Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis

Trovero Martínez, María Fernanda - Rodríguez-Casuriaga, Rosana - Romeo, Carlos - Santiñaque, Federico - François, Mateo - Folle Ungo, Gustavo A. - Benavente, Ricardo - Sotelo Silveira, José Roberto - Geisinger Wschebor, Adriana

Resumen:

The discovery of a large number of long noncoding RNAs (lncRNAs), and the finding that they may play key roles in different biological processes, have started to provide a new perspective in the understanding of gene regulation. It has been shown that the testes express the highest amount of lncRNAs among different vertebrate tissues. However, although some studies have addressed the characterization of lncRNAs along spermatogenesis, an exhaustive analysis of the differential expression of lncRNAs at its different stages is still lacking. Here, we present the results for lncRNA transcriptome profiling along mouse spermatogenesis, employing highly pure flow sorted spermatogenic stage-specific cell populations, strand-specific RNAseq, and a combination of up-to-date bioinformatic pipelines for analysis. We found that the vast majority of testicular lncRNA genes are expressed at post-meiotic stages (i.e. spermiogenesis), which are characterized by extensive post-transcriptional regulation. LncRNAs at different spermatogenic stages shared common traits in terms of transcript length, exon number, and biotypes. Most lncRNAs were lincRNAs, followed by a high representation of antisense (AS) lncRNAs. Co-expression analyses showed a high correlation along the different spermatogenic stage transitions between the expression patterns of AS lncRNAs and their overlapping protein-coding genes, raising possible clues about lncRNA-related regulatory mechanisms. Interestingly, we observed the colocalization of an AS lncRNA and its host sense mRNA in the chromatoid body, a round spermatidsspecific organelle that has been proposed as a reservoir of RNA-related regulatory machinery. An additional, intriguing observation is the almost complete lack of detectable expression for Y-linked testicular lncRNAs, despite that a high number of lncRNA genes are annotated for this chromosome


Detalles Bibliográficos
2020
LncRNAs
Spermatogenesis
Testis
RNAseq
Transcriptome
Inglés
Universidad de la República
COLIBRI
https://hdl.handle.net/20.500.12008/31651
Acceso abierto
Licencia Creative Commons Atribución (CC - By 4.0)
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author Trovero Martínez, María Fernanda
author2 Rodríguez-Casuriaga, Rosana
Romeo, Carlos
Santiñaque, Federico
François, Mateo
Folle Ungo, Gustavo A.
Benavente, Ricardo
Sotelo Silveira, José Roberto
Geisinger Wschebor, Adriana
author2_role author
author
author
author
author
author
author
author
author_facet Trovero Martínez, María Fernanda
Rodríguez-Casuriaga, Rosana
Romeo, Carlos
Santiñaque, Federico
François, Mateo
Folle Ungo, Gustavo A.
Benavente, Ricardo
Sotelo Silveira, José Roberto
Geisinger Wschebor, Adriana
author_role author
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collection COLIBRI
dc.contributor.filiacion.none.fl_str_mv Trovero Martínez María Fernanda, IIBCE
Rodríguez-Casuriaga Rosana, IIBCE
Romeo Carlos, IIBCE
Santiñaque Federico, IIBCE
François Mateo, IIBCE
Folle Ungo Gustavo A., IIBCE
Benavente Ricardo
Sotelo Silveira José Roberto, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Geisinger Wschebor Adriana, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
dc.creator.none.fl_str_mv Trovero Martínez, María Fernanda
Rodríguez-Casuriaga, Rosana
Romeo, Carlos
Santiñaque, Federico
François, Mateo
Folle Ungo, Gustavo A.
Benavente, Ricardo
Sotelo Silveira, José Roberto
Geisinger Wschebor, Adriana
dc.date.accessioned.none.fl_str_mv 2022-05-25T12:47:03Z
dc.date.available.none.fl_str_mv 2022-05-25T12:47:03Z
dc.date.issued.none.fl_str_mv 2020
dc.description.abstract.none.fl_txt_mv The discovery of a large number of long noncoding RNAs (lncRNAs), and the finding that they may play key roles in different biological processes, have started to provide a new perspective in the understanding of gene regulation. It has been shown that the testes express the highest amount of lncRNAs among different vertebrate tissues. However, although some studies have addressed the characterization of lncRNAs along spermatogenesis, an exhaustive analysis of the differential expression of lncRNAs at its different stages is still lacking. Here, we present the results for lncRNA transcriptome profiling along mouse spermatogenesis, employing highly pure flow sorted spermatogenic stage-specific cell populations, strand-specific RNAseq, and a combination of up-to-date bioinformatic pipelines for analysis. We found that the vast majority of testicular lncRNA genes are expressed at post-meiotic stages (i.e. spermiogenesis), which are characterized by extensive post-transcriptional regulation. LncRNAs at different spermatogenic stages shared common traits in terms of transcript length, exon number, and biotypes. Most lncRNAs were lincRNAs, followed by a high representation of antisense (AS) lncRNAs. Co-expression analyses showed a high correlation along the different spermatogenic stage transitions between the expression patterns of AS lncRNAs and their overlapping protein-coding genes, raising possible clues about lncRNA-related regulatory mechanisms. Interestingly, we observed the colocalization of an AS lncRNA and its host sense mRNA in the chromatoid body, a round spermatidsspecific organelle that has been proposed as a reservoir of RNA-related regulatory machinery. An additional, intriguing observation is the almost complete lack of detectable expression for Y-linked testicular lncRNAs, despite that a high number of lncRNA genes are annotated for this chromosome
dc.format.extent.es.fl_str_mv 17 h.
