"Small talk" in the innate immune system via RNA-containing extracellular vesicles

Frontiers in Immunology

Volumn 5, Issue OCT, 2014, Pages

  van der Grein, Susanne G ^a   Nolte 't Hoen, Esther N M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Exosomes; Extracellular vesicles; Infection; Innate immune system; MicroRNA

Indexed keywords

COMPLEMENT RECEPTOR; MICRORNA; SMALL UNTRANSLATED RNA; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TRANSFER RNA; VIRUS RNA;

B LYMPHOCYTE; CANCER CELL; CELL COMMUNICATION; CYTOKINE RELEASE; DENDRITIC CELL; EXOSOME; EXTRACELLULAR VESICLE; GENETIC REGULATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; REVIEW; T LYMPHOCYTE; TRANSPORT VESICLE; TRYPANOSOMA CRUZI;

EID: 84919430320     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00542     Document Type: Review

References (81)

1. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol (2009) 9(8):581-93. doi: 10.1038/nri2567
2. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol (2013) 200(4):373-83. doi:10.1083/jcb.201211138
3. EL Andaloussi S, Mager I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov (2013) 12(5):347-57. doi:10.1038/nrd3978
4. Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol (2014) 14(3):195-208. doi:10.1038/nri3622
5. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A (2004) 101(36):13368-73. doi:10.1073/pnas.0403453101
6. Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C. Exosomal-like vesicles are present in human blood plasma. Int Immunol (2005) 17(7):879-87. doi:10.1093/intimm/dxh267
7. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol (2007) 179(3):1969-78. doi:10.4049/jimmunol.179.3.1969
8. Nolte-'t Hoen EN, Wauben MH. Immune cell-derived vesicles: modulators and mediators of inflammation. Curr Pharm Des (2012) 18(16):2357-68. doi:10.2174/138161212800166013
9. Kowal J, Tkach M, Thery C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol (2014) 29C:116-25. doi:10.1016/j.ceb.2014.05.004
10. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med (1996) 183(3):1161-72. doi:10.1084/jem.183.3.1161
11. Pitt JM, Charrier M, Viaud S, Andre F, Besse B, Chaput N, et al. Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol (2014) 193(3):1006-11. doi:10.4049/jimmunol.1400703
12. Nieuwland R, Berckmans RJ, McGregor S, Boing AN, Romijn FP, Westendorp RG, et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood (2000) 95(3):930-5.
13. VanWijk MJ, Nieuwland R, Boer K, van der Post JA, VanBavel E, Sturk A. Microparticle subpopulations are increased in preeclampsia: possible involvement in vascular dysfunction? Am J Obstet Gynecol (2002) 187(2):450-6. doi:10.1067/mob.2002.124279
14. Xie J, Tato CM, Davis MM. How the immune system talks to itself: the varied role of synapses. Immunol Rev (2013) 251(1):65-79. doi:10.1111/imr.12017
15. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun (2011) 2:282. doi:10.1038/ncomms1285
16. Choudhuri K, Llodra J, Roth EW, Tsai J, Gordo S, Wucherpfennig KW, et al. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature (2014) 507(7490):118-23. doi:10.1038/nature12951
17. Buschow SI, Nolte-'t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic (2009) 10(10):1528-42. doi:10.1111/j.1600-0854.2009.00963.x
18. He T, Tang C, Liu Y, Ye Z, Wu X, Wei Y, et al. Bidirectional membrane molecule transfer between dendritic and T cells. Biochem Biophys Res Commun (2007) 359(2):202-8. doi:10.1016/j.bbrc.2007.05.099
19. Segura E, Guerin C, Hogg N, Amigorena S, Thery C. CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo. J Immunol (2007) 179(3):1489-96. doi:10.4049/jimmunol.179.3.1489
20. Nolte-'t Hoen EN, Buschow SI, Anderton SM, Stoorvogel W, Wauben MH. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood (2009) 113(9):1977-81. doi:10.1182/blood-2008-08-174094
21. Rana S, Yue S, Stadel D, Zoller M. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol (2012) 44(9):1574-84. doi:10.1016/j.biocel.2012.06.018
22. Saunderson SC, Dunn AC, Crocker PR, McLellan AD. CD169 mediates the capture of exosomes in spleen and lymph node. Blood (2014) 123(2):208-16. doi:10.1182/blood-2013-03-489732
23. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol (2001) 166(12):7309-18. doi:10.4049/jimmunol.166.12.7309
24. Papp K, Vegh P, Prechl J, Kerekes K, Kovacs J, Csikos G, et al. B lymphocytes and macrophages release cell membrane deposited C3-fragments on exosomes with T cell response-enhancing capacity. Mol Immunol (2008) 45(8):2343-51. doi:10.1016/j.molimm.2007.11.021
