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A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay

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Resumo:Eukaryotic cells possess surveillance mechanisms that detect and degrade defective transcripts. Aberrant transcripts include mRNAs with a premature termination codon (PTC), targeted by the nonsense-mediated decay (NMD) pathway, and mRNAs lacking a termination codon, targeted by the nonstop decay (NSD) pathway. The eukaryotic exosome, a ribonucleolytic complex, plays a crucial role in mRNA processing and turnover through its catalytic subunits PM/Scl100 (Rrp6 in yeast), DIS3 (Rrp44 in yeast), and DIS3L1. Additionally, eukaryotic cells have other ribonucleases, such as SMG6 and XRN1, that participate in RNA surveillance. However, the specific pathways through which ribonucleases recognize and degrade mRNAs remain elusive. In this study, we characterized the involvement of human ribonucleases, both nuclear and cytoplasmic, in the mRNA surveillance mechanisms of NMD and NSD. We performed knockdowns of SMG6, PM/Scl100, XRN1, DIS3, and DIS3L1, analyzing the resulting changes in mRNA levels of selected natural NMD targets by RT-qPCR. Additionally, we examined the levels of different human β-globin variants under the same conditions: wild-type, NMD-resistant, NMD-sensitive, and NSD-sensitive. Our results demonstrate that all the studied ribonucleases are involved in the decay of certain endogenous NMD targets. Furthermore, we observed that the ribonucleases SMG6 and DIS3 contribute to the degradation of all β-globin variants, with an exception for βNS in the former case. This is also the case for PM/Scl100, which affects all β-globin variants except the NMD-sensitive variants. In contrast, DIS3L1 and XRN1 show specificity for β-globin WT and NMD-resistant variants. These findings suggest that eukaryotic ribonucleases are target-specific rather than pathway-specific. In addition, our data suggest that ribonucleases play broader roles in mRNA surveillance and degradation mechanisms beyond just NMD and NSD.
Autores principais:da Costa, Paulo J.
Outros Autores:Menezes, Juliane; Guedes, Raquel; Reis, Filipa P.; Teixeira, Alexandre; Saramago, Margarida; Viegas, Sandra C.; Arraiano, Cecília M.; Romão, Luísa
Ano:2024
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso aberto
Instituição associada:Universidade de Lisboa
Idioma:inglês
Origem:Repositório da Universidade de Lisboa
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author da Costa, Paulo J.
author2 Menezes, Juliane
Guedes, Raquel
Reis, Filipa P.
Teixeira, Alexandre
Saramago, Margarida
Viegas, Sandra C.
Arraiano, Cecília M.
Romão, Luísa
author2_role author
author
author
author
author
author
author
author
author_facet da Costa, Paulo J.
Menezes, Juliane
Guedes, Raquel
Reis, Filipa P.
Teixeira, Alexandre
Saramago, Margarida
Viegas, Sandra C.
Arraiano, Cecília M.
Romão, Luísa
author_role author
contributor_name_str_mv Repositório Científico de Acesso Aberto da ULisboa
country_str PT
creators_json_txt [{\"Person.name\":\"da Costa, Paulo J.\"},{\"Person.name\":\"Menezes, Juliane\",\"Person.identifier.orcid\":\"0000-0003-3727-2096\"},{\"Person.name\":\"Guedes, Raquel\"},{\"Person.name\":\"Reis, Filipa P.\"},{\"Person.name\":\"Teixeira, Alexandre\"},{\"Person.name\":\"Saramago, Margarida\"},{\"Person.name\":\"Viegas, Sandra C.\"},{\"Person.name\":\"Arraiano, Cecília M.\"},{\"Person.name\":\"Romão, Luísa\"}]
datacite.contributors.contributor.contributorName.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
datacite.creators.creator.creatorName.fl_str_mv da Costa, Paulo J.
Menezes, Juliane
Guedes, Raquel
Reis, Filipa P.
Teixeira, Alexandre
Saramago, Margarida
Viegas, Sandra C.
Arraiano, Cecília M.
Romão, Luísa
datacite.date.Accepted.fl_str_mv 2024-10-01T00:00:00Z
datacite.date.available.fl_str_mv 2025-01-21T12:54:01Z
datacite.date.embargoed.fl_str_mv 2025-01-21T12:54:01Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_abf2
datacite.titles.title.fl_str_mv A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
dc.contributor.none.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
dc.creator.none.fl_str_mv da Costa, Paulo J.
Menezes, Juliane
Guedes, Raquel
Reis, Filipa P.
Teixeira, Alexandre
Saramago, Margarida
Viegas, Sandra C.
Arraiano, Cecília M.
