Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program

Tumors have aberrant proteomes that often do not match their corresponding transcriptome profiles. One possible cause of this discrepancy is the existence of aberrant RNA modification landscapes in the so-called epitranscriptome. Here, we report that human glioma cells undergo DNA methylation-associ...

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Autores: Janin, Maxime|||0000-0003-1013-4128, Ortiz-Barahona, V., de Moura, M. C., Martínez Cardús, Anna|||0000-0002-3937-8794, Llinàs-Arias, Pere|||0000-0002-3666-0532, Soler, Marta|||0000-0002-6656-957X, Nachmani, D., Pelletier, Joffrey|||0000-0001-9174-044X, Schumann, U., Calleja-Cervantes, María Eréndira|||0000-0003-0688-0793, Moran, S.|||0000-0003-4192-8983, Guil, Sonia|||0000-0002-2257-3331, Bueno-Costa, Alberto|||0000-0001-8700-2540, Piñeyro, David|||0000-0001-5633-3339, Perez-Salvia, Montserrat, Rosselló-Tortella, M., Piqué, Laia, Bech-Serra, Joan-Josep|||0000-0003-3486-781X, De La Torre Gómez, Gisela Carolina|||0000-0001-9363-291X, Vidal, August|||0000-0001-5727-2099, Martínez-Iniesta, M., Martín-Tejera, J. F., Villanueva, Alejandro|||0000-0001-5164-0006, Arias, Alexandra, Cuartas, Isabel, Aransay, Ana M.|||0000-0002-8271-612X, La Madrid, A. M., Carcaboso, Angel M.|||0000-0002-8485-426X, Santa-Maria, V., Mora, J., Fernández, Agustín F.|||0000-0002-3792-4085, Fraga, M. F., Aldecoa, Iban|||0000-0001-5774-7453, Pedrosa, Leire|||0000-0002-1852-4975, Graus Ribas, Francesc|||0000-0002-8924-8322, Vidal, Noemí|||0000-0002-2852-6667, Martinez, Fina|||0000-0002-0940-1025, Tortosa, Avelina|||0000-0002-9080-2976, Carrato, Cristina|||0000-0002-1953-8287, Balañá, Carmen|||0000-0003-0771-0390, Boudreau, M. W., Hergenrother, P. J., Kötter, P., Entian, K. D., Hench, Jürgen, Frank, Stephan|||0000-0001-6165-0187, Mansouri, S., Zadeh, G., Dans, P. D., Orozco López, Modesto|||0000-0002-8608-3278, Thomas, Gareth J., Blanco, Sandra, Seoane Suárez, Joan|||0000-0002-6541-5974, Preiss, T., Pandolfi, P. P., Esteller, M.|||0000-0003-4490-6093
Tipo de recurso: artículo
Fecha de publicación:2019
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:223379
Acceso en línea:https://ddd.uab.cat/record/223379
https://dx.doi.org/urn:doi:10.1007/s00401-019-02062-4
Access Level:acceso abierto
Palabra clave:Glioma
Epitranscriptomics
RNA methylation
Clinical outcome
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oai_identifier_str oai:ddd.uab.cat:223379
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
title Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
spellingShingle Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
Janin, Maxime|||0000-0003-1013-4128
Glioma
Epitranscriptomics
RNA methylation
Clinical outcome
title_short Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
title_full Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
title_fullStr Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
title_full_unstemmed Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
title_sort Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational program
dc.creator.none.fl_str_mv Janin, Maxime|||0000-0003-1013-4128
Ortiz-Barahona, V.
de Moura, M. C.
Martínez Cardús, Anna|||0000-0002-3937-8794
Llinàs-Arias, Pere|||0000-0002-3666-0532
Soler, Marta|||0000-0002-6656-957X
Nachmani, D.
Pelletier, Joffrey|||0000-0001-9174-044X
Schumann, U.
Calleja-Cervantes, María Eréndira|||0000-0003-0688-0793
Moran, S.|||0000-0003-4192-8983
Guil, Sonia|||0000-0002-2257-3331
Bueno-Costa, Alberto|||0000-0001-8700-2540
Piñeyro, David|||0000-0001-5633-3339
Perez-Salvia, Montserrat
Rosselló-Tortella, M.
