Processive recoding and metazoan evolution of selenoprotein P: up to 132 UGAs in molluscs

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• dc.contributor.author Baclaocos, Janinah
• dc.contributor.author Santesmasses Ruiz, Didac, 1978-
• dc.contributor.author Mariotti, Marco, 1984-
• dc.contributor.author Bierla, Katarzyna
• dc.contributor.author Vetick, Michael B.
• dc.contributor.author Lynch, Sharon
• dc.contributor.author McAllen, Rob
• dc.contributor.author Mackrill, John J.
• dc.contributor.author Loughran, Gary
• dc.contributor.author Guigó Serra, Roderic
• dc.contributor.author Szpunar, Joanna
• dc.contributor.author Copeland, Paul R.
• dc.contributor.author Gladyshev, Vadim N.
• dc.contributor.author Atkins, John F.
• dc.date.accessioned 2019-10-09T07:51:37Z
• dc.date.available 2019-10-09T07:51:37Z
• dc.date.issued 2019
• dc.description.abstract Selenoproteins typically contain a single selenocysteine, the 21st amino acid, encoded by a context-redefined UGA. However, human selenoprotein P (SelenoP) has a redox-functioning selenocysteine in its N-terminal domain and nine selenium transporter-functioning selenocysteines in its C-terminal domain. Here we show that diverse SelenoP genes are present across metazoa with highly variable numbers of Sec-UGAs, ranging from a single UGA in certain insects, to 9 in common spider, and up to 132 in bivalve molluscs. SelenoP genes were shaped by a dynamic evolutionary process linked to selenium usage. Gene evolution featured modular expansions of an ancestral multi-Sec domain, which led to particularly Sec-rich SelenoP proteins in many aquatic organisms. We focused on molluscs, and chose Pacific oyster Magallana gigas as experimental model. We show that oyster SelenoP mRNA with 46 UGAs is translated full-length in vivo. Ribosome profiling indicates that selenocysteine specification occurs with ~5% efficiency at UGA1 and approaches 100% efficiency at distal 3' UGAs. We report genetic elements relevant to its expression, including a leader open reading frame and an RNA structure overlapping the initiation codon that modulates ribosome progression in a selenium-dependent manner. Unlike their mammalian counterparts, the two SECIS elements in oyster SelenoP (3'UTR recoding elements) do not show functional differentiation in vitro. Oysters can increase their tissue selenium level up to 50-fold upon supplementation, which also results in extensive changes in selenoprotein expression.
• dc.description.sponsorship The work was supported by the following grants: NIH DK117149, GM065204, and AG021518 (V.N.G.); BIO2014-57291-R from the Spanish Ministry of Economy and Competitiveness (R.G.), NIH GM077073 (P.R.C.), Science Foundation Ireland (13/IA/1853), and Irish Research Council (IRCLA/2019/74 n) (J.F.A).
• dc.format.mimetype application/pdf
• dc.identifier.citation Baclaocos J, Santesmasses D, Mariotti M, Bierła K, Vetick MB, Lynch S et al. Processive recoding and metazoan evolution of selenoprotein P: up to 132 UGAs in molluscs. J Mol Biol. 2019;431(22):4381-407. DOI: 10.1016/j.jmb.2019.08.007
• dc.identifier.doi http://dx.doi.org/10.1016/j.jmb.2019.08.007
• dc.identifier.issn 0022-2836
• dc.identifier.uri http://hdl.handle.net/10230/42414
• dc.language.iso eng
• dc.publisher Elsevier
• dc.relation.ispartof Journal of Molecular Biology. 2019;431(22):4381-407
• dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/BIO2014-57291-R
• dc.rights © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by-nc-nd/4.0/
• dc.subject.keyword Selenoprotein
• dc.subject.keyword Selenocysteine
• dc.subject.keyword Recoding
• dc.subject.keyword Dynamic redefinition
• dc.subject.keyword Evolution
• dc.title Processive recoding and metazoan evolution of selenoprotein P: up to 132 UGAs in molluscs
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion