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Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma

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Resumo:In cancer, recurrent somatic single-nucleotide variants-which are rare in most paediatric cancers-are confined largely to protein-coding genes1-3. Here we report highly recurrent hotspot mutations (r.3A>G) of U1 spliceosomal small nuclear RNAs (snRNAs) in about 50% of Sonic hedgehog (SHH) medulloblastomas. These mutations were not present across other subgroups of medulloblastoma, and we identified these hotspot mutations in U1 snRNA in only <0.1% of 2,442 cancers, across 36 other tumour types. The mutations occur in 97% of adults (subtype SHHδ) and 25% of adolescents (subtype SHHα) with SHH medulloblastoma, but are largely absent from SHH medulloblastoma in infants. The U1 snRNA mutations occur in the 5' splice-site binding region, and snRNA-mutant tumours have significantly disrupted RNA splicing and an excess of 5' cryptic splicing events. Alternative splicing mediated by mutant U1 snRNA inactivates tumour-suppressor genes (PTCH1) and activates oncogenes (GLI2 and CCND2), and represents a target for therapy. These U1 snRNA mutations provide an example of highly recurrent and tissue-specific mutations of a non-protein-coding gene in cancer.
Autores principais:Suzuki, Hiromichi
Outros Autores:Kumar, Sachin A.; Shuai, Shimin; Diaz-Navarro, Ander; Gutierrez-Fernandez, Ana; De Antonellis, Pasqualino; Cavalli, Florence M. G.; Juraschka, Kyle; Farooq, Hamza; Shibahara, Ichiyo; Vladoiu, Maria C.; Zhang, Jiao; Abeysundara, Namal; Przelicki, David; Skowron, Patryk; Gauer, Nicole; Luu, Betty; Daniels, Craig; Wu, Xiaochong; Forget, Antoine; Momin, Ali; Wang, Jun; Dong, Weifan; Kim, Seung-Ki; Grajkowska, Wieslawa A.; Jouvet, Anne; Fèvre-Montange, Michelle; Garrè, Maria Luisa; Nageswara Rao, Amulya A.; Giannini, Caterina; Kros, Johan M; French, Pim J.; Jabado, Nada; Ng, Ho-Keung; Poon, Wai Sang; Eberhart, Charles G.; Pollack, Ian F.; Olson, James M.; Weiss, William A.; Kumabe, Toshihiro; López-Aguilar, Enrique; Lach, Boleslaw; Massimino, Maura; Van Meir, Erwin G.; Rubin, Joshua B.; Vibhakar, Rajeev; Chambless, Lola B.; Kijima, Noriyuki; Klekner, Almos; Bognár, László; Chan, Jennifer A.; Faria, Claudia; Ragoussis, Jiannis; Pfister, Stefan M.; Goldenberg, Anna; Wechsler-Reya, Robert J.; Bailey, Swneke D.; Garzia, Livia; Morrissy, A Sorana; Marra, Marco A.; Huang, Xi; Malkin, David; Ayrault, Olivier; Ramaswamy, Vijay; Puente, Xose S.; Calarco, John A.; Stein, Lincoln; Taylor, Michael D.
Ano:2019
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso restrito
Instituição associada:Universidade de Lisboa
Idioma:inglês
Origem:Repositório da Universidade de Lisboa
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author Suzuki, Hiromichi
author2 Kumar, Sachin A.
Shuai, Shimin
Diaz-Navarro, Ander
Gutierrez-Fernandez, Ana
De Antonellis, Pasqualino
Cavalli, Florence M. G.
Juraschka, Kyle
Farooq, Hamza
Shibahara, Ichiyo
Vladoiu, Maria C.
Zhang, Jiao
Abeysundara, Namal
Przelicki, David
Skowron, Patryk
Gauer, Nicole
Luu, Betty
Daniels, Craig
Wu, Xiaochong
Forget, Antoine
Momin, Ali
Wang, Jun
Dong, Weifan
Kim, Seung-Ki
Grajkowska, Wieslawa A.