25. Naslund TI, Gehrmann U, Qazi KR, Karlsson MC, Gabrielsson S. Dendritic cell-derived exosomes need to activate both T and B cells to induce antitumor immunity. J Immunol (2013) 190(6):2712-9. doi:10.4049/jimmunol.1203082
26. Batagov AO, Kuznetsov VA, Kurochkin IV. Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics (2011) 12(Suppl 3):S18. doi:10.1186/1471-2164-12-S3-S18
27. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol (2007) 9(6):654-9. doi:10.1038/ncb1596
28. Ekstrom K, Valadi H, Sjostrand M, Malmhall C, Bossios A, Eldh M, 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. J Extracell Vesicles (2012) 1:18389. doi:10.3402/jev.v1i0.18389
29. Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics (2012) 13:357. doi:10.1186/1471-2164-13-357
30. Crescitelli R, Lasser C, Szabo TG, Kittel A, Eldh M, Dianzani I, et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles (2013) 2:20677. doi:10.3402/jev.v2i0.20677
31. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol (2009) 11(9):1143-9. doi:10.1038/ncb1929
32. Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res (2012) 40(21):10937-49. doi:10.1093/nar/gks832
33. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, et al. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol (2009) 11(9):1150-6. doi:10.1038/ncb1930
34. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun (2013) 4:2980. doi:10.1038/ncomms3980
35. Nolte-'t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH, 't Hoen PA. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res (2012) 40(18):9272-85. doi:10.1093/nar/gks658
36. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science (2007) 316(5830):1484-8. doi:10.1126/science.1138341
37. Persson H, Kvist A, Vallon-Christersson J, Medstrand P, Borg A, Rovira C. The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat Cell Biol (2009) 11(10):1268-71. doi:10.1038/ncb1972
38. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA (2010) 16(4):673-95. doi:10.1261/rna.2000810
39. Miranda KC, Bond DT, McKee M, Skog J, Paunescu TG, Da Silva N, et al. Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease. Kidney Int (2010) 78(2):191-9. doi:10.1038/ki.2010.106
40. Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics (2013) 14:319. doi:10.1186/1471-2164-14-319
41. Cech TR, Steitz JA. The noncoding RNA revolution-trashing old rules to forge new ones. Cell (2014) 157(1):77-94. doi:10.1016/j.cell.2014.03.008
42. Gezer U, Ozgur E, Cetinkaya M, Isin M, Dalay N. Long non-coding RNAs with low expression levels in cells are enriched in secreted exosomes. Cell Biol Int (2014) 38(9):1076-9. doi:10.1002/cbin.10301
43. Kogure T, Yan IK, Lin WL, Patel T. Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: a mechanism of intercellular signaling in human hepatocellular cancer. Genes Cancer (2013) 4(7-8):261-72. doi:10.1177/1947601913499020
44. Takahashi K, Yan IK, Kogure T, Haga H, Patel T. Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellular cancer. FEBS Open Bio (2014) 4:458-67. doi:10.1016/j.fob.2014.04.007
45. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood (2012) 119(3):756-66. doi:10.1182/blood-2011-02-338004
46. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood (2013) 121(6):984-95. doi:10.1182/blood-2011-08-374793
47. Beninson LA, Fleshner M. Exosomes: an emerging factor in stress-induced immunomodulation. Semin Immunol (2014). doi:10.1016/j.smim.2013.12.001
48. Carroll-Portillo A, Surviladze Z, Cambi A, Lidke DS, Wilson BS. Mast cell synapses and exosomes: membrane contacts for information exchange. Front Immunol (2012) 3:46. doi:10.3389/fimmu.2012.00046
49. Bhatnagar S, Shinagawa K, Castellino FJ, Schorey JS. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood (2007) 110(9):3234-44. doi:10.1182/blood-2007-03-079152
50. Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood (2004) 104(8):2543-8. doi:10.1182/blood-2004-01-0361
51. Eldh M, Ekstrom K, Valadi H, Sjostrand M, Olsson B, Jernas M, et al. Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS One (2010) 5(12):e15353. doi:10.1371/journal.pone.0015353
52. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell (2010) 39(1):133-44. doi:10.1016/j.molcel.2010.06.010
53. Li J, Zhang Y, Liu Y, Dai X, Li W, Cai X, et al. Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. J Biol Chem (2013) 288(32):23586-96. doi:10.1074/jbc. M113.489302
54. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature (2008) 451(7182):1125-9. doi:10.1038/nature06607
55. Sugatani T, Hruska KA. MicroRNA-223 is a key factor in osteoclast differentiation. J Cell Biochem (2007) 101(4):996-9. doi:10.1002/jcb.21335
