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Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction

Shurtleff, Matthew J, Temoche-Diaz, Morayma M, Karfilis, Kate V, Ri, Sayaka, Schekman, Randy·2016·eLife
DOI 10.7554/elife.19276PMC PMC5047747

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Abstract

Exosomes are small vesicles that are secreted from metazoan cells and may convey selected membrane proteins and small RNAs to target cells for the control of cell migration, development and metastasis. To study the mechanisms of RNA packaging into exosomes, we devised a purification scheme based on the membrane marker CD63 to isolate a single exosome species secreted from HEK293T cells. Using immunoisolated CD63-containing exosomes we identified a set of miRNAs that are highly enriched with respect to their cellular levels. To explore the biochemical requirements for exosome biogenesis and RNA packaging, we devised a cell-free reaction that recapitulates the species-selective enclosure of miR-223 in isolated membranes supplemented with cytosol. We found that the RNA-binding protein Y-box protein I (YBX1) binds to and is required for the sorting of miR-223 in the cell-free reaction. Furthermore, YBX1 serves an important role in the secretion of miRNAs in exosomes by HEK293T cells.

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Research works printed but not linked: 61

  1. Arroyo, 2011, Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma, PNAS, 108, 5003, 10.1073/pnas.1019055108 · DOI · Paper page
  2. Bailey, 2009, MEME SUITE: tools for motif discovery and searching, Nucleic Acids Research, 37, W202, 10.1093/nar/gkp335 · DOI · Paper page
  3. Bann, 2014, A murine retrovirus co-Opts YB-1, a translational regulator and stress granule-associated protein, to facilitate virus assembly, Journal of Virology, 88, 4434, 10.1128/JVI.02607-13 · DOI
  4. Blankenberg, 2010, Galaxy: a web-based genome analysis tool for experimentalists, Current Protocols in Molecular Biology, Chapter 19, 10.1002/0471142727.mb1910s89 · DOI
  5. Blenkiron, 2013, Links between the oncoprotein YB-1 and small non-coding RNAs in breast cancer, PLoS One, 8, e80171, 10.1371/journal.pone.0080171 · DOI
  6. Bobrie, 2012, Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation, Journal of Extracellular Vesicles, 1, 18397, 10.3402/jev.v1i0.18397 · DOI
  7. Booth, 2006, Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane, Journal of Cell Biology, 172, 923, 10.1083/jcb.200508014 · DOI
  8. Buschow, 2010, MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis, Immunology and Cell Biology, 88, 851, 10.1038/icb.2010.64 · DOI
  9. Cha, 2015, KRAS-dependent sorting of miRNA to exosomes, eLife, 4, e07197, 10.7554/eLife.07197 · DOI
  10. Chevillet, 2014, Quantitative and stoichiometric analysis of the microRNA content of exosomes, PNAS, 111, 14888, 10.1073/pnas.1408301111 · DOI
  11. Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annual Review of Cell and Developmental Biology, 30, 255, 10.1146/annurev-cellbio-101512-122326 · DOI · Paper page
  12. Cook, 2011, RBPDB: a database of RNA-binding specificities, Nucleic Acids Research, 39, D301, 10.1093/nar/gkq1069 · DOI · Paper page
  13. Eiring, 2010, miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts, Cell, 140, 652, 10.1016/j.cell.2010.01.007 · DOI
  14. Elkayam, 2012, The structure of human argonaute-2 in complex with miR-20a, Cell, 150, 100, 10.1016/j.cell.2012.05.017 · DOI
  15. Falguières, 2008, In vitro budding of intralumenal vesicles into late endosomes is regulated by Alix and Tsg101, Molecular Biology of the Cell, 19, 4942, 10.1091/mbc.E08-03-0239 · DOI