Piqué, Laia
Bech-Serra, Joan-Josep|||0000-0003-3486-781X
De La Torre Gómez, Gisela Carolina|||0000-0001-9363-291X
Vidal, August|||0000-0001-5727-2099
Martínez-Iniesta, M.
Martín-Tejera, J. F.
Villanueva, Alejandro|||0000-0001-5164-0006
Arias, Alexandra
Cuartas, Isabel
Aransay, Ana M.|||0000-0002-8271-612X
La Madrid, A. M.
Carcaboso, Angel M.|||0000-0002-8485-426X
Santa-Maria, V.
Mora, J.
Fernández, Agustín F.|||0000-0002-3792-4085
Fraga, M. F.
Aldecoa, Iban|||0000-0001-5774-7453
Pedrosa, Leire|||0000-0002-1852-4975
Graus Ribas, Francesc|||0000-0002-8924-8322
Vidal, Noemí|||0000-0002-2852-6667
Martinez, Fina|||0000-0002-0940-1025
Tortosa, Avelina|||0000-0002-9080-2976
Carrato, Cristina|||0000-0002-1953-8287
Balañá, Carmen|||0000-0003-0771-0390
Boudreau, M. W.
Hergenrother, P. J.
Kötter, P.
Entian, K. D.
Hench, Jürgen
Frank, Stephan|||0000-0001-6165-0187
Mansouri, S.
Zadeh, G.
Dans, P. D.
Orozco López, Modesto|||0000-0002-8608-3278
Thomas, Gareth J.
Blanco, Sandra
Seoane Suárez, Joan|||0000-0002-6541-5974
Preiss, T.
Pandolfi, P. P.
Esteller, M.|||0000-0003-4490-6093
author Janin, Maxime|||0000-0003-1013-4128
author_facet Janin, Maxime|||0000-0003-1013-4128
Ortiz-Barahona, V.
de Moura, M. C.
Martínez Cardús, Anna|||0000-0002-3937-8794
Llinàs-Arias, Pere|||0000-0002-3666-0532
Soler, Marta|||0000-0002-6656-957X
Nachmani, D.
Pelletier, Joffrey|||0000-0001-9174-044X
Schumann, U.
Calleja-Cervantes, María Eréndira|||0000-0003-0688-0793
Moran, S.|||0000-0003-4192-8983
Guil, Sonia|||0000-0002-2257-3331
Bueno-Costa, Alberto|||0000-0001-8700-2540
Piñeyro, David|||0000-0001-5633-3339
Perez-Salvia, Montserrat
Rosselló-Tortella, M.
Piqué, Laia
Bech-Serra, Joan-Josep|||0000-0003-3486-781X
De La Torre Gómez, Gisela Carolina|||0000-0001-9363-291X
Vidal, August|||0000-0001-5727-2099
Martínez-Iniesta, M.
Martín-Tejera, J. F.
Villanueva, Alejandro|||0000-0001-5164-0006
Arias, Alexandra
Cuartas, Isabel
Aransay, Ana M.|||0000-0002-8271-612X
La Madrid, A. M.
Carcaboso, Angel M.|||0000-0002-8485-426X
Santa-Maria, V.
Mora, J.
Fernández, Agustín F.|||0000-0002-3792-4085
Fraga, M. F.
Aldecoa, Iban|||0000-0001-5774-7453
Pedrosa, Leire|||0000-0002-1852-4975
Graus Ribas, Francesc|||0000-0002-8924-8322
Vidal, Noemí|||0000-0002-2852-6667
Martinez, Fina|||0000-0002-0940-1025
Tortosa, Avelina|||0000-0002-9080-2976
Carrato, Cristina|||0000-0002-1953-8287
Balañá, Carmen|||0000-0003-0771-0390
Boudreau, M. W.
Hergenrother, P. J.
Kötter, P.
Entian, K. D.
Hench, Jürgen
Frank, Stephan|||0000-0001-6165-0187
Mansouri, S.
Zadeh, G.
Dans, P. D.
Orozco López, Modesto|||0000-0002-8608-3278
Thomas, Gareth J.
Blanco, Sandra
Seoane Suárez, Joan|||0000-0002-6541-5974
Preiss, T.
