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eIF3 interacts with histone H4 messenger RNA to regulate its translation

In eukaryotes, various alternative translation initiation mechanisms have been unveiled for the translation of specific mRNAs. Some do not conform to the conventional scanning-initiation model. Translation initiation of histone H4 mRNA combines both canonical (cap-dependent) and viral initiation str...

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Autores principales: Hayek, Hassan, Gross, Lauriane, Janvier, Aurélie, Schaeffer, Laure, Martin, Franck, Eriani, Gilbert, Allmang, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8102920/
https://www.ncbi.nlm.nih.gov/pubmed/33766559
http://dx.doi.org/10.1016/j.jbc.2021.100578
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author Hayek, Hassan
Gross, Lauriane
Janvier, Aurélie
Schaeffer, Laure
Martin, Franck
Eriani, Gilbert
Allmang, Christine
author_facet Hayek, Hassan
Gross, Lauriane
Janvier, Aurélie
Schaeffer, Laure
Martin, Franck
Eriani, Gilbert
Allmang, Christine
author_sort Hayek, Hassan
collection PubMed
description In eukaryotes, various alternative translation initiation mechanisms have been unveiled for the translation of specific mRNAs. Some do not conform to the conventional scanning-initiation model. Translation initiation of histone H4 mRNA combines both canonical (cap-dependent) and viral initiation strategies (no-scanning, internal recruitment of initiation factors). Specific H4 mRNA structures tether the translation machinery directly onto the initiation codon and allow massive production of histone H4 during the S phase of the cell cycle. The human eukaryotic translation initiation factor 3 (eIF3), composed of 13 subunits (a-m), was shown to selectively recruit and control the expression of several cellular mRNAs. Whether eIF3 mediates H4 mRNA translation remains to be elucidated. Here, we report that eIF3 binds to a stem-loop structure (eIF3-BS) located in the coding region of H4 mRNA. Combining cross-linking and ribonucleoprotein immunoprecipitation experiments in vivo and in vitro, we also found that eIF3 binds to H1, H2A, H2B, and H3 histone mRNAs. We identified direct contacts between eIF3c, d, e, g subunits, and histone mRNAs but observed distinct interaction patterns to each histone mRNA. Our results show that eIF3 depletion in vivo reduces histone mRNA binding and modulates histone neosynthesis, suggesting that synthesis of histones is sensitive to the levels of eIF3. Thus, we provide evidence that eIF3 acts as a regulator of histone translation.
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spelling pubmed-81029202021-05-14 eIF3 interacts with histone H4 messenger RNA to regulate its translation Hayek, Hassan Gross, Lauriane Janvier, Aurélie Schaeffer, Laure Martin, Franck Eriani, Gilbert Allmang, Christine J Biol Chem Research Article In eukaryotes, various alternative translation initiation mechanisms have been unveiled for the translation of specific mRNAs. Some do not conform to the conventional scanning-initiation model. Translation initiation of histone H4 mRNA combines both canonical (cap-dependent) and viral initiation strategies (no-scanning, internal recruitment of initiation factors). Specific H4 mRNA structures tether the translation machinery directly onto the initiation codon and allow massive production of histone H4 during the S phase of the cell cycle. The human eukaryotic translation initiation factor 3 (eIF3), composed of 13 subunits (a-m), was shown to selectively recruit and control the expression of several cellular mRNAs. Whether eIF3 mediates H4 mRNA translation remains to be elucidated. Here, we report that eIF3 binds to a stem-loop structure (eIF3-BS) located in the coding region of H4 mRNA. Combining cross-linking and ribonucleoprotein immunoprecipitation experiments in vivo and in vitro, we also found that eIF3 binds to H1, H2A, H2B, and H3 histone mRNAs. We identified direct contacts between eIF3c, d, e, g subunits, and histone mRNAs but observed distinct interaction patterns to each histone mRNA. Our results show that eIF3 depletion in vivo reduces histone mRNA binding and modulates histone neosynthesis, suggesting that synthesis of histones is sensitive to the levels of eIF3. Thus, we provide evidence that eIF3 acts as a regulator of histone translation. American Society for Biochemistry and Molecular Biology 2021-03-23 /pmc/articles/PMC8102920/ /pubmed/33766559 http://dx.doi.org/10.1016/j.jbc.2021.100578 Text en © 2021 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Research Article
Hayek, Hassan
Gross, Lauriane
Janvier, Aurélie
Schaeffer, Laure
Martin, Franck
Eriani, Gilbert
Allmang, Christine
eIF3 interacts with histone H4 messenger RNA to regulate its translation
title eIF3 interacts with histone H4 messenger RNA to regulate its translation
title_full eIF3 interacts with histone H4 messenger RNA to regulate its translation
title_fullStr eIF3 interacts with histone H4 messenger RNA to regulate its translation
title_full_unstemmed eIF3 interacts with histone H4 messenger RNA to regulate its translation
title_short eIF3 interacts with histone H4 messenger RNA to regulate its translation
title_sort eif3 interacts with histone h4 messenger rna to regulate its translation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8102920/
https://www.ncbi.nlm.nih.gov/pubmed/33766559
http://dx.doi.org/10.1016/j.jbc.2021.100578
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