Jouvet, Anne
Fèvre-Montange, Michelle
Garrè, Maria Luisa
Nageswara Rao, Amulya A.
Giannini, Caterina
Kros, Johan M
French, Pim J.
Jabado, Nada
Ng, Ho-Keung
Poon, Wai Sang
Eberhart, Charles G.
Pollack, Ian F.
Olson, James M.
Weiss, William A.
Kumabe, Toshihiro
López-Aguilar, Enrique
Lach, Boleslaw
Massimino, Maura
Van Meir, Erwin G.
Rubin, Joshua B.
Vibhakar, Rajeev
Chambless, Lola B.
Kijima, Noriyuki
Klekner, Almos
Bognár, László
Chan, Jennifer A.
Faria, Claudia
Ragoussis, Jiannis
Pfister, Stefan M.
Goldenberg, Anna
Wechsler-Reya, Robert J.
Bailey, Swneke D.
Garzia, Livia
Morrissy, A Sorana
Marra, Marco A.
Huang, Xi
Malkin, David
Ayrault, Olivier
Ramaswamy, Vijay
Puente, Xose S.
Calarco, John A.
Stein, Lincoln
Taylor, Michael D.
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author_facet Suzuki, Hiromichi
Kumar, Sachin A.
Shuai, Shimin
Diaz-Navarro, Ander
Gutierrez-Fernandez, Ana
De Antonellis, Pasqualino
Cavalli, Florence M. G.
Juraschka, Kyle
Farooq, Hamza
Shibahara, Ichiyo
Vladoiu, Maria C.
Zhang, Jiao
Abeysundara, Namal
Przelicki, David
Skowron, Patryk
Gauer, Nicole
Luu, Betty
Daniels, Craig
Wu, Xiaochong
Forget, Antoine
Momin, Ali
Wang, Jun
Dong, Weifan
Kim, Seung-Ki
Grajkowska, Wieslawa A.
Jouvet, Anne
Fèvre-Montange, Michelle
Garrè, Maria Luisa
Nageswara Rao, Amulya A.
Giannini, Caterina
Kros, Johan M
French, Pim J.
Jabado, Nada
Ng, Ho-Keung
Poon, Wai Sang
Eberhart, Charles G.
Pollack, Ian F.
Olson, James M.
Weiss, William A.
Kumabe, Toshihiro
López-Aguilar, Enrique
Lach, Boleslaw
Massimino, Maura
Van Meir, Erwin G.
Rubin, Joshua B.
Vibhakar, Rajeev
Chambless, Lola B.
Kijima, Noriyuki
Klekner, Almos
Bognár, László
Chan, Jennifer A.
Faria, Claudia
Ragoussis, Jiannis
Pfister, Stefan M.
Goldenberg, Anna
Wechsler-Reya, Robert J.
Bailey, Swneke D.
Garzia, Livia
Morrissy, A Sorana
Marra, Marco A.
Huang, Xi
Malkin, David
Ayrault, Olivier
Ramaswamy, Vijay
Puente, Xose S.
Calarco, John A.
Stein, Lincoln
Taylor, Michael D.
author_role author
contributor_name_str_mv Repositório Científico de Acesso Aberto da ULisboa
country_str PT
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datacite.contributors.contributor.contributorName.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
datacite.creators.creator.creatorName.fl_str_mv Suzuki, Hiromichi
Kumar, Sachin A.
Shuai, Shimin
Diaz-Navarro, Ander
Gutierrez-Fernandez, Ana
De Antonellis, Pasqualino
Cavalli, Florence M. G.
Juraschka, Kyle
Farooq, Hamza
Shibahara, Ichiyo
Vladoiu, Maria C.
Zhang, Jiao
Abeysundara, Namal
Przelicki, David
Skowron, Patryk
Gauer, Nicole
Luu, Betty
Daniels, Craig
Wu, Xiaochong
Forget, Antoine
Momin, Ali
Wang, Jun
Dong, Weifan
Kim, Seung-Ki
Grajkowska, Wieslawa A.
Jouvet, Anne
Fèvre-Montange, Michelle
Garrè, Maria Luisa
Nageswara Rao, Amulya A.