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dc.identifier.citation.es.fl_str_mv Trovero Martínez, M, Rodríguez-Casuriaga, R, Romeo, C, [y otros] "Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis". RNA Biology. [en línea] 2020, 17(3): 350-365. 17 h. DOI: 10.1080/15476286.2019.1700332
dc.identifier.doi.none.fl_str_mv 10.1080/15476286.2019.1700332
dc.identifier.issn.none.fl_str_mv 1555-8584
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12008/31651
dc.language.iso.none.fl_str_mv en
eng
dc.publisher.es.fl_str_mv Taylor and Francis
dc.relation.ispartof.es.fl_str_mv RNA Biology, 2020, 17(3): 350-365
dc.rights.license.none.fl_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.none.fl_str_mv reponame:COLIBRI
instname:Universidad de la República
instacron:Universidad de la República
dc.subject.es.fl_str_mv LncRNAs
Spermatogenesis
Testis
RNAseq
Transcriptome
dc.title.none.fl_str_mv Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
dc.type.es.fl_str_mv Artículo
dc.type.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description The discovery of a large number of long noncoding RNAs (lncRNAs), and the finding that they may play key roles in different biological processes, have started to provide a new perspective in the understanding of gene regulation. It has been shown that the testes express the highest amount of lncRNAs among different vertebrate tissues. However, although some studies have addressed the characterization of lncRNAs along spermatogenesis, an exhaustive analysis of the differential expression of lncRNAs at its different stages is still lacking. Here, we present the results for lncRNA transcriptome profiling along mouse spermatogenesis, employing highly pure flow sorted spermatogenic stage-specific cell populations, strand-specific RNAseq, and a combination of up-to-date bioinformatic pipelines for analysis. We found that the vast majority of testicular lncRNA genes are expressed at post-meiotic stages (i.e. spermiogenesis), which are characterized by extensive post-transcriptional regulation. LncRNAs at different spermatogenic stages shared common traits in terms of transcript length, exon number, and biotypes. Most lncRNAs were lincRNAs, followed by a high representation of antisense (AS) lncRNAs. Co-expression analyses showed a high correlation along the different spermatogenic stage transitions between the expression patterns of AS lncRNAs and their overlapping protein-coding genes, raising possible clues about lncRNA-related regulatory mechanisms. Interestingly, we observed the colocalization of an AS lncRNA and its host sense mRNA in the chromatoid body, a round spermatidsspecific organelle that has been proposed as a reservoir of RNA-related regulatory machinery. An additional, intriguing observation is the almost complete lack of detectable expression for Y-linked testicular lncRNAs, despite that a high number of lncRNA genes are annotated for this chromosome
eu_rights_str_mv openAccess
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identifier_str_mv Trovero Martínez, M, Rodríguez-Casuriaga, R, Romeo, C, [y otros] "Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis". RNA Biology. [en línea] 2020, 17(3): 350-365. 17 h. DOI: 10.1080/15476286.2019.1700332
1555-8584
10.1080/15476286.2019.1700332
instacron_str Universidad de la República
institution Universidad de la República
instname_str Universidad de la República
language eng
language_invalid_str_mv en
network_acronym_str COLIBRI
network_name_str COLIBRI
oai_identifier_str oai:colibri.udelar.edu.uy:20.500.12008/31651
publishDate 2020
reponame_str COLIBRI
repository.mail.fl_str_mv mabel.seroubian@seciu.edu.uy
repository.name.fl_str_mv COLIBRI - Universidad de la República
repository_id_str 4771
rights_invalid_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
spelling Trovero Martínez María Fernanda, IIBCERodríguez-Casuriaga Rosana, IIBCERomeo Carlos, IIBCESantiñaque Federico, IIBCEFrançois Mateo, IIBCEFolle Ungo Gustavo A., IIBCEBenavente RicardoSotelo Silveira José Roberto, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Geisinger Wschebor Adriana, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.2022-05-25T12:47:03Z2022-05-25T12:47:03Z2020Trovero Martínez, M, Rodríguez-Casuriaga, R, Romeo, C, [y otros] "Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis". RNA Biology. [en línea] 2020, 17(3): 350-365. 