Biogenesis, delivery, and function of extracellular RNA

The Extracellular RNA (exRNA) Communication Consortium was launched by the National Institutes of Health to focus on the extent to which RNA might function in a non-cell-autonomous manner. With the availability of increasingly sensitive tools, small amounts of RNA can be detected in serum, plasma, and other bodily fluids. The exact mechanism(s) by which RNA can be secreted from cells and the mechanisms for the delivery and uptake by recipient cells remain to be determined. This review will summarize current knowledge about the biogenesis and delivery of exRNA and outline projects seeking to understand the functional impact of exRNA.

[1]  B. Ganem RNA world , 1987, Nature.

[2]  Eric R Kandel,et al.  Local protein synthesis and its role in synapse-specific plasticity , 2000, Current Opinion in Neurobiology.

[3]  Craig P. Hunter,et al.  Systemic RNAi in C. elegans Requires the Putative Transmembrane Protein SID-1 , 2002, Science.

[4]  W. J. Lucas,et al.  A Systemic Small RNA Signaling System in Plants , 2004, The Plant Cell Online.

[5]  Lin He,et al.  MicroRNAs: small RNAs with a big role in gene regulation , 2004, Nature Reviews Genetics.

[6]  M. Ratajczak,et al.  Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes , 2006, Cancer Immunology, Immunotherapy.

[7]  G. Lachenal,et al.  Exosomes are released by cultured cortical neurones , 2006, Molecular and Cellular Neuroscience.

[8]  P. O’Farrell,et al.  The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing , 2006, Nature Cell Biology.

[9]  J. Lötvall,et al.  Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells , 2007, Nature Cell Biology.

[10]  J. Mattick,et al.  RNAs as extracellular signaling molecules. , 2008, Journal of molecular endocrinology.

[11]  Petra Schwille,et al.  Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes , 2008, Science.

[12]  G. van Meer,et al.  No ESCRTs for Exosomes , 2008, Science.

[13]  Qinxi Li,et al.  Axin determines cell fate by controlling the p53 activation threshold after DNA damage , 2009, Nature Cell Biology.

[14]  Daehee Hwang,et al.  Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells , 2009, BMC Genomics.

[15]  Graça Raposo,et al.  Exosomes--vesicular carriers for intercellular communication. , 2009, Current opinion in cell biology.

[16]  Kevin Kim,et al.  Silencing by small RNAs is linked to endosomal trafficking , 2009, Nature Cell Biology.

[17]  Y. Matsuki,et al.  Secretory Mechanisms and Intercellular Transfer of MicroRNAs in Living Cells*♦ , 2010, The Journal of Biological Chemistry.

[18]  Hamid Cheshmi Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers , 2011 .

[19]  C. Hunter,et al.  SID-1 is a dsRNA-selective dsRNA-gated channel. , 2011, RNA.

[20]  K. Vickers,et al.  MicroRNAs are Transported in Plasma and Delivered to Recipient Cells by High-Density Lipoproteins , 2011, Nature Cell Biology.

[21]  E. Kroh,et al.  Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma , 2011, Proceedings of the National Academy of Sciences.

[22]  G. Ayers,et al.  Amphiregulin Exosomes Increase Cancer Cell Invasion , 2011, Current Biology.

[23]  A. Aravin,et al.  PIWI-interacting small RNAs: the vanguard of genome defence , 2011, Nature Reviews Molecular Cell Biology.

[24]  Arsen O. Batagov,et al.  Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles , 2011, BMC Genomics.

[25]  Fátima Sánchez-Cabo,et al.  Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells , 2011, Nature communications.

[26]  Paulo P. Amaral,et al.  The Reality of Pervasive Transcription , 2011, PLoS biology.

[27]  Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. , 2012, Blood.

[28]  Roberta Galli,et al.  MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response , 2012, Proceedings of the National Academy of Sciences.

[29]  R. Coffey,et al.  Proteomic Analysis of Exosomes from Mutant KRAS Colon Cancer Cells Identifies Intercellular Transfer of Mutant KRAS* , 2012, Molecular & Cellular Proteomics.

[30]  Achilleas S. Frangakis,et al.  Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs , 2012, Nature Cell Biology.

[31]  P. Altevogt,et al.  Vesiclepedia: A Compendium for Extracellular Vesicles with Continuous Community Annotation , 2012, PLoS biology.

[32]  D. Teis,et al.  The ESCRT machinery , 2012, Current Biology.

[33]  H. Buermans,et al.  Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions , 2012, Nucleic acids research.

[34]  Jian-Bing Fan,et al.  miR-1289 and “Zipcode”-like Sequence Enrich mRNAs in Microvesicles , 2012, Molecular therapy. Nucleic acids.

[35]  Hadi Valadi,et al.  Characterization of mRNA and microRNA in human mast cell-derived exosomes and their transfer to other mast cells and blood CD34 progenitor cells , 2012, Journal of extracellular vesicles.

[36]  A. Hill,et al.  Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells , 2012, Nucleic acids research.

[37]  Howard Y. Chang,et al.  Genome regulation by long noncoding RNAs. , 2012, Annual review of biochemistry.

[38]  T. Jensen,et al.  Dealing with pervasive transcription. , 2013, Molecular cell.