Giannini, Caterina
Kros, Johan M
French, Pim J.
Jabado, Nada
Ng, Ho-Keung
Poon, Wai Sang
Eberhart, Charles G.
Pollack, Ian F.
Olson, James M.
Weiss, William A.
Kumabe, Toshihiro
López-Aguilar, Enrique
Lach, Boleslaw
Massimino, Maura
Van Meir, Erwin G.
Rubin, Joshua B.
Vibhakar, Rajeev
Chambless, Lola B.
Kijima, Noriyuki
Klekner, Almos
Bognár, László
Chan, Jennifer A.
Faria, Claudia
Ragoussis, Jiannis
Pfister, Stefan M.
Goldenberg, Anna
Wechsler-Reya, Robert J.
Bailey, Swneke D.
Garzia, Livia
Morrissy, A Sorana
Marra, Marco A.
Huang, Xi
Malkin, David
Ayrault, Olivier
Ramaswamy, Vijay
Puente, Xose S.
Calarco, John A.
Stein, Lincoln
Taylor, Michael D.
datacite.date.Accepted.fl_str_mv 2019-01-01T00:00:00Z
datacite.date.available.fl_str_mv 2021-02-17T17:10:37Z
datacite.date.embargoed.fl_str_mv 2021-02-17T17:10:37Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_16ec
datacite.titles.title.fl_str_mv Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
dc.contributor.none.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
dc.creator.none.fl_str_mv Suzuki, Hiromichi
Kumar, Sachin A.
Shuai, Shimin
Diaz-Navarro, Ander
Gutierrez-Fernandez, Ana
De Antonellis, Pasqualino
Cavalli, Florence M. G.
Juraschka, Kyle
Farooq, Hamza
Shibahara, Ichiyo
Vladoiu, Maria C.
Zhang, Jiao
Abeysundara, Namal
Przelicki, David
Skowron, Patryk
Gauer, Nicole
Luu, Betty
Daniels, Craig
Wu, Xiaochong
Forget, Antoine
Momin, Ali
Wang, Jun
Dong, Weifan
Kim, Seung-Ki
Grajkowska, Wieslawa A.
Jouvet, Anne
Fèvre-Montange, Michelle
Garrè, Maria Luisa
Nageswara Rao, Amulya A.
Giannini, Caterina
Kros, Johan M
French, Pim J.
Jabado, Nada
Ng, Ho-Keung
Poon, Wai Sang
Eberhart, Charles G.
Pollack, Ian F.
Olson, James M.
Weiss, William A.
Kumabe, Toshihiro
López-Aguilar, Enrique
Lach, Boleslaw
Massimino, Maura
Van Meir, Erwin G.
Rubin, Joshua B.
Vibhakar, Rajeev
Chambless, Lola B.
Kijima, Noriyuki
Klekner, Almos
Bognár, László
Chan, Jennifer A.
Faria, Claudia
Ragoussis, Jiannis
Pfister, Stefan M.
Goldenberg, Anna
Wechsler-Reya, Robert J.
Bailey, Swneke D.
Garzia, Livia
Morrissy, A Sorana
Marra, Marco A.
Huang, Xi
Malkin, David
Ayrault, Olivier
Ramaswamy, Vijay
Puente, Xose S.
Calarco, John A.
Stein, Lincoln
Taylor, Michael D.
