Peptidomic discovery of short open reading frame–encoded peptides in human cells

The human genome contains stretches of DNA sequence with unknown function. Peptidomics coupled to RNA-Seq now reveals a class of short open reading frames in human genomes that are translated into small peptides. The complete extent to which the human genome is translated into polypeptides is of fun...

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Published in	Nature chemical biology Vol. 9; no. 1; pp. 59 - 64
Main Authors	Slavoff, Sarah A, Mitchell, Andrew J, Schwaid, Adam G, Cabili, Moran N, Ma, Jiao, Levin, Joshua Z, Karger, Amir D, Budnik, Bogdan A, Rinn, John L, Saghatelian, Alan
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.01.2013 Nature Publishing Group
Subjects	631/208/726/1912 631/92/475 Biochemical Engineering Biochemistry Bioorganic Chemistry Cell Biology Cellular biology Chemistry Chemistry/Food Science Codon Humans Mammals Open Reading Frames Peptides Peptides - chemistry Polypeptides Proteome Proteomics RNA, Messenger - genetics
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Abstract	The human genome contains stretches of DNA sequence with unknown function. Peptidomics coupled to RNA-Seq now reveals a class of short open reading frames in human genomes that are translated into small peptides. The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10–1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated.
AbstractList	The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10-1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated. The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10-1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated. [PUBLICATION ABSTRACT] The amount of the transcriptome that is translated into polypeptides is of fundamental importance. We developed a peptidomic strategy to detect short ORF (sORF)-encoded polypeptides (SEPs) in human cells. We identified 90 SEPs, 86 of which are novel, the largest number of human SEPs ever reported. SEP abundances range from 10-1000 molecules per cell, identical to known proteins. SEPs arise from sORFs in non-coding RNAs as well as multi-cistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that non-canonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8/1866) of long intergenic non-coding RNAs (lincRNAs). Together, these results provide the strongest evidence to date that the human proteome is more complex than previously appreciated. The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10-1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated.The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10-1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated. The human genome contains stretches of DNA sequence with unknown function. Peptidomics coupled to RNA-Seq now reveals a class of short open reading frames in human genomes that are translated into small peptides. The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short open reading frame (sORF)-encoded polypeptides (SEPs) in human cells. We identify 90 SEPs, 86 of which are previously uncharacterized, which is the largest number of human SEPs ever reported. SEP abundances range from 10–1,000 molecules per cell, identical to abundances of known proteins. SEPs arise from sORFs in noncoding RNAs as well as multicistronic mRNAs, and many SEPs initiate with non-AUG start codons, indicating that noncanonical translation may be more widespread in mammals than previously thought. In addition, coding sORFs are present in a small fraction (8 out of 1,866) of long intergenic noncoding RNAs. Together, these results provide strong evidence that the human proteome is more complex than previously appreciated.
Author	Saghatelian, Alan Levin, Joshua Z Ma, Jiao Mitchell, Andrew J Schwaid, Adam G Cabili, Moran N Rinn, John L Slavoff, Sarah A Karger, Amir D Budnik, Bogdan A
AuthorAffiliation	4 Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115, USA 8 Center of Systems Biology, Mass Spectrometry and Proteomics Lab, Faculty of Arts and Sciences, Harvard University, 52 Oxford St, Northwest Labs, B243.20, Cambridge, Massachusetts 02138, USA 7 Research Computing, Division of Science, Faculty of Arts and Sciences, Harvard University, 38 Oxford St, Room 211A, Cambridge, Massachusetts 02138, USA 1 Department of Chemistry and Chemical Biology, Harvard University, Cambridge, Massachusetts 02138, USA 5 Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA 3 Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA 6 Genome Sequencing & Analysis Program, Broad Institute of MIT and Harvard, 320 Charles Street, Cambridge, Massachusetts 02141, USA 2 Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA
AuthorAffiliation_xml	– name: 5 Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA – name: 2 Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA – name: 4 Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115, USA – name: 6 Genome Sequencing & Analysis Program, Broad Institute of MIT and Harvard, 320 Charles Street, Cambridge, Massachusetts 02141, USA – name: 7 Research Computing, Division of Science, Faculty of Arts and Sciences, Harvard University, 38 Oxford St, Room 211A, Cambridge, Massachusetts 02138, USA – name: 1 Department of Chemistry and Chemical Biology, Harvard University, Cambridge, Massachusetts 02138, USA – name: 3 Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA – name: 8 Center of Systems Biology, Mass Spectrometry and Proteomics Lab, Faculty of Arts and Sciences, Harvard University, 52 Oxford St, Northwest Labs, B243.20, Cambridge, Massachusetts 02138, USA
Author_xml	– sequence: 1 givenname: Sarah A surname: Slavoff fullname: Slavoff, Sarah A organization: Department of Chemistry and Chemical Biology, Harvard University – sequence: 2 givenname: Andrew J surname: Mitchell fullname: Mitchell, Andrew J organization: Department of Molecular and Cellular Biology, Harvard University – sequence: 3 givenname: Adam G surname: Schwaid fullname: Schwaid, Adam G organization: Department of Chemistry and Chemical Biology, Harvard University – sequence: 4 givenname: Moran N surname: Cabili fullname: Cabili, Moran N organization: Broad Institute of MIT and Harvard, Department of Systems Biology, Harvard Medical School, Department of Stem Cell and Regenerative Biology, Harvard University – sequence: 5 givenname: Jiao surname: Ma fullname: Ma, Jiao organization: Department of Chemistry and Chemical Biology, Harvard University – sequence: 6 givenname: Joshua Z surname: Levin fullname: Levin, Joshua Z organization: Genome Sequencing and Analysis Program, Broad Institute of MIT and Harvard – sequence: 7 givenname: Amir D surname: Karger fullname: Karger, Amir D organization: Division of Science, Research Computing, Faculty of Arts and Sciences, Harvard University – sequence: 8 givenname: Bogdan A surname: Budnik fullname: Budnik, Bogdan A organization: Center of Systems Biology, Mass Spectrometry and Proteomics Laboratory, Faculty of Arts and Sciences, Harvard University – sequence: 9 givenname: John L surname: Rinn fullname: Rinn, John L organization: Broad Institute of MIT and Harvard, Department of Stem Cell and Regenerative Biology, Harvard University – sequence: 10 givenname: Alan surname: Saghatelian fullname: Saghatelian, Alan email: saghatelian@chemistry.harvard.edu organization: Department of Chemistry and Chemical Biology, Harvard University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23160002$$D View this record in MEDLINE/PubMed
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Snippet	The human genome contains stretches of DNA sequence with unknown function. Peptidomics coupled to RNA-Seq now reveals a class of short open reading frames in... The complete extent to which the human genome is translated into polypeptides is of fundamental importance. We report a peptidomic strategy to detect short... The amount of the transcriptome that is translated into polypeptides is of fundamental importance. We developed a peptidomic strategy to detect short ORF...
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SubjectTerms	631/208/726/1912 631/92/475 Biochemical Engineering Biochemistry Bioorganic Chemistry Cell Biology Cellular biology Chemistry Chemistry/Food Science Codon Humans Mammals Open Reading Frames Peptides Peptides - chemistry Polypeptides Proteome Proteomics RNA, Messenger - genetics
Title	Peptidomic discovery of short open reading frame–encoded peptides in human cells
URI	https://link.springer.com/article/10.1038/nchembio.1120 https://www.ncbi.nlm.nih.gov/pubmed/23160002 https://www.proquest.com/docview/1284330594 https://www.proquest.com/docview/1239055765 https://pubmed.ncbi.nlm.nih.gov/PMC3625679
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