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Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity

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Resumo:Removal of introns from pre-messenger RNAs (pre-mRNAs) via splicing provides a versatile means of genetic regulation that is often disrupted in human diseases. To decipher how splicing occurs in real time, we directly examined with single-molecule sensitivity the kinetics of intron excision from pre-mRNA in the nucleus of living human cells. By using two different RNA labeling methods, MS2 and λN, we show that β-globin introns are transcribed and excised in 20-30 s. Furthermore, we show that replacing the weak polypyrimidine (Py) tract in mouse immunoglobulin μ (IgM) pre-mRNA by a U-rich Py decreases the intron lifetime, thus providing direct evidence that splice-site strength influences splicing kinetics. We also found that RNA polymerase II transcribes at elongation rates ranging between 3 and 6 kb min(-1) and that transcription can be rate limiting for splicing. These results have important implications for a mechanistic understanding of cotranscriptional splicing regulation in the live-cell context.
Autores principais:Martin, Robert M.
Outros Autores:Rino, José; Carvalho, Célia; Kirchhausen, Tomas; Carmo-Fonseca, Maria
Ano:2013
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 Martin, Robert M.
author2 Rino, José
Carvalho, Célia
Kirchhausen, Tomas
Carmo-Fonseca, Maria
author2_role author
author
author
author
author_facet Martin, Robert M.
Rino, José
Carvalho, Célia
Kirchhausen, Tomas
Carmo-Fonseca, Maria
author_role author
contributor_name_str_mv Repositório Científico de Acesso Aberto da ULisboa
country_str PT
creators_json_txt [{\"Person.name\":\"Martin, Robert M.\",\"Person.identifier.orcid\":\"0000-0001-5600-7525\"},{\"Person.name\":\"Rino, José\",\"Person.identifier.orcid\":\"0000-0002-0637-4527\"},{\"Person.name\":\"Carvalho, Célia\",\"Person.identifier.orcid\":\"0000-0002-5980-595X\"},{\"Person.name\":\"Kirchhausen, Tomas\"},{\"Person.name\":\"Carmo-Fonseca, Maria\",\"Person.identifier.orcid\":\"0000-0002-3402-7143\"}]
datacite.contributors.contributor.contributorName.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
datacite.creators.creator.creatorName.fl_str_mv Martin, Robert M.
Rino, José
Carvalho, Célia
Kirchhausen, Tomas
Carmo-Fonseca, Maria
datacite.date.Accepted.fl_str_mv 2013-01-01T00:00:00Z
datacite.date.available.fl_str_mv 2021-12-03T15:47:59Z
datacite.date.embargoed.fl_str_mv 2021-12-03T15:47:59Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_abf2
datacite.titles.title.fl_str_mv Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
dc.contributor.none.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
dc.creator.none.fl_str_mv Martin, Robert M.
Rino, José
Carvalho, Célia
Kirchhausen, Tomas
Carmo-Fonseca, Maria
dc.date.Accepted.fl_str_mv 2013-01-01T00:00:00Z
dc.date.available.fl_str_mv 2021-12-03T15:47:59Z
dc.date.embargoed.fl_str_mv 2021-12-03T15:47:59Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10451/50271
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Elsevier
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.title.fl_str_mv Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Removal of introns from pre-messenger RNAs (pre-mRNAs) via splicing provides a versatile means of genetic regulation that is often disrupted in human diseases. To decipher how splicing occurs in real time, we directly examined with single-molecule sensitivity the kinetics of intron excision from pre-mRNA in the nucleus of living human cells. By using two different RNA labeling methods, MS2 and λN, we show that β-globin introns are transcribed and excised in 20-30 s. Furthermore, we show that replacing the weak polypyrimidine (Py) tract in mouse immunoglobulin μ (IgM) pre-mRNA by a U-rich Py decreases the intron lifetime, thus providing direct evidence that splice-site strength influences splicing kinetics. We also found that RNA polymerase II transcribes at elongation rates ranging between 3 and 6 kb min(-1) and that transcription can be rate limiting for splicing. These results have important implications for a mechanistic understanding of cotranscriptional splicing regulation in the live-cell context.
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eu_rights_str_mv openAccess
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funding.funder.alternateName_str_mv FCT
FCT
funding.funder.identifier_str_mv http://doi.org/10.13039/501100001871
http://doi.org/10.13039/501100001871
funding.funder.name_str_mv Fundação para a Ciência e a Tecnologia
Fundação para a Ciência e a Tecnologia
funding.name_str_mv 3599-PPCDT
id ul_f92e89bba1323ef5cc4e10d00124cffb
identifier.url.fl_str_mv http://hdl.handle.net/10451/50271
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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:10451/50271
organization_str_mv urn:organizationAcronym:ul
person_str_mv Martin, Robert M.