dc.date.Accepted.fl_str_mv 2019-01-01T00:00:00Z
dc.date.available.fl_str_mv 2021-02-17T17:10:37Z
dc.date.embargoed.fl_str_mv 2021-02-17T17:10:37Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10451/46407
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Springer Nature
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_16ec
dc.title.fl_str_mv Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description In cancer, recurrent somatic single-nucleotide variants-which are rare in most paediatric cancers-are confined largely to protein-coding genes1-3. Here we report highly recurrent hotspot mutations (r.3A>G) of U1 spliceosomal small nuclear RNAs (snRNAs) in about 50% of Sonic hedgehog (SHH) medulloblastomas. These mutations were not present across other subgroups of medulloblastoma, and we identified these hotspot mutations in U1 snRNA in only <0.1% of 2,442 cancers, across 36 other tumour types. The mutations occur in 97% of adults (subtype SHHδ) and 25% of adolescents (subtype SHHα) with SHH medulloblastoma, but are largely absent from SHH medulloblastoma in infants. The U1 snRNA mutations occur in the 5' splice-site binding region, and snRNA-mutant tumours have significantly disrupted RNA splicing and an excess of 5' cryptic splicing events. Alternative splicing mediated by mutant U1 snRNA inactivates tumour-suppressor genes (PTCH1) and activates oncogenes (GLI2 and CCND2), and represents a target for therapy. These U1 snRNA mutations provide an example of highly recurrent and tissue-specific mutations of a non-protein-coding gene in cancer.
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eu_rights_str_mv restrictedAccess
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fulltext.url.fl_str_mv https://repositorio.ulisboa.pt/bitstreams/4883936f-7ede-400b-9909-2acfd56ddef6/download
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identifier.url.fl_str_mv http://hdl.handle.net/10451/46407
instacron_str ul
institution Universidade de Lisboa
instname_str Universidade de Lisboa
language eng
network_acronym_str ul
network_name_str Repositório da Universidade de Lisboa
oai_identifier_str oai:repositorio.ulisboa.pt:10451/46407
organization_str_mv urn:organizationAcronym:ul
person_str_mv Suzuki, Hiromichi
Kumar, Sachin A.
Shuai, Shimin
Diaz-Navarro, Ander
Gutierrez-Fernandez, Ana
De Antonellis, Pasqualino
Cavalli, Florence M. G.
Juraschka, Kyle
Farooq, Hamza
Shibahara, Ichiyo
Vladoiu, Maria C.
Zhang, Jiao
Abeysundara, Namal
Przelicki, David
Skowron, Patryk
Gauer, Nicole
Luu, Betty
Daniels, Craig
Wu, Xiaochong
Forget, Antoine
Momin, Ali
Wang, Jun
Dong, Weifan
Kim, Seung-Ki
Grajkowska, Wieslawa A.
Jouvet, Anne
Fèvre-Montange, Michelle
Garrè, Maria Luisa
Nageswara Rao, Amulya A.
Giannini, Caterina
Kros, Johan M
French, Pim J.
Jabado, Nada
Ng, Ho-Keung
Poon, Wai Sang
Eberhart, Charles G.
Pollack, Ian F.
Olson, James M.
Weiss, William A.
Kumabe, Toshihiro
López-Aguilar, Enrique
Lach, Boleslaw
Massimino, Maura
Van Meir, Erwin G.
Rubin, Joshua B.
Vibhakar, Rajeev
Chambless, Lola B.
Kijima, Noriyuki
Klekner, Almos
Bognár, László
Chan, Jennifer A.
Faria, Claudia
Faria, Claudia
https://www.ciencia-id.pt/AD1B-C408-B6A8
AD1B-C408-B6A8
http://orcid.org/0000-0003-1259-9922
0000-0003-1259-9922
Ragoussis, Jiannis
Pfister, Stefan M.
Goldenberg, Anna
Wechsler-Reya, Robert J.
Bailey, Swneke D.
Garzia, Livia
Morrissy, A Sorana
Marra, Marco A.
Huang, Xi
Malkin, David
Ayrault, Olivier
Ramaswamy, Vijay
Puente, Xose S.
Calarco, John A.