Pandolfi, P. P.
Esteller, M.|||0000-0003-4490-6093
author_role author
author2 Ortiz-Barahona, V.
de Moura, M. C.
Martínez Cardús, Anna|||0000-0002-3937-8794
Llinàs-Arias, Pere|||0000-0002-3666-0532
Soler, Marta|||0000-0002-6656-957X
Nachmani, D.
Pelletier, Joffrey|||0000-0001-9174-044X
Schumann, U.
Calleja-Cervantes, María Eréndira|||0000-0003-0688-0793
Moran, S.|||0000-0003-4192-8983
Guil, Sonia|||0000-0002-2257-3331
Bueno-Costa, Alberto|||0000-0001-8700-2540
Piñeyro, David|||0000-0001-5633-3339
Perez-Salvia, Montserrat
Rosselló-Tortella, M.
Piqué, Laia
Bech-Serra, Joan-Josep|||0000-0003-3486-781X
De La Torre Gómez, Gisela Carolina|||0000-0001-9363-291X
Vidal, August|||0000-0001-5727-2099
Martínez-Iniesta, M.
Martín-Tejera, J. F.
Villanueva, Alejandro|||0000-0001-5164-0006
Arias, Alexandra
Cuartas, Isabel
Aransay, Ana M.|||0000-0002-8271-612X
La Madrid, A. M.
Carcaboso, Angel M.|||0000-0002-8485-426X
Santa-Maria, V.
Mora, J.
Fernández, Agustín F.|||0000-0002-3792-4085
Fraga, M. F.
Aldecoa, Iban|||0000-0001-5774-7453
Pedrosa, Leire|||0000-0002-1852-4975
Graus Ribas, Francesc|||0000-0002-8924-8322
Vidal, Noemí|||0000-0002-2852-6667
Martinez, Fina|||0000-0002-0940-1025
Tortosa, Avelina|||0000-0002-9080-2976
Carrato, Cristina|||0000-0002-1953-8287
Balañá, Carmen|||0000-0003-0771-0390
Boudreau, M. W.
Hergenrother, P. J.
Kötter, P.
Entian, K. D.
Hench, Jürgen
Frank, Stephan|||0000-0001-6165-0187
Mansouri, S.
Zadeh, G.
Dans, P. D.
Orozco López, Modesto|||0000-0002-8608-3278
Thomas, Gareth J.
Blanco, Sandra
Seoane Suárez, Joan|||0000-0002-6541-5974
Preiss, T.
Pandolfi, P. P.
Esteller, M.|||0000-0003-4490-6093
author2_role author
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author
author
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author
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author
author
author
author
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author
author
author
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author
author
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dc.contributor.none.fl_str_mv Universitat Autònoma de Barcelona
dc.subject.none.fl_str_mv Glioma
Epitranscriptomics
RNA methylation
Clinical outcome
topic Glioma
Epitranscriptomics
RNA methylation
Clinical outcome
description Tumors have aberrant proteomes that often do not match their corresponding transcriptome profiles. One possible cause of this discrepancy is the existence of aberrant RNA modification landscapes in the so-called epitranscriptome. Here, we report that human glioma cells undergo DNA methylation-associated epigenetic silencing of NSUN5, a candidate RNA methyltransferase for 5-methylcytosine. In this setting, NSUN5 exhibits tumor-suppressor characteristics in vivo glioma models. We also found that NSUN5 loss generates an unmethylated status at the C3782 position of 28S rRNA that drives an overall depletion of protein synthesis, and leads to the emergence of an adaptive translational program for survival under conditions of cellular stress. Interestingly, NSUN5 epigenetic inactivation also renders these gliomas sensitive to bioactivatable substrates of the stress-related enzyme NQO1. Most importantly, NSUN5 epigenetic inactivation is a hallmark of glioma patients with long-term survival for this otherwise devastating disease.
