The translation of non-canonical open reading frames controls mucosal immunity
The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-can...
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| Published in | Nature (London) Vol. 564; no. 7736; pp. 434 - 438 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.12.2018
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential
1
,
2
. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as ‘non-protein coding’. Although the idea that such non-canonical ORFs can encode functional proteins is controversial
3
,
4
, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF ‘hidden’ within the long non-coding RNA
Aw112010
is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease.
In mouse macrophages, a range of short and non-ATG-initiated open reading frames that can generate proteins are identified, one of which is shown to be essential for host immunity to enteric mucosal infection and inflammation. |
|---|---|
| AbstractList | The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential1,2. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial3,4, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease.The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential1,2. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial3,4, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease. The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential.sup.1,2. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial.sup.3,4, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease.In mouse macrophages, a range of short and non-ATG-initiated open reading frames that can generate proteins are identified, one of which is shown to be essential for host immunity to enteric mucosal infection and inflammation. The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential . Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial , we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease. The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential.sup.1,2. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial.sup.3,4, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease. The annotation of the mammalian protein coding genome is incomplete. Arbitrary open reading frame (ORF) size restriction and the absolute requirement for a methionine codon as the sole initiator of translation, have constrained identification of potentially important transcripts with non-canonical protein coding potential 1 , 2 . Using unbiased transcriptomic approaches in macrophages responding to bacterial infection, we show widespread ribosome association with a large number of RNAs that were previously annotated as “non-protein coding”. Although the ability of such non-canonical ORFs to encode functional protein is controversial 3 , 4 , we identify a plethora of novel short and non-ATG initiated ORFs with the ability to generate stable and spatially distinct proteins. Importantly, we show that the translation of a novel ORF ‘hidden’ within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. Together this work expands our interpretation of the protein coding genome and demonstrates the critical nature of proteinaceous products generated from non-canonical ORFs to the immune response in vivo . We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein coding genes in immunity and disease. The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential 1 , 2 . Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as ‘non-protein coding’. Although the idea that such non-canonical ORFs can encode functional proteins is controversial 3 , 4 , we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF ‘hidden’ within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from non-canonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease. In mouse macrophages, a range of short and non-ATG-initiated open reading frames that can generate proteins are identified, one of which is shown to be essential for host immunity to enteric mucosal infection and inflammation. The annotation of the mammalian protein-coding genome is incomplete. Arbitrary size restriction of open reading frames (ORFs) and the absolute requirement for a methionine codon as the sole initiator of translation have constrained the identification of potentially important transcripts with non-canonical protein-coding potential. Here, using unbiased transcriptomic approaches in macrophages that respond to bacterial infection, we show that ribosomes associate with a large number of RNAs that were previously annotated as 'non-protein coding'. Although the idea that such non-canonical ORFs can encode functional proteins is controversial, we identify a range of short and non-ATG-initiated ORFs that can generate stable and spatially distinct proteins. Notably, we show that the translation of a new ORF 'hidden' within the long non-coding RNA Aw112010 is essential for the orchestration of mucosal immunity during both bacterial infection and colitis. This work expands our interpretation of the protein-coding genome and demonstrates that proteinaceous products generated from noncanonical ORFs are crucial for the immune response in vivo. We therefore propose that the misannotation of non-canonical ORF-containing genes as non-coding RNAs may obscure the essential role of a multitude of previously undiscovered protein-coding genes in immunity and disease. |
| Audience | Academic |
