Transposable element exonization generates a reservoir of evolving and functional protein isoforms

Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance...

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Published inCell Vol. 187; no. 26; pp. 7603 - 7620.e22
Main Authors Arribas, Yago A., Baudon, Blandine, Rotival, Maxime, Suárez, Guadalupe, Bonté, Pierre-Emmanuel, Casas, Vanessa, Roubert, Apollinaire, Klein, Paul, Bonnin, Elisa, Mchich, Basma, Legoix, Patricia, Baulande, Sylvain, Sadacca, Benjamin, Diharce, Julien, Waterfall, Joshua J., Etchebest, Catherine, Carrascal, Montserrat, Goudot, Christel, Quintana-Murci, Lluís, Burbage, Marianne, Merlotti, Antonela, Amigorena, Sebastian
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 26.12.2024
Elsevier
Subjects
Alternative Splicing - genetics
cryptic splice sites
DNA Transposable Elements - genetics
Evolution, Molecular
exon birth
Exons - genetics
Humans
Immunology
Life Sciences
natural selection
non-canonical proteome
protein evolution
protein isoforms
Protein Isoforms - genetics
Protein Isoforms - metabolism
protein structure
proteome
Proteomics
ribosome profiling
ribosomes
Ribosomes - metabolism
RNA Splice Sites - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
transcriptome
Transcriptome - genetics
transcriptomics
transposable elements
transposons
unannotated splicing
protein structure
ribosome profiling
protein evolution
protein isoforms
proteomics
non-canonical proteome
unannotated splicing
cryptic splice sites
transposable elements
exon birth
Protein structure
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Abstract Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance remains unclear. Here, we use transcriptome assembly, ribosome profiling, and proteomics to describe a population of 1,227 unannotated TE exonizing isoforms generated by mRNA splicing and recurrent in human populations. Despite being shorter and lowly expressed, these isoforms are shared between individuals and efficiently translated. Functional analyses show stable expression, specific cellular localization, and, in some cases, modified functions. Exonized TEs are rich in ancient genes, whereas the involved splice sites are recent and can be evolutionarily conserved. In addition, exonized TEs contribute to the secondary structure of the emerging isoforms, supporting their functional relevance. We conclude that TE-spliced isoforms represent a diversity reservoir of functional proteins on which natural selection can act. [Display omitted] •Transposable element (TE) exonization expands the diversity of the human proteome•TE-spliced isoforms can have distinct functions compared with canonical isoforms•Exonized TEs can be evolutionarily conserved and add young sequences to ancient genes•Exonized TEs contribute to the overall secondary structure of proteins Transposable element exonization by unannotated splicing events produces stable protein isoforms with acquired functions that are subject to evolutionary selection.
AbstractList Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance remains unclear. Here, we use transcriptome assembly, ribosome profiling, and proteomics to describe a population of 1,227 unannotated TE exonizing isoforms generated by mRNA splicing and recurrent in human populations. Despite being shorter and lowly expressed, these isoforms are shared between individuals and efficiently translated. Functional analyses show stable expression, specific cellular localization, and, in some cases, modified functions. Exonized TEs are rich in ancient genes, whereas the involved splice sites are recent and can be evolutionarily conserved. In addition, exonized TEs contribute to the secondary structure of the emerging isoforms, supporting their functional relevance. We conclude that TE-spliced isoforms represent a diversity reservoir of functional proteins on which natural selection can act.
Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance remains unclear. Here, we use transcriptome assembly, ribosome profiling, and proteomics to describe a population of 1,227 unannotated TE exonizing isoforms generated by mRNA splicing and recurrent in human populations. Despite being shorter and lowly expressed, these isoforms are shared between individuals and efficiently translated. Functional analyses show stable expression, specific cellular localization, and, in some cases, modified functions. Exonized TEs are rich in ancient genes, whereas the involved splice sites are recent and can be evolutionarily conserved. In addition, exonized TEs contribute to the secondary structure of the emerging isoforms, supporting their functional relevance. We conclude that TE-spliced isoforms represent a diversity reservoir of functional proteins on which natural selection can act. [Display omitted] •Transposable element (TE) exonization expands the diversity of the human proteome•TE-spliced isoforms can have distinct functions compared with canonical isoforms•Exonized TEs can be evolutionarily conserved and add young sequences to ancient genes•Exonized TEs contribute to the overall secondary structure of proteins Transposable element exonization by unannotated splicing events produces stable protein isoforms with acquired functions that are subject to evolutionary selection.
Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance remains unclear. Here, we use transcriptome assembly, ribosome profiling, and proteomics to describe a population of 1,227 unannotated TE exonizing isoforms generated by mRNA splicing and recurrent in human populations. Despite being shorter and lowly expressed, these isoforms are shared between individuals and efficiently translated. Functional analyses show stable expression, specific cellular localization, and, in some cases, modified functions. Exonized TEs are rich in ancient genes, whereas the involved splice sites are recent and can be evolutionarily conserved. In addition, exonized TEs contribute to the secondary structure of the emerging isoforms, supporting their functional relevance. We conclude that TE-spliced isoforms represent a diversity reservoir of functional proteins on which natural selection can act.Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses identified thousands of unannotated spliced transcripts with exonizing TEs, but their contribution to the proteome and biological relevance remains unclear. Here, we use transcriptome assembly, ribosome profiling, and proteomics to describe a population of 1,227 unannotated TE exonizing isoforms generated by mRNA splicing and recurrent in human populations. Despite being shorter and lowly expressed, these isoforms are shared between individuals and efficiently translated. Functional analyses show stable expression, specific cellular localization, and, in some cases, modified functions. Exonized TEs are rich in ancient genes, whereas the involved splice sites are recent and can be evolutionarily conserved. In addition, exonized TEs contribute to the secondary structure of the emerging isoforms, supporting their functional relevance. We conclude that TE-spliced isoforms represent a diversity reservoir of functional proteins on which natural selection can act.
Author Baudon, Blandine
Goudot, Christel
Waterfall, Joshua J.
Arribas, Yago A.
Roubert, Apollinaire
Bonté, Pierre-Emmanuel
Klein, Paul
Legoix, Patricia
Carrascal, Montserrat
Bonnin, Elisa
Mchich, Basma
Casas, Vanessa
Suárez, Guadalupe
Burbage, Marianne
Quintana-Murci, Lluís
Etchebest, Catherine
Diharce, Julien
Rotival, Maxime
Baulande, Sylvain
Amigorena, Sebastian
Merlotti, Antonela
Sadacca, Benjamin
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Issue 26
Keywords protein structure
ribosome profiling
protein evolution
protein isoforms
proteomics
non-canonical proteome
unannotated splicing
cryptic splice sites
transposable elements
exon birth
Protein structure
Language English
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Snippet Alternative splicing enhances protein diversity in different ways, including through exonization of transposable elements (TEs). Recent transcriptomic analyses...
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SubjectTerms Alternative Splicing - genetics
cryptic splice sites
DNA Transposable Elements - genetics
Evolution, Molecular
exon birth
Exons - genetics
Humans
Immunology
Life Sciences
natural selection
non-canonical proteome
protein evolution
protein isoforms
Protein Isoforms - genetics
Protein Isoforms - metabolism
protein structure
proteome
Proteomics
ribosome profiling
ribosomes
Ribosomes - metabolism
RNA Splice Sites - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
transcriptome
Transcriptome - genetics
transcriptomics
transposable elements
transposons
unannotated splicing
Title Transposable element exonization generates a reservoir of evolving and functional protein isoforms
URI https://dx.doi.org/10.1016/j.cell.2024.11.011
https://www.ncbi.nlm.nih.gov/pubmed/39667937
https://www.proquest.com/docview/3146663951
https://www.proquest.com/docview/3242050837
https://pasteur.hal.science/pasteur-04908000
Volume 187
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