publishDate 2019
dc.date.none.fl_str_mv 2
2019-01-01
2019
2019-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/223379
https://dx.doi.org/urn:doi:10.1007/s00401-019-02062-4
url https://ddd.uab.cat/record/223379
https://dx.doi.org/urn:doi:10.1007/s00401-019-02062-4
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv European Commission https://doi.org/10.13039/501100000780 268626
Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 SAF2014-55000-R
Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PIE13-00022
Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PI16-01278
Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 CB1-12-00312
Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PT13-0010-0009
Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2009/SGR-1315
Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2014/SGR-633
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
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
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Epigenetic loss of RNA-methyltransferase NSUN5 in glioma targets ribosomes to drive a stress adaptive translational programJanin, Maxime|||0000-0003-1013-4128Ortiz-Barahona, V.de Moura, M. C.Martínez Cardús, Anna|||0000-0002-3937-8794Llinàs-Arias, Pere|||0000-0002-3666-0532Soler, Marta|||0000-0002-6656-957XNachmani, D.Pelletier, Joffrey|||0000-0001-9174-044XSchumann, U.Calleja-Cervantes, María Eréndira|||0000-0003-0688-0793Moran, S.|||0000-0003-4192-8983Guil, Sonia|||0000-0002-2257-3331Bueno-Costa, Alberto|||0000-0001-8700-2540Piñeyro, David|||0000-0001-5633-3339Perez-Salvia, MontserratRosselló-Tortella, M.Piqué, LaiaBech-Serra, Joan-Josep|||0000-0003-3486-781XDe La Torre Gómez, Gisela Carolina|||0000-0001-9363-291XVidal, August|||0000-0001-5727-2099Martínez-Iniesta, M.Martín-Tejera, J. F.Villanueva, Alejandro|||0000-0001-5164-0006Arias, AlexandraCuartas, IsabelAransay, Ana M.|||0000-0002-8271-612XLa Madrid, A. M.Carcaboso, Angel M.|||0000-0002-8485-426XSanta-Maria, V.Mora, J.Fernández, Agustín F.|||0000-0002-3792-4085Fraga, M. F.Aldecoa, Iban|||0000-0001-5774-7453Pedrosa, Leire|||0000-0002-1852-4975Graus Ribas, Francesc|||0000-0002-8924-8322Vidal, Noemí|||0000-0002-2852-6667Martinez, Fina|||0000-0002-0940-1025Tortosa, Avelina|||0000-0002-9080-2976Carrato, Cristina|||0000-0002-1953-8287Balañá, Carmen|||0000-0003-0771-0390Boudreau, M. W.Hergenrother, P. J.Kötter, P.Entian, K. D.Hench, JürgenFrank, Stephan|||0000-0001-6165-0187Mansouri, S.Zadeh, G.Dans, P. D.Orozco López, Modesto|||0000-0002-8608-3278Thomas, Gareth J.Blanco, SandraSeoane Suárez, Joan|||0000-0002-6541-5974Preiss, T.Pandolfi, P. P.Esteller, M.|||0000-0003-4490-6093GliomaEpitranscriptomicsRNA methylationClinical outcomeTumors have aberrant proteomes that often do not match their corresponding transcriptome profiles. One possible cause of this discrepancy is the existence of aberrant RNA modification landscapes in the so-called epitranscriptome. Here, we report that human glioma cells undergo DNA methylation-associated epigenetic silencing of NSUN5, a candidate RNA methyltransferase for 5-methylcytosine. In this setting, NSUN5 exhibits tumor-suppressor characteristics in vivo glioma models. We also found that NSUN5 loss generates an unmethylated status at the C3782 position of 28S rRNA that drives an overall depletion of protein synthesis, and leads to the emergence of an adaptive translational program for survival under conditions of cellular stress. Interestingly, NSUN5 epigenetic inactivation also renders these gliomas sensitive to bioactivatable substrates of the stress-related enzyme NQO1. Most importantly, NSUN5 epigenetic inactivation is a hallmark of glioma patients with long-term survival for this otherwise devastating disease.Universitat Autònoma de Barcelona 22019-01-0120192019-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/223379https://dx.doi.org/urn:doi:10.1007/s00401-019-02062-4reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengEuropean Commission https://doi.org/10.13039/501100000780 268626Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 SAF2014-55000-RInstituto de Salud Carlos III https://doi.org/10.13039/501100004587 PIE13-00022Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PI16-01278Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 CB1-12-00312Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PT13-0010-0009Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2009/SGR-1315Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2014/SGR-633open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:2233792026-06-06T12:50:31Z
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