| Author | Harman, Christian C. D. Kroehling, Lina Steach, Holly R. Flavell, Richard A. Jackson, Ruaidhrí Bailis, Will Solis, Angel G. Khitun, Alexandra Khan, Omair M. Skadow, Mathias H. York, Autumn G. Chang, Lelina Jarret, Abigail Duizer, Coco Slavoff, Sarah Brewer, J. Richard Bielecki, Piotr |
| AuthorAffiliation | 4 Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06529, United States 2 Department of Chemistry, Yale University, New Haven, Connecticut 06520, United States 3 Chemical Biology Institute, Yale University, West Haven, Connecticut 06516, United States 5 Howard Hughes Medical Institute, Yale University, New Haven, CT 06520, USA 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA |
| AuthorAffiliation_xml | – name: 4 Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06529, United States – name: 3 Chemical Biology Institute, Yale University, West Haven, Connecticut 06516, United States – name: 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA – name: 2 Department of Chemistry, Yale University, New Haven, Connecticut 06520, United States – name: 5 Howard Hughes Medical Institute, Yale University, New Haven, CT 06520, USA |
| Author_xml | – sequence: 1 givenname: Ruaidhrí surname: Jackson fullname: Jackson, Ruaidhrí organization: Department of Immunobiology, Yale University School of Medicine – sequence: 2 givenname: Lina surname: Kroehling fullname: Kroehling, Lina organization: Department of Immunobiology, Yale University School of Medicine – sequence: 3 givenname: Alexandra surname: Khitun fullname: Khitun, Alexandra organization: Department of Chemistry, Yale University – sequence: 4 givenname: Will surname: Bailis fullname: Bailis, Will organization: Department of Immunobiology, Yale University School of Medicine – sequence: 5 givenname: Abigail surname: Jarret fullname: Jarret, Abigail organization: Department of Immunobiology, Yale University School of Medicine – sequence: 6 givenname: Autumn G. surname: York fullname: York, Autumn G. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 7 givenname: Omair M. surname: Khan fullname: Khan, Omair M. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 8 givenname: J. Richard surname: Brewer fullname: Brewer, J. Richard organization: Department of Immunobiology, Yale University School of Medicine – sequence: 9 givenname: Mathias H. surname: Skadow fullname: Skadow, Mathias H. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 10 givenname: Coco surname: Duizer fullname: Duizer, Coco organization: Department of Immunobiology, Yale University School of Medicine – sequence: 11 givenname: Christian C. D. surname: Harman fullname: Harman, Christian C. D. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 12 givenname: Lelina surname: Chang fullname: Chang, Lelina organization: Department of Immunobiology, Yale University School of Medicine – sequence: 13 givenname: Piotr surname: Bielecki fullname: Bielecki, Piotr organization: Department of Immunobiology, Yale University School of Medicine – sequence: 14 givenname: Angel G. surname: Solis fullname: Solis, Angel G. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 15 givenname: Holly R. surname: Steach fullname: Steach, Holly R. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 16 givenname: Sarah surname: Slavoff fullname: Slavoff, Sarah organization: Department of Chemistry, Yale University, Chemical Biology Institute, Yale University, Department of Molecular Biophysics and Biochemistry, Yale University – sequence: 17 givenname: Richard A. surname: Flavell fullname: Flavell, Richard A. email: richard.flavell@yale.edu organization: Department of Immunobiology, Yale University School of Medicine, Howard Hughes Medical Institute, Yale University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30542152$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Springer Nature Limited 2018 COPYRIGHT 2018 Nature Publishing Group Copyright Nature Publishing Group Dec 20-Dec 27, 2018 |
| Copyright_xml | – notice: Springer Nature Limited 2018 – notice: COPYRIGHT 2018 Nature Publishing Group – notice: Copyright Nature Publishing Group Dec 20-Dec 27, 2018 |
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| DOI | 10.1038/s41586-018-0794-7 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 R.J. conceived the project, performed experiments, analyzed the data and wrote the manuscript. L.K. performed all bioinformatics analysis and aided in writing of the manuscript. A.K. preformed all the mass spectrometry experiments, analyzed data and aided in writing of the manuscript. W.B. performed experiments and contributed major conceptual insight into the work. A.J. and A.G.Y. participated in experimental design, conducted experiments, analyzed data and offered vital conceptual insight. O.M.K., J.R.B., M.H.S. and C.D. performed experiments and analyzed data. C.C.D.H. helped with bioinformatics analysis and provided helpful conceptual discussion. L.C., P.B., A.G.S. and H.R.S. helped with experiments. S.S. supervised all mass spectrometry work and contributed to the overall interpretation of this work. R.A.F. supervised the project, helped interpret the work and supervised writing of the manuscript. No author has a competing financial interest. Contributions |
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| Title | The translation of non-canonical open reading frames controls mucosal immunity |
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