  16. Friedländer, 2012, miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades, Nucleic Acids Research, 40, 37, 10.1093/nar/gkr688 · DOI · Paper page
  17. Frye, 2009, Y-box protein-1 is actively secreted through a non-classical pathway and acts as an extracellular mitogen, EMBO Reports, 10, 783, 10.1038/embor.2009.81 · DOI
  18. Gagnon, 2014, Analysis of nuclear RNA interference in human cells by subcellular fractionation and Argonaute loading, Nature Protocols, 9, 2045, 10.1038/nprot.2014.135 · DOI
  19. Gallois-Montbrun, 2007, Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules, Journal of Virology, 81, 2165, 10.1128/JVI.02287-06 · DOI
  20. Gerstberger, 2014, A census of human RNA-binding proteins, Nature Reviews Genetics, 15, 829, 10.1038/nrg3813 · DOI · Paper page
  21. Giardine, 2005, Galaxy: a platform for interactive large-scale genome analysis, Genome Research, 15, 1451, 10.1101/gr.4086505 · DOI
  22. Gibbings, 2009, Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity, Nature Cell Biology, 11, 1143, 10.1038/ncb1929 · DOI
  23. Goecks, 2010, Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences, Genome Biology, 11, R86, 10.1186/gb-2010-11-8-r86 · DOI
  24. Goodarzi, 2015, Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement, Cell, 161, 790, 10.1016/j.cell.2015.02.053 · DOI · Paper page
  25. Goodier, 2007, LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex, Molecular and Cellular Biology, 27, 6469, 10.1128/MCB.00332-07 · DOI
  26. Guo, 2014, 3'-Biotin-tagged microRNA-27 does not associate with Argonaute proteins in cells, RNA, 20, 985, 10.1261/rna.045054.114 · DOI
  27. Ismail, 2013, Macrophage microvesicles induce macrophage differentiation and miR-223 transfer, Blood, 121, 984, 10.1182/blood-2011-08-374793 · DOI
  28. Janas, 2015, Mechanisms of RNA loading into exosomes, FEBS Letters, 589, 1391, 10.1016/j.febslet.2015.04.036 · DOI
  29. Kedersha, 2007, Mammalian stress granules and processing bodies, Methods in Enzymology, 431, 61, 10.1016/S0076-6879(07)31005-7 · DOI
  30. Larkin, 2007, Clustal W and Clustal X version 2.0, Bioinformatics, 23, 2947, 10.1093/bioinformatics/btm404 · DOI
  31. Li, 2013, Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity, Nature Immunology, 14, 793, 10.1038/ni.2647 · DOI
  32. Li, 2012, Expression of YB-1 enhances production of murine leukemia virus vectors by stabilizing genomic viral RNA, Protein & Cell, 3, 943, 10.1007/s13238-012-2090-x · DOI
  33. Liu, 2015, Noncoding RNAs that associate with YB-1 alter proliferation in prostate cancer cells, RNA, 21, 1159, 10.1261/rna.045559.114 · DOI
  34. Luberto, 2002, Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase, Journal of Biological Chemistry, 277, 41128, 10.1074/jbc.M206747200 · DOI
  35. Lyabin, 2014, YB-1 protein: functions and regulation, Wiley Interdisciplinary Reviews, 5, 95, 10.1002/wrna.1200 · DOI · Paper page
  36. MacRae, 2008, In vitro reconstitution of the human RISC-loading complex, PNAS, 105, 512, 10.1073/pnas.0710869105 · DOI
  37. Malhotra, 2013, Unconventional protein secretion: an evolving mechanism, The EMBO Journal, 32, 1660, 10.1038/emboj.2013.104 · DOI
  38. McKenzie, 2016, KRAS-MEK Signaling Controls Ago2 Sorting into Exosomes, Cell Reports, 15, 978, 10.1016/j.celrep.2016.03.085 · DOI
  39. Mitchell, 2008, Circulating microRNAs as stable blood-based markers for cancer detection, PNAS, 105, 10513, 10.1073/pnas.0804549105 · DOI · Paper page
  40. Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nature Communications, 2, 282, 10.1038/ncomms1285 · DOI
  41. Mu, 2013, YB-1 stabilizes HIV-1 genomic RNA and enhances viral production, Protein & Cell, 4, 591, 10.1007/s13238-013-3011-3 · DOI
