Extracellular Vesicle RNA: A Universal Mediator of Microbial Communication?

Trends in Microbiology

Volumn 26, Issue 5, 2018, Pages 401-410

  Tsatsaronis, James A ^a,d   Franch Arroyo, Sandra ^a   Resch, Ulrike ^a   Charpentier, Emmanuelle ^a,b,c  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UMEÅ UNIVERSITY   (Sweden)

^c HUMBOLDT UNIVERSITY   (Germany)

^d UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

extracellular vesicles; gene silencing; OMV; RNA; TLR

Indexed keywords

CRYOPYRIN; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; RETINOIC ACID INDUCIBLE PROTEIN I; RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

BACTERIAL MEMBRANE; BACTERIUM; EXOSOME; FUNGUS; GENE CONTROL; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTIST; REVIEW; RNA TRANSPORT; TARGET CELL; ARCHAEON; CELL COMMUNICATION; EUKARYOTE; GENE SILENCING; METABOLISM; PHYSIOLOGY; PROKARYOTIC CELL;

ARCHAEA; CELL COMMUNICATION; EUKARYOTA; EXTRACELLULAR VESICLES; GENE EXPRESSION; GENE SILENCING; IMMUNITY, INNATE; PROKARYOTIC CELLS; RNA;

EID: 85043450331     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2018.02.009     Document Type: Review

References (65)