Martin, Robert M.
https://www.ciencia-id.pt/7516-6C51-460B
7516-6C51-460B
http://orcid.org/0000-0001-5600-7525
0000-0001-5600-7525
Rino, José
Rino, José
https://www.ciencia-id.pt/A117-FBDB-A27B
A117-FBDB-A27B
http://orcid.org/0000-0002-0637-4527
0000-0002-0637-4527
Carvalho, Célia
Carvalho, Célia
https://www.ciencia-id.pt/DD18-667D-59FE
DD18-667D-59FE
http://orcid.org/0000-0002-5980-595X
0000-0002-5980-595X
Kirchhausen, Tomas
Carmo-Fonseca, Maria
Carmo-Fonseca, Maria
https://www.ciencia-id.pt/B31F-0435-0753
B31F-0435-0753
http://orcid.org/0000-0002-3402-7143
0000-0002-3402-7143
publishDate 2013
publisher.none.fl_str_mv Elsevier
reponame_str Repositório da Universidade de Lisboa
repository_id_str urn:repositoryAcronym:ul
service_str_mv urn:repositoryAcronym:ul
spelling engElsevierpt_PTRemoval of introns from pre-messenger RNAs (pre-mRNAs) via splicing provides a versatile means of genetic regulation that is often disrupted in human diseases. To decipher how splicing occurs in real time, we directly examined with single-molecule sensitivity the kinetics of intron excision from pre-mRNA in the nucleus of living human cells. By using two different RNA labeling methods, MS2 and λN, we show that β-globin introns are transcribed and excised in 20-30 s. Furthermore, we show that replacing the weak polypyrimidine (Py) tract in mouse immunoglobulin μ (IgM) pre-mRNA by a U-rich Py decreases the intron lifetime, thus providing direct evidence that splice-site strength influences splicing kinetics. We also found that RNA polymerase II transcribes at elongation rates ranging between 3 and 6 kb min(-1) and that transcription can be rate limiting for splicing. These results have important implications for a mechanistic understanding of cotranscriptional splicing regulation in the live-cell context.application/pdfpt_PTLive-cell visualization of pre-mRNA splicing with single-molecule sensitivityPersonalMartin, Robert M.DSpacehttp://dspace.org/items/d50e7a9a-5216-4738-a5c6-94c8c0b85a1dDSpacehttp://dspace.org/items/d50e7a9a-5216-4738-a5c6-94c8c0b85a1dMartinRobert ManfredCiência IDhttps://www.ciencia-id.pt7516-6C51-460BORCIDhttp://orcid.org0000-0001-5600-7525PersonalRino, JoséDSpacehttp://dspace.org/items/54f3b487-a7a1-4597-aa2e-65f660855937DSpacehttp://dspace.org/items/54f3b487-a7a1-4597-aa2e-65f660855937Rino HenriquesJosé MiguelCiência IDhttps://www.ciencia-id.ptA117-FBDB-A27BORCIDhttp://orcid.org0000-0002-0637-4527PersonalCarvalho, CéliaDSpacehttp://dspace.org/items/0bc60872-4f9a-44d0-9bd6-13c82c3298c2DSpacehttp://dspace.org/items/0bc60872-4f9a-44d0-9bd6-13c82c3298c2CarvalhoCéliaCiência IDhttps://www.ciencia-id.ptDD18-667D-59FEORCIDhttp://orcid.org0000-0002-5980-595XKirchhausen, TomasPersonalCarmo-Fonseca, MariaDSpacehttp://dspace.org/items/f4cae50c-2389-4b6a-8e3a-8fd8e538add0DSpacehttp://dspace.org/items/f4cae50c-2389-4b6a-8e3a-8fd8e538add0Carmo-FonsecaMariaCiência IDhttps://www.ciencia-id.ptB31F-0435-0753ORCIDhttp://orcid.org0000-0002-3402-7143Scopus Author IDhttps://www.scopus.com7007128195HostingInstitutionOrganizationalRepositório Científico de Acesso Aberto da ULisboae-mailmailto:repositorio@reitoria.ulisboa.ptrepositorio@reitoria.ulisboa.ptISSNIsPartOf2211-1247DOIIsPartOf10.1016/j.celrep.2013.08.0132021-12-03T15:47:59Z20132013-01-01T00:00:00ZHandlehttp://hdl.handle.net/10451/50271http://purl.org/coar/access_right/c_abf2open access3725795 bytesFundação para a Ciência e a TecnologiaSplicing and stochasticity in programmed cell death decisions3599-PPCDTCrossref Funder IDhttp://doi.org/10.13039/501100001871Fundação para a Ciência e a TecnologiaA SYNTHETIC BIOLOGY APPROACH TO STUDY SPLICING REGULATIONCrossref Funder IDhttp://doi.org/10.13039/501100001871literaturehttp://purl.org/coar/resource_type/c_6501journal article2013http://creativecommons.org/licenses/by-nc-nd/4.0/http://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://repositorio.ulisboa.pt/bitstreams/89050d87-edce-4cff-9c64-ce570af648f4/downloadCell Reports4611441155
spellingShingle Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
Martin, Robert M.
status SINGLETON
title Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
title_full Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
title_fullStr Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
title_full_unstemmed Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
title_short Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
title_sort Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity
url http://hdl.handle.net/10451/50271
visible 1