Developmental RNA-Seq transcriptomics of haploid germ cells and spermatozoa uncovers novel pathways associated with teleost spermiogenesis

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  • dc.contributor.author Castro-Arnau, Júlia
  • dc.contributor.author Chauvigné, François
  • dc.contributor.author Gómez-Garrido, Jèssica
  • dc.contributor.author Esteve-Codina, Anna
  • dc.contributor.author Dabad, Marc
  • dc.contributor.author Alioto, Tyler
  • dc.contributor.author Finn, Roderick Nigel
  • dc.contributor.author Cerdà, Joan
  • dc.date.accessioned 2022-11-08T07:13:09Z
  • dc.date.available 2022-11-08T07:13:09Z
  • dc.date.issued 2022
  • dc.description.abstract In non-mammalian vertebrates, the molecular mechanisms involved in the transformation of haploid germ cells (HGCs) into spermatozoa (spermiogenesis) are largely unknown. Here, we investigated this process in the marine teleost gilthead seabream (Sparus aurata) through the examination of the changes in the transcriptome between cell-sorted HGCs and ejaculated sperm (SPZEJ). Samples were collected under strict quality controls employing immunofluorescence microscopy as well as by determining the sperm motion kinematic parameters by computer-assisted sperm analysis. Deep sequencing by RNA-seq identified a total of 7286 differentially expressed genes (DEGs) (p-value < 0.01) between both cell types, of which nearly half were upregulated in SPZEJ compared to HCGs. In addition, approximately 9000 long non-coding RNAs (lncRNAs) were found, of which 56% were accumulated or emerged de novo in SPZEJ. The upregulated transcripts are involved in transcriptional and translational regulation, chromatin and cytoskeleton organization, metabolic processes such as glycolysis and oxidative phosphorylation, and also include a number of ion and water channels, exchangers, transporters and receptors. Pathway analysis conducted on DEGs identified 37 different signaling pathways enriched in SPZEJ, including 13 receptor pathways, from which the most predominant correspond to the chemokine and cytokine, gonadotropin-releasing hormone receptor and platelet derived growth factor signaling pathways. Our data provide new insight into the mRNA and lncRNA cargos of teleost spermatozoa and uncover the possible involvement of novel endocrine mechanisms during the differentiation and maturation of spermatozoa.
  • dc.description.sponsorship This work was supported by the Spanish Ministry of Science and Innovation (MCIN/AEI/https://doi.org/10.13039/501100011033) and FEDER “A way of making Europe”, European Union, Grant no. AGL2016-76802-R (to J.C.). F.C. and J.C.A. were supported, respectively, by the “Ramon y Cajal” programe (RYC-2015-17103) and a predoctoral (BES-2017-080778) contract from Spanish MCIN. A.E.C. was funded by ISCIII/MCIN (PT17/0009/0019) and co-funded by FEDER, whereas R.N.F. was supported by the University of Bergen, Norway. We also acknowledge support of the Spanish MICIN through the Instituto de Salud Carlos III and to the EMBL partnership, the Centro de Excelencia Severo Ochoa, the Generalitat de Catalunya through the CERCA Programme, Departament de Salut and Departament d’Empresa i Coneixement, and funds from the European Regional Development Fund (Programa Operatiu FEDER de Catalunya 2014-2020) cofinanced by the Spanish MCIN (Programa Operativo FEDER Plurirregional de España (POPE) 2014-2020).
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Castro-Arnau J, Chauvigné F, Gómez-Garrido J, Esteve-Codina A, Dabad M, Alioto T, Finn RN, Cerdà J. Developmental RNA-Seq transcriptomics of haploid germ cells and spermatozoa uncovers novel pathways associated with teleost spermiogenesis. Sci Rep. 2022 Aug 19;12(1):14162. DOI: 10.1038/s41598-022-18422-2
  • dc.identifier.doi http://dx.doi.org/10.1038/s41598-022-18422-2
  • dc.identifier.issn 2045-2322
  • dc.identifier.uri http://hdl.handle.net/10230/54747
  • dc.language.iso eng
  • dc.publisher Nature Research
  • dc.relation.ispartof Sci Rep. 2022 Aug 19;12(1):14162
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/AGL2016-76802-R
  • dc.rights © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.keyword Reproductive biology
  • dc.subject.keyword Transcriptomics
  • dc.title Developmental RNA-Seq transcriptomics of haploid germ cells and spermatozoa uncovers novel pathways associated with teleost spermiogenesis
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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