1. Cech, T.R., Steitz, J.A., The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157 (2014), 77–94.
2. Fritz, J.V., et al. Sources and functions of extracellular small RNAs in human circulation. Annu. Rev. Nutr. 36 (2016), 301–336.
3. Valadi, H., et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9 (2007), 654–659.
4. Yáñez-Mó M., et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 4, 2015, 27066.
5. Quinn, J.F., et al. Extracellular RNAs: development as biomarkers of human disease. J. Extracell. Vesicles, 4, 2015, 27495.
6. Ainsztein, A.M., et al. The NIH Extracellular RNA Communication Consortium. J. Extracell. Vesicles, 4, 2015, 27493.
7. Wang, K., et al. The complex exogenous RNA spectra in human plasma: an interface with human gut biota?. PLoS One, 7, 2012, e51009.
8. Hoy, A.M., et al. Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLOS Negl. Trop. Dis., 8, 2014, e2701.
9. Beatty, M., et al. Small RNAs from plants, bacteria and fungi within the order Hypocreales are ubiquitous in human plasma. BMC Genomics, 15, 2014, 933.
10. Colombo, M., et al. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289.
11. Brown, L., et al. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol. 13 (2015), 620–630.
12. Biller, S.J., et al. Bacterial vesicles in marine ecosystems. Science 343 (2014), 183–186.
13. Coakley, G., et al. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol. 31 (2015), 477–489.
14. Schwechheimer, C., Kuehn, M.J., Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13 (2015), 605–619.
15. Ellis, T.N., Kuehn, M.J., Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74 (2010), 81–94.
16. Deatherage, B.L., Cookson, B.T., Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 80 (2012), 1948–1957.
17. Mashburn, L.M., Whiteley, M., Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437 (2005), 422–425.
18. Acevedo, R., et al. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol., 5, 2014, 121.
19. Dorward, D.W., et al. Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 171 (1989), 2499–2505.
20. Yaron, S., et al. Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl. Environ. Microbiol. 66 (2000), 4414–4420.
21. Koeppen, K., et al. A novel mechanism of host–pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog., 12, 2016, e1005672.
22. Sjöström, A.E., et al. Membrane vesicle-mediated release of bacterial RNA. Sci. Rep., 5, 2015, 15329.
23. Rodriguez-Rodrigues, N., et al. Prokaryotic RNA associated to bacterial viability induces polymorphonuclear neutrophil activation. Front. Cell Infect. Microbiol., 7, 2017, 306.
24. Abdullah, Z., et al. RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 31 (2012), 4153–4164.
25. Kamm, R.C., Smith, A.G., Ribonuclease activity in human plasma. Clin. Biochem. 5 (1972), 198–200.
26. Blenkiron, C., et al. Uropathogenic Escherichia coli releases extracellular vesicles that are associated with RNA. PLoS One, 11, 2016, e0160440.
27. Resch, U., et al. A two-component regulatory system impacts extracellular membrane-derived vesicle production in group A Streptococcus. mBio, 7, 2016, e00207-16.
28. Ghosal, A., et al. The extracellular RNA complement of Escherichia coli. MicrobiologyOpen 4 (2015), 252–266.
29. Ho, M.-H., et al. Functional advantages of Porphyromonas gingivalis vesicles. PLoS One, 10, 2015, e0123448.
30. Peres da Silva, R., et al. Extracellular vesicle-mediated export of fungal RNA. Sci. Rep., 5, 2015, 7763.
31. Bayer-Santos, E., et al. Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol. Biochem. Parasitol. 193 (2014), 71–74.
32. T. Appl. Environ. Microbiol. 81 (2015), 4591–4599.
33. Abels, E.R., Breakefield, X.O., Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell. Mol. Neurobiol. 36 (2016), 301–312.
34. Batagov, A.O., et al. Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics, 12, 2011, S18.
35. McMahon, K.J., et al. Biogenesis of outer membrane vesicles in Serratia marcescens is thermoregulated and can be induced by activation of the Rcs phosphorelay system. J. Bacteriol. 194 (2012), 3241–3249.
36. Haurat, M.F., et al. Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 286 (2011), 1269–1276.
37. Bitto, N.J., et al. Bacterial membrane vesicles transport their DNA cargo into host cells. Sci. Rep., 7, 2017, 7072.
38. Buck, A.H., et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat. Commun., 5, 2014, 5488.
39. Lambertz, U., et al. Small RNAs derived from tRNAs and rRNAs are highly enriched in exosomes from both old and new world Leishmania providing evidence for conserved exosomal RNA packaging. BMC Genomics, 16, 2015, 151.
40. Garcia-Silva, M.R., et al. Hints of tRNA-derived small RNAs role in RNA silencing mechanisms. Genes 3 (2012), 603–614.
41. Hille, F., Charpentier, E., CRISPR-Cas: biology, mechanisms and relevance. Philos. Trans. R. Soc. Lond. B Biol. Sci., 371, 2016, 20150496.
42. Timmons, L., Fire, A., Specific interference by ingested dsRNA. Nature, 395, 1998, 854.
43. Liu, H., et al. Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat. Commun., 3, 2012, 1073.
44. Weiberg, A., et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342 (2013), 118–123.
45. Garcia-Silva, M.R., 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. 113 (2014), 285–304.
46. Garcia-Silva, M.R., et al. Gene expression changes induced by Trypanosoma cruzi shed microvesicles in mammalian host cells: relevance of tRNA-derived halves. BioMed Res. Int., 2014, 2014, e305239.
47. Choi, J.W., et al. Secretable small RNAs via outer membrane vesicles in periodontal pathogens. J. Dent. Res. 96 (2017), 458–466.
48. Eigenbrod, T., Dalpke, A.H., Bacterial RNA: an underestimated stimulus for innate immune responses. J. Immunol. 195 (2015), 411–418.
49. Biondo, C., et al. Recognition of fungal RNA by TLR7 has a nonredundant role in host defense against experimental candidiasis. Eur. J. Immunol. 42 (2012), 2632–2643.
50. Caetano, B.C., et al. Requirement of UNC93B1 reveals a critical role for Toll-like receptor 7 in host resistance to primary infection with Trypanosoma cruzi. J. Immunol. 187 (2011), 1903–1911.
51. Takeuchi, O., Akira, S., Pattern recognition receptors and inflammation. Cell 140 (2010), 805–820.
52. Brencicova, E., Diebold, S.S., Nucleic acids and endosomal pattern recognition: how to tell friend from foe?. Front. Cell Infect. Microbiol., 3, 2013, 37.
53. Kaparakis-Liaskos, M., Ferrero, R.L., Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol. 15 (2015), 375–387.
54. Choi, S.J., et al. Active immunization with extracellular vesicles derived from Staphylococcus aureus effectively protects against staphylococcal lung infections, mainly via Th1 cell-mediated immunity. PLoS One, 10, 2015, e0136021.
55. Sander, L.E., et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474 (2011), 385–389.
56. Pollak, C.N., et al. Outer membrane vesicles from Brucella abortus promote bacterial internalization by human monocytes and modulate their innate immune response. PLoS One, 7, 2012, e50214.
57. Winter, J., et al. Helicobacter pylori membrane vesicles stimulate innate pro- and anti-inflammatory responses and induce apoptosis in Jurkat T cells. Infect. Immun. 82 (2014), 1372–1381.
58. Vanaja, S.K., et al. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165 (2016), 1106–1119.
59. Shen, Y., et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12 (2012), 509–520.
60. McNab, F., et al. Type I interferons in infectious disease. Nat. Rev. Immunol. 15 (2015), 87–103.
61. Dauros Singorenko, P., et al. Isolation of membrane vesicles from prokaryotes: a technical and biological comparison reveals heterogeneity. J. Extracell. Vesicles, 6, 2017, 1324731.
62. Turnbull, L., et al. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat. Commun., 7, 2016, 11220.
63. Choi, J.-W., et al. Isolation and characterization of a microRNA-size secretable small RNA in Streptococcus sanguinis. Cell Biochem. Biophys., 45, 2016, 406.
64. Rayner, S., et al. Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis. Sci. Rep., 7, 2017, 39742.
65. Twu, O., et al. Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host∶ parasite interactions. PLoS Pathog., 9, 2013, e1003482.