17 h. DOI: 10.1080/15476286.2019.17003321555-8584https://hdl.handle.net/20.500.12008/3165110.1080/15476286.2019.1700332The discovery of a large number of long noncoding RNAs (lncRNAs), and the finding that they may play key roles in different biological processes, have started to provide a new perspective in the understanding of gene regulation. It has been shown that the testes express the highest amount of lncRNAs among different vertebrate tissues. However, although some studies have addressed the characterization of lncRNAs along spermatogenesis, an exhaustive analysis of the differential expression of lncRNAs at its different stages is still lacking. Here, we present the results for lncRNA transcriptome profiling along mouse spermatogenesis, employing highly pure flow sorted spermatogenic stage-specific cell populations, strand-specific RNAseq, and a combination of up-to-date bioinformatic pipelines for analysis. We found that the vast majority of testicular lncRNA genes are expressed at post-meiotic stages (i.e. spermiogenesis), which are characterized by extensive post-transcriptional regulation. LncRNAs at different spermatogenic stages shared common traits in terms of transcript length, exon number, and biotypes. Most lncRNAs were lincRNAs, followed by a high representation of antisense (AS) lncRNAs. Co-expression analyses showed a high correlation along the different spermatogenic stage transitions between the expression patterns of AS lncRNAs and their overlapping protein-coding genes, raising possible clues about lncRNA-related regulatory mechanisms. Interestingly, we observed the colocalization of an AS lncRNA and its host sense mRNA in the chromatoid body, a round spermatidsspecific organelle that has been proposed as a reservoir of RNA-related regulatory machinery. An additional, intriguing observation is the almost complete lack of detectable expression for Y-linked testicular lncRNAs, despite that a high number of lncRNA genes are annotated for this chromosomeSubmitted by Verdun Juan Pablo (jverdun@fcien.edu.uy) on 2022-05-24T22:40:12Z No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 10.108015476286.2019.1700332.pdf: 5577681 bytes, checksum: 8d25ccb626a04a607bffe970fde9bf7f (MD5)Approved for entry into archive by Faget Cecilia (lfaget@fcien.edu.uy) on 2022-05-25T12:06:19Z (GMT) No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 10.108015476286.2019.1700332.pdf: 5577681 bytes, checksum: 8d25ccb626a04a607bffe970fde9bf7f (MD5)Made available in DSpace by Luna Fabiana (fabiana.luna@seciu.edu.uy) on 2022-05-25T12:47:03Z (GMT). No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 10.108015476286.2019.1700332.pdf: 5577681 bytes, checksum: 8d25ccb626a04a607bffe970fde9bf7f (MD5) Previous issue date: 202017 h.application/pdfenengTaylor and FrancisRNA Biology, 2020, 17(3): 350-365Las obras depositadas en el Repositorio se rigen por la Ordenanza de los Derechos de la Propiedad Intelectual de la Universidad de la República.(Res. Nº 91 de C.D.C. de 8/III/1994 – D.O. 7/IV/1994) y por la Ordenanza del Repositorio Abierto de la Universidad de la República (Res. Nº 16 de C.D.C. de 07/10/2014)info:eu-repo/semantics/openAccessLicencia Creative Commons Atribución (CC - By 4.0)LncRNAsSpermatogenesisTestisRNAseqTranscriptomeRevealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesisArtículoinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionreponame:COLIBRIinstname:Universidad de la Repúblicainstacron:Universidad de la RepúblicaTrovero Martínez, María FernandaRodríguez-Casuriaga, RosanaRomeo, CarlosSantiñaque, FedericoFrançois, MateoFolle Ungo, Gustavo A.Benavente, RicardoSotelo Silveira, José RobertoGeisinger Wschebor, AdrianaLICENSElicense.txtlicense.txttext/plain; charset=utf-84267http://localhost:8080/xmlui/bitstream/20.500.12008/31651/5/license.txt6429389a7df7277b72b7924fdc7d47a9MD55CC-LICENSElicense_urllicense_urltext/plain; charset=utf-844http://localhost:8080/xmlui/bitstream/20.500.12008/31651/2/license_urla0ebbeafb9d2ec7cbb19d7137ebc392cMD52license_textlicense_texttext/html; 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- Universidad de la Repúblicafalse
spellingShingle Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
Trovero Martínez, María Fernanda
LncRNAs
Spermatogenesis
Testis
RNAseq
Transcriptome
status_str publishedVersion
title Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
title_full Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
title_fullStr Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
title_full_unstemmed Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
title_short Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
title_sort Revealing stage-specific expression patterns of long noncoding RNAs along mouse spermatogenesis
topic LncRNAs
Spermatogenesis
Testis
RNAseq
Transcriptome
url https://hdl.handle.net/20.500.12008/31651