd2-46b93d01e35b
Fernandez-Zapico, M.E. (Martín E.)|||/items/4c4f76f4-afec-47be-91c9-c67d0d54ac41
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author2 García-Fernández-de-Barrena, M. (Maite)|||/items/cfa77580-40b9-43a4-b237-b234ef7fb6cb
Ortiz-Ruiz, M.C. (Maria C.)|||/items/09b93e00-0da7-4e32-9886-c38de07ab5f6
Almada, L.L. (Luciana L.)|||/items/29677c79-da0b-4a29-bd71-e9decae1754c
Hu, C. (Chunling)|||/items/04d72539-99e2-4a40-9d9a-fe4332595efe
Elsawa, S.F. (Sherine F.)|||/items/02d1ebd6-836d-4779-bf7f-1e1ec8d3eca4
Mills, L.D. (Lisa D.)|||/items/b81b93df-bff2-442f-b492-56f24ed207e2
Romecin, P.A. (Paola A.)|||/items/33e6aef0-baf2-4fff-8713-a939bc5b5208
Gulaid, K.H. (Kadra H.)|||/items/3ef3f71a-343d-497d-bdfb-289f38c7ad06
Moser, C.D. (Catherine D.)|||/items/3d8e33b8-8262-427a-93ab-539c1e4a0ee6
Han, J.J. (Jing-Jing)|||/items/5e8b3ed8-ecf1-48c1-95ce-0211edb115d3
Vrabel, A. (Anne)|||/items/03e9ec35-008f-48ed-888d-1d25b4b38612
Hanse, E.A. (Eric A.)|||/items/9870e4ef-6d80-42f5-8c8c-2a8b921b211b
Akogyeram, N.A. (Nicholas A.)|||/items/7279c976-f97e-489f-95b1-b12703773889
Albrecht, J.H. (Jeffrey H.)|||/items/f9b39250-7c51-4c1f-891f-7fa16145edbc
Monga, S.P. (Satdarshan P.)|||/items/068189ef-613a-48f4-9e6d-fc7ae6b5a6da
Sanderson, S.O. (Schuyler O.)|||/items/d012fcf9-0953-422c-acf1-2157ecf9152b
Prieto, J. (Jesús)|||/items/0d9c3dec-4a09-400d-8c83-23ece1096c71
Roberts, L.R. (Lewis R.)|||/items/53e58801-8eb8-49f9-9fd2-46b93d01e35b
Fernandez-Zapico, M.E. (Martín E.)|||/items/4c4f76f4-afec-47be-91c9-c67d0d54ac41
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dc.contributor.none.fl_str_mv Dadun. Depósito Académico Digital Universidad de Navarra
dc.subject.none.fl_str_mv Gene Knockout
Liver
Regeneration
Transcription Factors
Wnt Signaling
topic Gene Knockout
Liver
Regeneration
Transcription Factors
Wnt Signaling
description issue regeneration requires the activation of a set of specific growth signaling pathways. The identity of these cascades and their biological roles are known; however, the molecular mechanisms regulating the interplay between these pathways remain poorly understood. Here, we define a new role for SULFATASE 2 (SULF2) in regulating tissue regeneration and define the WNT-GLI1 axis as a novel downstream effector for this sulfatase in a liver model of tissue regeneration. SULF2 is a heparan sulfate 6-O-endosulfatase, which releases growth factors from extracellular storage sites turning active multiple signaling pathways. We demonstrate that SULF2-KO mice display delayed regeneration after partial hepatectomy (PH). Mechanistic analysis of the SULF2-KO phenotype showed a decrease in WNT signaling pathway activity in vivo. In isolated hepatocytes, SULF2 deficiency blocked WNT-induced β-CATENIN nuclear translocation, TCF activation, and proliferation. Furthermore, we identified the transcription factor GLI1 as a novel target of the SULF2-WNT cascade. WNT induces GLI1 expression in a SULF2- and β-CATENIN-dependent manner. GLI1-KO mice phenocopied the SULF2-KO, showing delayed regeneration and decreased hepatocyte proliferation. Moreover, we identified CYCLIN D1, a key mediator of cell growth during tissue regeneration, as a GLI1 transcriptional target. GLI1 binds to the cyclin d1 promoter and regulates its activity and expression. Finally, restoring GLI1 expression in the liver of SULF2-KO mice after PH rescues CYCLIN D1 expression and hepatocyte proliferation to wild-type levels. Thus, together these findings define a novel pathway in which SULF2 regulates tissue regeneration in part via the activation of a novel WNT-GLI1-CYCLIN D1 pathway.
publishDate 2013
dc.date.none.fl_str_mv 2013
2013-01-01
2013
2013-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/10171/121014
url https://hdl.handle.net/10171/121014
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Dadun. Depósito Académico Digital de la Universidad de Navarra
instname:Universidad de Navarra
instname_str Universidad de Navarra
reponame_str Dadun. Depósito Académico Digital de la Universidad de Navarra
collection Dadun. Depósito Académico Digital de la Universidad de Navarra
repository.name.fl_str_mv
repository.mail.fl_str_mv
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