  42. Nam, 2011, Molecular basis for interaction of let-7 microRNAs with Lin28, Cell, 147, 1080, 10.1016/j.cell.2011.10.020 · DOI
  43. Pegtel, 2010, Functional delivery of viral miRNAs via exosomes, PNAS, 107, 6328, 10.1073/pnas.0914843107 · DOI
  44. Rana, 2013, Exosomal tumor microRNA modulates premetastatic organ cells, Neoplasia, 15, 281, 10.1593/neo.122010 · DOI
  45. Rauen, 2009, YB-1 acts as a ligand for Notch-3 receptors and modulates receptor activation, Journal of Biological Chemistry, 284, 26928, 10.1074/jbc.M109.046599 · DOI
  46. Rous, 2002, Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes, Molecular Biology of the Cell, 13, 1071, 10.1091/mbc.01-08-0409 · DOI
  47. Schirle, 2012, The crystal structure of human Argonaute2, Science, 336, 1037, 10.1126/science.1221551 · DOI
  48. Skog, 2008, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers, Nature Cell Biology, 10, 1470, 10.1038/ncb1800 · DOI · Paper page
  49. Squadrito, 2014, Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells, Cell Reports, 8, 1432, 10.1016/j.celrep.2014.07.035 · DOI · Paper page
  50. Théry, 2011, Exosomes: secreted vesicles and intercellular communications, F1000 Biology Reports, 3, 15, 10.3410/B3-15 · DOI · Paper page
  51. Trajkovic, 2008, Ceramide triggers budding of exosome vesicles into multivesicular endosomes, Science, 319, 1244, 10.1126/science.1153124 · DOI
  52. Tran, 2009, Cargo sorting into multivesicular bodies in vitro, PNAS, 106, 17395, 10.1073/pnas.0909473106 · DOI
  53. Turchinovich, 2011, Characterization of extracellular circulating microRNA, Nucleic Acids Research, 39, 7223, 10.1093/nar/gkr254 · DOI · Paper page
  54. Tuschl, 1999, Targeted mRNA degradation by double-stranded RNA in vitro, Genes & Development, 13, 3191, 10.1101/gad.13.24.3191 · DOI
  55. Ung, 2014, Exosome proteomics reveals transcriptional regulator proteins with potential to mediate downstream pathways, Cancer Science, 105, 1384, 10.1111/cas.12534 · DOI
  56. Van Deun, 2014, The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling, Journal of Extracellular Vesicles, 3, 24858, 10.3402/jev.v3.24858 · DOI
  57. Villarroya-Beltri, 2013, Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs, Nature Communications, 4, 2980, 10.1038/ncomms3980 · DOI · Paper page
  58. Wang, 2013, A complex network of factors with overlapping affinities represses splicing through intronic elements, Nature Structural & Molecular Biology, 20, 36, 10.1038/nsmb.2459 · DOI
  59. Wei, 2012, YB-1 binds to CAUC motifs and stimulates exon inclusion by enhancing the recruitment of U2AF to weak polypyrimidine tracts, Nucleic Acids Research, 40, 8622, 10.1093/nar/gks579 · DOI · Paper page
  60. Yuyama, 2012, Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia, Journal of Biological Chemistry, 287, 10977, 10.1074/jbc.M111.324616 · DOI
  61. Zhang, 2013, Cell biology. Unconventional secretion, unconventional solutions, Science, 340, 559, 10.1126/science.1234740 · DOI

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Metadata

Authors
Shurtleff, M. J., Temoche-Diaz, M. M., Karfilis, K. V., Ri, S., & Schekman, R.
Affiliations
  • Department of Plant and Microbial Biology, University of California, Berkeley, United States
  • Institute of Molecular Biology, University of Oregon, Eugene, United States
  • Department of Molecular and Cellular Biology, Howard Hughes Medical Institute, University of California, Berkeley, United States
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2016-08-25
Volume
5
ISSN
2050-084X
DOI
10.7554/elife.19276
PMC
PMC5047747
Cited by
621
References
8
Language
en
Licence
Funders
Howard Hughes Medical Institute (Investigator)

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