Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs
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 doma...
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Online Access: | http://hdl.handle.net/10468/8769 https://doi.org/10.1016/j.jmb.2019.08.007 |
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ftunivcollcork:oai:cora.ucc.ie:10468/8769 2023-08-27T04:11:27+02:00 Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs Baclaocos, Janinah Santesmasses, Didac Mariotti, Marco Bierła, Katarzyna Vetick, Michael B. Lynch, Sharon McAllen, Rob Mackrill, John J. Loughran, Gary Guigó, Roderic Szpunar, Joanna Copeland, Paul R. Gladyshev, Vadim N. Atkins, John F. 2019-08-20 application/pdf application/vnd.openxmlformats-officedocument.spreadsheetml.sheet http://hdl.handle.net/10468/8769 https://doi.org/10.1016/j.jmb.2019.08.007 en eng Academic Press info:eu-repo/grantAgreement/SFI/SFI Investigator Programme/13/IA/1853/IE/Dynamic redefinition of codons: From antivirals to an essential micronutrient/ https://www.sciencedirect.com/science/article/pii/S0022283619305133?via%3Dihub Baclaocos, J., Santesmasses, D., Mariotti, M., Bierła, K., Vetick, M. B., Lynch, S., McAllen, R., Mackrill, J. J., Loughran, G., Guigó, R., Szpunar, J., Copeland, P. R., Gladyshev, V. N. and Atkins, J. F. (2019) 'Processive Recoding and Metazoan Evolution of Selenoprotein P: Up to 132 UGAs in Molluscs', Journal of Molecular Biology.,(27pp.) [In press] DOI:10.1016/j.jmb.2019.08.007 doi:10.1016/j.jmb.2019.08.007 1089-8638 27 0022-2836 Journal of Molecular Biology 1 http://hdl.handle.net/10468/8769 ©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/) http://creativecommons.org/licenses/by-nc-nd/4.0/ Selenoprotein Selenocysteine Recoding Dynamic redefinition Evolution Article (peer-reviewed) 2019 ftunivcollcork https://doi.org/10.1016/j.jmb.2019.08.007 2023-08-06T14:31:27Z 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. Article in Journal/Newspaper Pacific oyster University College Cork, Ireland: Cork Open Research Archive (CORA) Pacific Journal of Molecular Biology 431 22 4381 4407 |
institution |
Open Polar |
collection |
University College Cork, Ireland: Cork Open Research Archive (CORA) |
op_collection_id |
ftunivcollcork |
language |
English |
topic |
Selenoprotein Selenocysteine Recoding Dynamic redefinition Evolution |
spellingShingle |
Selenoprotein Selenocysteine Recoding Dynamic redefinition Evolution Baclaocos, Janinah Santesmasses, Didac Mariotti, Marco Bierła, Katarzyna Vetick, Michael B. Lynch, Sharon McAllen, Rob Mackrill, John J. Loughran, Gary Guigó, Roderic Szpunar, Joanna Copeland, Paul R. Gladyshev, Vadim N. Atkins, John F. Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
topic_facet |
Selenoprotein Selenocysteine Recoding Dynamic redefinition Evolution |
description |
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. |
format |
Article in Journal/Newspaper |
author |
Baclaocos, Janinah Santesmasses, Didac Mariotti, Marco Bierła, Katarzyna Vetick, Michael B. Lynch, Sharon McAllen, Rob Mackrill, John J. Loughran, Gary Guigó, Roderic Szpunar, Joanna Copeland, Paul R. Gladyshev, Vadim N. Atkins, John F. |
author_facet |
Baclaocos, Janinah Santesmasses, Didac Mariotti, Marco Bierła, Katarzyna Vetick, Michael B. Lynch, Sharon McAllen, Rob Mackrill, John J. Loughran, Gary Guigó, Roderic Szpunar, Joanna Copeland, Paul R. Gladyshev, Vadim N. Atkins, John F. |
author_sort |
Baclaocos, Janinah |
title |
Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
title_short |
Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
title_full |
Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
title_fullStr |
Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
title_full_unstemmed |
Processive recoding and metazoan evolution of selenoprotein P: Up to 132 UGAs in molluscs |
title_sort |
processive recoding and metazoan evolution of selenoprotein p: up to 132 ugas in molluscs |
publisher |
Academic Press |
publishDate |
2019 |
url |
http://hdl.handle.net/10468/8769 https://doi.org/10.1016/j.jmb.2019.08.007 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Pacific oyster |
genre_facet |
Pacific oyster |
op_relation |
info:eu-repo/grantAgreement/SFI/SFI Investigator Programme/13/IA/1853/IE/Dynamic redefinition of codons: From antivirals to an essential micronutrient/ https://www.sciencedirect.com/science/article/pii/S0022283619305133?via%3Dihub Baclaocos, J., Santesmasses, D., Mariotti, M., Bierła, K., Vetick, M. B., Lynch, S., McAllen, R., Mackrill, J. J., Loughran, G., Guigó, R., Szpunar, J., Copeland, P. R., Gladyshev, V. N. and Atkins, J. F. (2019) 'Processive Recoding and Metazoan Evolution of Selenoprotein P: Up to 132 UGAs in Molluscs', Journal of Molecular Biology.,(27pp.) [In press] DOI:10.1016/j.jmb.2019.08.007 doi:10.1016/j.jmb.2019.08.007 1089-8638 27 0022-2836 Journal of Molecular Biology 1 http://hdl.handle.net/10468/8769 |
op_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/) http://creativecommons.org/licenses/by-nc-nd/4.0/ |
op_doi |
https://doi.org/10.1016/j.jmb.2019.08.007 |
container_title |
Journal of Molecular Biology |
container_volume |
431 |
container_issue |
22 |
container_start_page |
4381 |
op_container_end_page |
4407 |
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1775354229681029120 |