56. Haneklaus M, Gerlic M, O'Neill LA, Masters SL. miR-223: infection, inflammation and cancer. J Intern Med (2013) 274(3):215-26. doi:10.1111/joim.12099
57. Aucher A, Rudnicka D, Davis DM. MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J Immunol (2013) 191(12):6250-60. doi:10.4049/jimmunol.1301728
58. Li D, Jia H, Zhang H, Lv M, Liu J, Zhang Y, et al. TLR4 signaling induces the release of microparticles by tumor cells that regulate inflammatory cytokine IL-6 of macrophages via microRNA let-7b. Oncoimmunology (2012) 1(5):687-93. doi:10.4161/onci.19854
59. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, et al. MicroRNAs bind to toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A (2012) 109(31):E2110-6. doi:10.1073/pnas.1209414109
60. Mobergslien A, Sioud M. Exosome-derived miRNAs and cellular miRNAs activate innate immunity. J Innate Immun (2014) 6(1):105-10. doi:10.1159/000351460
61. Sioud M, Furset G, Cekaite L. Suppression of immunostimulatory siRNA-driven innate immune activation by 2'-modified RNAs. Biochem Biophys Res Commun (2007) 361(1):122-6. doi:10.1016/j.bbrc.2007.06.177
62. Anand PK, Anand E, Bleck CK, Anes E, Griffiths G. Exosomal Hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS One (2010) 5(4):e10136. doi:10.1371/journal.pone.0010136
63. Wurdinger T, Gatson NN, Balaj L, Kaur B, Breakefield XO, Pegtel DM. Extracellular vesicles and their convergence with viral pathways. Adv Virol (2012) 2012:767694. doi:10.1155/2012/767694
64. Meckes DG Jr, Raab-Traub N. Microvesicles and viral infection. J Virol (2011) 85(24):12844-54. doi:10.1128/JVI.05853-11
65. Flanagan J, Middeldorp J, Sculley T. Localization of the Epstein-Barr virus protein LMP 1 to exosomes. J Gen Virol (2003) 84(Pt 7):1871-9. doi:10.1099/vir.0.18944-0
66. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A (2010) 107(14):6328-33. doi:10.1073/pnas.0914843107
67. Canitano A, Venturi G, Borghi M, Ammendolia MG, Fais S. Exosomes released in vitro from Epstein-Barr virus (EBV)-infected cells contain EBV-encoded latent phase mRNAs. Cancer Lett (2013) 337(2):193-9. doi:10.1016/j.canlet.2013.05.012
68. Gourzones C, Gelin A, Bombik I, Klibi J, Verillaud B, Guigay J, et al. Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J (2010) 7:271. doi:10.1186/1743-422X-7-271
69. Haneklaus M, Gerlic M, Kurowska-Stolarska M, Rainey AA, Pich D, McInnes IB, et al. Cutting edge: miR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1beta production. J Immunol (2012) 189(8):3795-9. doi:10.4049/jimmunol.1200312
70. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, Whitten-Bauer C, et al. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe (2012) 12(4):558-70. doi:10.1016/j.chom.2012.08.010
71. Wieland SF, Takahashi K, Boyd B, Whitten-Bauer C, Ngo N, de la Torre JC, et al. Human plasmacytoid dendritic cells sense lymphocytic choriomeningitis virus-infected cells in vitro. J Virol (2014) 88(1):752-7. doi:10.1128/JVI.01714-13
72. Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun (2012) 80(6):1948-57. doi:10.1128/IAI.06014-11
73. Barteneva NS, Maltsev N, Vorobjev IA. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol (2013) 3:49. doi:10.3389/fcimb.2013.00049
74. Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol (2010) 64:163-84. doi:10.1146/annurev.micro.091208.073413
75. Bayer-Santos E, Lima FM, Ruiz JC, Almeida IC, da Silveira JF. Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol Biochem Parasitol (2014) 193(2):71-4. doi:10.1016/j.molbiopara.2014.02.004
76. Garcia-Silva MR, das Neves RF, Cabrera-Cabrera F, Sanguinetti J, Medeiros LC, Robello C, et al. Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitol Res (2014) 113(1):285-304. doi:10.1007/s00436-013-3655-1
77. Raina M, Ibba M. tRNAs as regulators of biological processes. Front Genet (2014) 5:171. doi:10.3389/fgene.2014.00171
78. Garcia-Silva MR, Cabrera-Cabrera F, das Neves RF, Souto-Padron T, de Souza W, Cayota A. Gene expression changes induced by Trypanosoma cruzi shed microvesicles in mammalian host cells: relevance of tRNA-derived halves. Biomed Res Int (2014) 2014:305239. doi:10.1155/2014/305239
79. Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, et al. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res (2014) 42(11):7290-304. doi:10.1093/nar/gku347
80. Li CC, Eaton SA, Young PE, Lee M, Shuttleworth R, Humphreys DT, et al. Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol (2013) 10(8):1333-44. doi:10.4161/rna.25281
81. Hoy AM, Buck AH. Extracellular small RNAs: what, where, why? Biochem Soc Trans (2012) 40(4):886-90. doi:10.1042/BST20120019