[39]  Francesco Marabita,et al.  Intracellular Modulation, Extracellular Disposal and Serum Increase of MiR-150 Mark Lymphocyte Activation , 2013, PloS one.

[40]  Arsen O Batagov,et al.  Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3′-untranslated regions , 2013, Biology Direct.

[41]  Michael T. McManus,et al.  Pervasive Transcription of the Human Genome Produces Thousands of Previously Unidentified Long Intergenic Noncoding RNAs , 2013, PLoS genetics.

[42]  Thomas Tuschl,et al.  Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations , 2013, Proceedings of the National Academy of Sciences.

[43]  Stefan L Ameres,et al.  Diversifying microRNA sequence and function , 2013, Nature Reviews Molecular Cell Biology.

[44]  T. Okada,et al.  Ongoing activation of sphingosine 1-phosphate receptors mediates maturation of exosomal multivesicular endosomes , 2013, Nature Communications.

[45]  K. Sliwa,et al.  MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. , 2013, The Journal of clinical investigation.

[46]  Jun Lu,et al.  Antigen-specific, antibody-coated, exosome-like nanovesicles deliver suppressor T-cell microRNA-150 to effector T cells to inhibit contact sensitivity. , 2013, The Journal of allergy and clinical immunology.

[47]  Melissa G. Piper,et al.  Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. , 2013, Blood.

[48]  X. Chen,et al.  microRNAs are ligands of Toll-like receptors. , 2013, RNA.

[49]  F. Sánchez‐Madrid,et al.  Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs , 2013, Nature Communications.

[50]  Michael T. McManus,et al.  T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire , 2013, The Journal of experimental medicine.

[51]  Scott Kennedy,et al.  Endogenous Nuclear RNAi Mediates Behavioral Adaptation to Odor , 2013, Cell.

[52]  Yang Li,et al.  RNA Interference Functions as an Antiviral Immunity Mechanism in Mammals , 2013, Science.

[53]  Shinobu Ueda,et al.  Systemically Injected Exosomes Targeted to EGFR Deliver Antitumor MicroRNA to Breast Cancer Cells. , 2013, Molecular therapy : the journal of the American Society of Gene Therapy.

[54]  J. Lötvall,et al.  Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes , 2013, Journal of extracellular vesicles.

[55]  H. Cline,et al.  Exosomes function in cell–cell communication during brain circuit development , 2013, Current Opinion in Neurobiology.

[56]  D. Davis,et al.  MicroRNAs Transfer from Human Macrophages to Hepato-Carcinoma Cells and Inhibit Proliferation , 2013, The Journal of Immunology.

[57]  J. Rothstein,et al.  Neuronal Exosomal miRNA-dependent Translational Regulation of Astroglial Glutamate Transporter GLT1* , 2013, The Journal of Biological Chemistry.

[58]  George A Calin,et al.  Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. , 2014, Cancer cell.

[59]  H. Ishwaran,et al.  Exosome Transfer from Stromal to Breast Cancer Cells Regulates Therapy Resistance Pathways , 2014, Cell.

[60]  Mark Ibberson,et al.  Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. , 2014, Cell reports.

[61]  T. Ørntoft,et al.  Cellular disposal of miR23b by RAB27-dependent exosome release is linked to acquisition of metastatic properties. , 2014, Cancer research.

[62]  M. Cooperberg,et al.  miR-19, miR-345, miR-519c-5p Serum Levels Predict Adverse Pathology in Prostate Cancer Patients Eligible for Active Surveillance , 2014, PloS one.

[63]  Aaron N. Chang,et al.  MicroRNA-494 Within an Oncogenic MicroRNA Megacluster Regulates G1/S Transition in Liver Tumorigenesis Through Suppression of Mutated in Colorectal Cancer , 2013, Hepatology.

[64]  E. Marbán,et al.  Exosomes as Critical Agents of Cardiac Regeneration Triggered by Cell Therapy , 2014, Stem cell reports.

[65]  Weiying Zhou,et al.  Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. , 2014, Cancer cell.

[66]  G. Hartmann,et al.  Antiviral immunity via RIG-I-mediated recognition of RNA bearing 5′-diphosphates , 2014, Nature.

[67]  Muneesh Tewari,et al.  Quantitative and stoichiometric analysis of the microRNA content of exosomes , 2014, Proceedings of the National Academy of Sciences.

[68]  Isobel S Okoye,et al.  MicroRNA-Containing T-Regulatory-Cell-Derived Exosomes Suppress Pathogenic T Helper 1 Cells , 2014, Immunity.

[69]  C. Théry,et al.  Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. , 2014, Annual review of cell and developmental biology.

[70]  Isobel S Okoye,et al.  MicroRNA-Containing T-Regulatory-Cell-Derived Exosomes Suppress Pathogenic T Helper 1 Cells , 2014, Immunity.

[71]  D. Hall,et al.  C. elegans Ciliated Sensory Neurons Release Extracellular Vesicles that Function in Animal Communication , 2014, Current Biology.

[72]  B. Ylstra,et al.  Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. , 2014, Cell reports.

[73]  P. Robbins,et al.  Regulation of immune responses by extracellular vesicles , 2014, Nature Reviews Immunology.

[74]  Murray J. Cairns,et al.  Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons , 2014, Nucleic acids research.