Romão, Luísa
dc.date.Accepted.fl_str_mv 2024-10-01T00:00:00Z
dc.date.available.fl_str_mv 2025-01-21T12:54:01Z
dc.date.embargoed.fl_str_mv 2025-01-21T12:54:01Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10400.5/97398
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv MDPI
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.title.fl_str_mv A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Eukaryotic cells possess surveillance mechanisms that detect and degrade defective transcripts. Aberrant transcripts include mRNAs with a premature termination codon (PTC), targeted by the nonsense-mediated decay (NMD) pathway, and mRNAs lacking a termination codon, targeted by the nonstop decay (NSD) pathway. The eukaryotic exosome, a ribonucleolytic complex, plays a crucial role in mRNA processing and turnover through its catalytic subunits PM/Scl100 (Rrp6 in yeast), DIS3 (Rrp44 in yeast), and DIS3L1. Additionally, eukaryotic cells have other ribonucleases, such as SMG6 and XRN1, that participate in RNA surveillance. However, the specific pathways through which ribonucleases recognize and degrade mRNAs remain elusive. In this study, we characterized the involvement of human ribonucleases, both nuclear and cytoplasmic, in the mRNA surveillance mechanisms of NMD and NSD. We performed knockdowns of SMG6, PM/Scl100, XRN1, DIS3, and DIS3L1, analyzing the resulting changes in mRNA levels of selected natural NMD targets by RT-qPCR. Additionally, we examined the levels of different human β-globin variants under the same conditions: wild-type, NMD-resistant, NMD-sensitive, and NSD-sensitive. Our results demonstrate that all the studied ribonucleases are involved in the decay of certain endogenous NMD targets. Furthermore, we observed that the ribonucleases SMG6 and DIS3 contribute to the degradation of all β-globin variants, with an exception for βNS in the former case. This is also the case for PM/Scl100, which affects all β-globin variants except the NMD-sensitive variants. In contrast, DIS3L1 and XRN1 show specificity for β-globin WT and NMD-resistant variants. These findings suggest that eukaryotic ribonucleases are target-specific rather than pathway-specific. In addition, our data suggest that ribonucleases play broader roles in mRNA surveillance and degradation mechanisms beyond just NMD and NSD.
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eu_rights_str_mv openAccess
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language eng
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oai_identifier_str oai:repositorio.ulisboa.pt:10400.5/97398
organization_str_mv urn:organizationAcronym:ul
person_str_mv da Costa, Paulo J.
Menezes, Juliane
Menezes, Juliane
https://www.ciencia-id.pt/1714-0687-B84D
1714-0687-B84D
http://orcid.org/0000-0003-3727-2096
0000-0003-3727-2096
Guedes, Raquel
Reis, Filipa P.
Teixeira, Alexandre
Saramago, Margarida
Viegas, Sandra C.
Arraiano, Cecília M.
Romão, Luísa
publishDate 2024
publisher.none.fl_str_mv MDPI
reponame_str Repositório da Universidade de Lisboa
repository_id_str urn:repositoryAcronym:ul
service_str_mv urn:repositoryAcronym:ul
spelling engMDPIpt_PTEukaryotic cells possess surveillance mechanisms that detect and degrade defective transcripts. Aberrant transcripts include mRNAs with a premature termination codon (PTC), targeted by the nonsense-mediated decay (NMD) pathway, and mRNAs lacking a termination codon, targeted by the nonstop decay (NSD) pathway. The eukaryotic exosome, a ribonucleolytic complex, plays a crucial role in mRNA processing and turnover through its catalytic subunits PM/Scl100 (Rrp6 in yeast), DIS3 (Rrp44 in yeast), and DIS3L1. Additionally, eukaryotic cells have other ribonucleases, such as SMG6 and XRN1, that participate in RNA surveillance. However, the specific pathways through which ribonucleases recognize and degrade mRNAs remain elusive. In this study, we characterized the involvement of human ribonucleases, both nuclear and cytoplasmic, in the mRNA surveillance mechanisms of NMD and NSD. We performed knockdowns of SMG6, PM/Scl100, XRN1, DIS3, and DIS3L1, analyzing the resulting changes in mRNA levels of selected natural NMD targets by RT-qPCR. Additionally, we examined the levels of different human β-globin variants under the same conditions: wild-type, NMD-resistant, NMD-sensitive, and NSD-sensitive. Our results demonstrate that all the studied ribonucleases are involved in the decay of certain endogenous NMD targets. Furthermore, we observed that the ribonucleases SMG6 and DIS3 contribute to the degradation of all β-globin variants, with an exception for βNS in the former case. This is also the case for PM/Scl100, which affects all β-globin variants except the NMD-sensitive variants. In contrast, DIS3L1 and XRN1 show specificity for β-globin WT and NMD-resistant variants. These findings suggest that eukaryotic ribonucleases are target-specific rather than pathway-specific. In addition, our data suggest that ribonucleases play broader roles in mRNA surveillance and degradation mechanisms beyond just NMD and NSD.application/pdfpt_PTA Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decayda Costa, Paulo J.PersonalMenezes, JulianeDSpacehttp://dspace.org/items/10743a71-d1d4-4cb1-a4e6-8f5f342947aaDSpacehttp://dspace.org/items/10743a71-d1d4-4cb1-a4e6-8f5f342947aaMenezesJulianeCiência IDhttps://www.ciencia-id.pt1714-0687-B84DORCIDhttp://orcid.org0000-0003-3727-2096Guedes, RaquelReis, Filipa P.Teixeira, AlexandreSaramago, MargaridaViegas, Sandra C.Arraiano, Cecília M.Romão, LuísaHostingInstitutionOrganizationalRepositório Científico de Acesso Aberto da ULisboae-mailmailto:repositorio@reitoria.ulisboa.ptrepositorio@reitoria.ulisboa.ptDOIIsPartOf10.3390/genes151013082025-01-21T12:54:01Z2024-102024-10-01T00:00:00ZHandlehttp://hdl.handle.net/10400.5/97398http://purl.org/coar/access_right/c_abf2open access1553580 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal article2024-10http://creativecommons.org/licenses/by/4.0/http://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://repositorio.ulisboa.pt/bitstreams/3a615413-38c7-43e0-8000-f2fca4cec69b/downloadGenes15101308
spellingShingle A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
da Costa, Paulo J.
status SINGLETON
title A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
title_full A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
title_fullStr A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
title_full_unstemmed A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
title_short A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
title_sort A Comparative Overview of the Role of Human Ribonucleases in Nonsense-Mediated mRNA Decay
url http://hdl.handle.net/10400.5/97398
visible 1