MicroRNA sequence codes for small extracellular vesicle release and cellular retention

Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression 1 – 3 . However, the mechanism by which miRNA...

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Vydáno v:	Nature (London) Ročník 601; číslo 7893; s. 446 - 451
Hlavní autoři:	Garcia-Martin, Ruben, Wang, Guoxiao, Brandão, Bruna B., Zanotto, Tamires M., Shah, Samah, Kumar Patel, Sandip, Schilling, Birgit, Kahn, C. Ronald
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London Nature Publishing Group UK 20.01.2022 Nature Publishing Group
Témata:	38/77 38/91 42/44 45/41 45/70 631/337/384/331 631/443/319 82/58 96/106 96/109 Adipocytes Adipocytes - cytology Cell Communication Cell interactions Clonal deletion Endothelium Endothelium - cytology Exosomes Exosomes - genetics Exosomes - metabolism Extracellular vesicles Extracellular Vesicles - genetics Extracellular Vesicles - metabolism Gene expression Humanities and Social Sciences Insertion Liver - cytology MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA multidisciplinary Muscles Muscles - cytology Retention Ribonucleic acid RNA RNA-binding protein Science Science (multidisciplinary) Secretion
ISSN:	0028-0836, 1476-4687, 1476-4687
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Abstract	Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression 1 – 3 . However, the mechanism by which miRNAs are sorted into exosomes/sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion of these CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies. MicroRNAs encode sorting sequences that determine whether they are secreted in exosomal vesicles to regulate gene expression in distant cells or retained in cells that produced them, with different sequences used by individual cell types.
AbstractList	Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression . However, the mechanism by which miRNAs are sorted into exosomes/sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion of these CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies. Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression1-3. However, the mechanism by which miRNAs are sorted into exosomes/ sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion ofthese CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies. Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression1-3. However, the mechanism by which miRNAs are sorted into exosomes/sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion of these CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies.Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression1-3. However, the mechanism by which miRNAs are sorted into exosomes/sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion of these CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies. Exosomes/small extracellular vesicles (sEV) provide a unique mode of cell-to-cell communication in which miRNAs produced and released from one cell are taken up by cells at a distance where they can lead to changes in gene expression1–3. However, the mechanism by which miRNAs get sorted into exosomes/sEV or retained in cells remains largely unknown. Here, we demonstrate that miRNAs possess sorting sequences that determine their sEV secretion or cellular retention and that different cell-types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell-type. Insertion or deletion of these CELLmotifs or EXOmotifs into a miRNA increases or decreases their retention in the cell of production or secretion into sEV/exosomes. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights in linking circulating exosomal miRNAs to tissue-of-origin, it also provides an approach to improved targeting in RNA-mediated therapies. Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released from one cell are taken up by cells at a distance where they can enact changes in gene expression 1 – 3 . However, the mechanism by which miRNAs are sorted into exosomes/sEVs or retained in cells remains largely unknown. Here we demonstrate that miRNAs possess sorting sequences that determine their secretion in sEVs (EXOmotifs) or cellular retention (CELLmotifs) and that different cell types, including white and brown adipocytes, endothelium, liver and muscle, make preferential use of specific sorting sequences, thus defining the sEV miRNA profile of that cell type. Insertion or deletion of these CELLmotifs or EXOmotifs in a miRNA increases or decreases retention in the cell of production or secretion into exosomes/sEVs. Two RNA-binding proteins, Alyref and Fus, are involved in the export of miRNAs carrying one of the strongest EXOmotifs, CGGGAG. Increased miRNA delivery mediated by EXOmotifs leads to enhanced inhibition of target genes in distant cells. Thus, this miRNA code not only provides important insights that link circulating exosomal miRNAs to tissues of origin, but also provides an approach for improved targeting in RNA-mediated therapies. MicroRNAs encode sorting sequences that determine whether they are secreted in exosomal vesicles to regulate gene expression in distant cells or retained in cells that produced them, with different sequences used by individual cell types.
Author	Zanotto, Tamires M. Garcia-Martin, Ruben Shah, Samah Schilling, Birgit Brandão, Bruna B. Kumar Patel, Sandip Kahn, C. Ronald Wang, Guoxiao
AuthorAffiliation	1 Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, Massachusetts 02215, USA 2 The Buck Institute for Research on Aging, Novato, California 94945, USA
AuthorAffiliation_xml	– name: 2 The Buck Institute for Research on Aging, Novato, California 94945, USA – name: 1 Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Author_xml	– sequence: 1 givenname: Ruben orcidid: 0000-0003-2049-4960 surname: Garcia-Martin fullname: Garcia-Martin, Ruben organization: Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School – sequence: 2 givenname: Guoxiao surname: Wang fullname: Wang, Guoxiao organization: Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School – sequence: 3 givenname: Bruna B. orcidid: 0000-0001-8762-6310 surname: Brandão fullname: Brandão, Bruna B. organization: Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School – sequence: 4 givenname: Tamires M. surname: Zanotto fullname: Zanotto, Tamires M. organization: Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School – sequence: 5 givenname: Samah surname: Shah fullname: Shah, Samah organization: The Buck Institute for Research on Aging – sequence: 6 givenname: Sandip orcidid: 0000-0002-0651-4438 surname: Kumar Patel fullname: Kumar Patel, Sandip organization: The Buck Institute for Research on Aging – sequence: 7 givenname: Birgit orcidid: 0000-0001-9907-2749 surname: Schilling fullname: Schilling, Birgit organization: The Buck Institute for Research on Aging – sequence: 8 givenname: C. Ronald orcidid: 0000-0002-7583-9228 surname: Kahn fullname: Kahn, C. Ronald email: c.ronald.kahn@joslin.harvard.edu organization: Section of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/34937935$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 RGM designed research, performed experiments and analyzed the data shown in Fig. 1–4 and Extended Data Fig. 1–10, and wrote the manuscript. GW helped with vector generations for miRNA overexpression shown in Fig. 3a–f and Extended Data Fig. 7–9. BBB helped with size exclusion chromatography experiments shown in Extended Data Fig. 6. TMZ helped with analysis of miRNA profiling and motifs shown in Fig. 1 and 2. SS, SKP and BS performed the proteomic study and its analysis shown in Fig.3g–j and Extended Data Fig.10a–c. CRK designed the research, wrote the manuscript, and supervised the project. Author contributions
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Snippet	Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released... Exosomes and other small extracellular vesicles (sEVs) provide a unique mode of cell-to-cell communication in which microRNAs (miRNAs) produced and released... Exosomes/small extracellular vesicles (sEV) provide a unique mode of cell-to-cell communication in which miRNAs produced and released from one cell are taken...
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SubjectTerms	38/77 38/91 42/44 45/41 45/70 631/337/384/331 631/443/319 82/58 96/106 96/109 Adipocytes Adipocytes - cytology Cell Communication Cell interactions Clonal deletion Endothelium Endothelium - cytology Exosomes Exosomes - genetics Exosomes - metabolism Extracellular vesicles Extracellular Vesicles - genetics Extracellular Vesicles - metabolism Gene expression Humanities and Social Sciences Insertion Liver - cytology MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA multidisciplinary Muscles Muscles - cytology Retention Ribonucleic acid RNA RNA-binding protein Science Science (multidisciplinary) Secretion
Title	MicroRNA sequence codes for small extracellular vesicle release and cellular retention
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