Stein, Lincoln
Taylor, Michael D.
publishDate 2019
publisher.none.fl_str_mv Springer Nature
reponame_str Repositório da Universidade de Lisboa
repository_id_str urn:repositoryAcronym:ul
service_str_mv urn:repositoryAcronym:ul
spelling engSpringer Naturept_PTIn cancer, recurrent somatic single-nucleotide variants-which are rare in most paediatric cancers-are confined largely to protein-coding genes1-3. Here we report highly recurrent hotspot mutations (r.3A>G) of U1 spliceosomal small nuclear RNAs (snRNAs) in about 50% of Sonic hedgehog (SHH) medulloblastomas. These mutations were not present across other subgroups of medulloblastoma, and we identified these hotspot mutations in U1 snRNA in only <0.1% of 2,442 cancers, across 36 other tumour types. The mutations occur in 97% of adults (subtype SHHδ) and 25% of adolescents (subtype SHHα) with SHH medulloblastoma, but are largely absent from SHH medulloblastoma in infants. The U1 snRNA mutations occur in the 5' splice-site binding region, and snRNA-mutant tumours have significantly disrupted RNA splicing and an excess of 5' cryptic splicing events. Alternative splicing mediated by mutant U1 snRNA inactivates tumour-suppressor genes (PTCH1) and activates oncogenes (GLI2 and CCND2), and represents a target for therapy. These U1 snRNA mutations provide an example of highly recurrent and tissue-specific mutations of a non-protein-coding gene in cancer.application/pdfpt_PTRecurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastomaSuzuki, HiromichiKumar, Sachin A.Shuai, ShiminDiaz-Navarro, AnderGutierrez-Fernandez, AnaDe Antonellis, PasqualinoCavalli, Florence M. G.Juraschka, KyleFarooq, HamzaShibahara, IchiyoVladoiu, Maria C.Zhang, JiaoAbeysundara, NamalPrzelicki, DavidSkowron, PatrykGauer, NicoleLuu, BettyDaniels, CraigWu, XiaochongForget, AntoineMomin, AliWang, JunDong, WeifanKim, Seung-KiGrajkowska, Wieslawa A.Jouvet, AnneFèvre-Montange, MichelleGarrè, Maria LuisaNageswara Rao, Amulya A.Giannini, CaterinaKros, Johan MFrench, Pim J.Jabado, NadaNg, Ho-KeungPoon, Wai SangEberhart, Charles G.Pollack, Ian F.Olson, James M.Weiss, William A.Kumabe, ToshihiroLópez-Aguilar, EnriqueLach, BoleslawMassimino, MauraVan Meir, Erwin G.Rubin, Joshua B.Vibhakar, RajeevChambless, Lola B.Kijima, NoriyukiKlekner, AlmosBognár, LászlóChan, Jennifer A.PersonalFaria, ClaudiaDSpacehttp://dspace.org/items/94ff2476-7001-4e97-9396-4a8716a7cbbaDSpacehttp://dspace.org/items/94ff2476-7001-4e97-9396-4a8716a7cbbaFariaClaudiaCiência IDhttps://www.ciencia-id.ptAD1B-C408-B6A8ORCIDhttp://orcid.org0000-0003-1259-9922Ragoussis, JiannisPfister, Stefan M.Goldenberg, AnnaWechsler-Reya, Robert J.Bailey, Swneke D.Garzia, LiviaMorrissy, A SoranaMarra, Marco A.Huang, XiMalkin, DavidAyrault, OlivierRamaswamy, VijayPuente, Xose S.Calarco, John A.Stein, LincolnTaylor, Michael D.HostingInstitutionOrganizationalRepositório Científico de Acesso Aberto da ULisboae-mailmailto:repositorio@reitoria.ulisboa.ptrepositorio@reitoria.ulisboa.ptISSNIsPartOf0028-0836DOIIsPartOf10.1038/s41586-019-1650-02021-02-17T17:10:37Z20192019-01-01T00:00:00ZHandlehttp://hdl.handle.net/10451/46407http://purl.org/coar/access_right/c_16ecrestricted access12977499 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal articlehttp://purl.org/coar/access_right/c_16ecapplication/pdffulltexthttps://repositorio.ulisboa.pt/bitstreams/4883936f-7ede-400b-9909-2acfd56ddef6/downloadNature5747780707711
spellingShingle Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
Suzuki, Hiromichi
status SINGLETON
title Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
title_full Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
title_fullStr Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
title_full_unstemmed Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
title_short Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
title_sort Recurrent noncoding U1 snRNA mutations drive cryptic splicing in SHH medulloblastoma
url http://hdl.handle.net/10451/46407
visible 1