Comparative transcriptomic analysis of human and Drosophila extracellular vesicles

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lefebvre, Fabio Alexis ^a,b   Benoit Bouvrette, Louis Philip ^a,b   Perras, Lilyanne ^a,b   Blanchet Cohen, Alexis ^a   Garnier, Delphine ^c,d   Rak, Janusz ^c   Lécuyer, Éric ^a,b,e  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MONTREAL CHILDREN S HOSPITAL   (Canada)

^d NANTES UNIVERSITY HOSPITAL   (France)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL NUCLEOLAR RNA; TRANSCRIPTOME;

ANIMAL; DROSOPHILA; EXOSOME; GENETICS; HUMAN; METABOLISM; SPECIES DIFFERENCE; ULTRASTRUCTURE;

ANIMALS; DROSOPHILA; EXTRACELLULAR VESICLES; HUMANS; RNA, SMALL NUCLEOLAR; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84974577198     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27680     Document Type: Article

References (89)

1. Tsui, N. B., Ng, E. K. & Lo, Y. M. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin Chem 48, 1647-1653 (2002).
2. Skog, J. et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10, 1470-1476, doi: ncb1800 10.1038/ncb1800 (2008).
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, 654-659, doi: ncb1596 10.1038/ncb1596 (2007).
4. Baj-Krzyworzeka, M. et al. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother 55, 808-818, doi: 10.1007/s00262-005-0075-9 (2006).
5. Raposo, G. & Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200, 373-383, doi: jcb.201211138 10.1083/jcb.201211138 (2013).
6. Muralidharan-Chari, V., Clancy, J. W., Sedgwick, A. & D'Souza-Schorey, C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123, 1603-1611, doi: 10.1242/jcs.064386 (2010).
7. Raposo, G. et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183, 1161-1172 (1996).
8. Al-Nedawi, K. et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10, 619-624, doi: ncb172510.1038/ncb1725 (2008).
9. Balaj, L. et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2, 180, doi: 10.1038/ncomms1180 (2011).
10. Crescitelli, R. et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2, doi: 10.3402/jev.v2i0.20677 20677 (2013).
11. Lasser, C. et al. RNA-containing exosomes in human nasal secretions. Am J Rhinol Allergy 25, 89-93, doi: 357310.2500/ ajra.2011.25.3573 (2011).
12. Kogure, T., Yan, I. K., Lin, W. L. & Patel, T. Extracellular Vesicle-Mediated Transfer of a Novel Long Noncoding RNA TUC339: A Mechanism of Intercellular Signaling in Human Hepatocellular Cancer. Genes Cancer 4, 261-272, doi: 10.1177/1947601913499020 (2013).
13. Zhang, L. et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature 527, 100-104, doi: 10.1038/nature15376 (2015).
14. Kogure, T., Lin, W. L., Yan, I. K., Braconi, C. & Patel, T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 54, 1237-1248, doi: 10.1002/hep.24504 (2011).
15. Bobrie, A. & Thery, C. Unraveling the physiological functions of exosome secretion by tumors. Oncoimmunology 2, e22565, doi: 10.4161/onci.225652012ONCOIMM0322 (2013).
16. Deregibus, M. C. et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110, 2440-2448, doi: blood-2007-03-07870910.1182/blood-2007-03-078709 (2007).
17. Sjostrom, A. E., Sandblad, L., Uhlin, B. E. & Wai, S. N. Membrane vesicle-mediated release of bacterial RNA. Sci Rep 5, 15329, doi: 10.1038/srep15329 (2015).
18. Bayer-Santos, E., Lima, F. M., Ruiz, J. C., Almeida, I. C. & da Silveira, J. F. Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol Biochem Parasitol 193, 71-74, doi: 10.1016/j.molbiopara.2014.02.004 (2014).
19. Peres da Silva, R. et al. Extracellular vesicle-mediated export of fungal RNA. Sci Rep 5, 7763, doi: 10.1038/srep07763 (2015).
20. Cody, N. A., Iampietro, C. & Lécuyer, E. The many functions of mRNA localization during normal development and disease: From pillar to post. WIREs Dev Biol, doi: 10.1002/wdev.113 (2013).
21. Lecuyer, E. et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187 (2007).
22. Beckett, K. et al. Drosophila S2 cells secrete wingless on exosome-like vesicles but the wingless gradient forms independently of exosomes. Traffic 14, 82-96, doi: 10.1111/tra.12016 (2012).
23. Gross, J. C., Chaudhary, V., Bartscherer, K. & Boutros, M. Active Wnt proteins are secreted on exosomes. Nat Cell Biol 14, 1036-1045, doi: ncb257410.1038/ncb2574 (2012).
24. Koppen, T. et al. Proteomics analyses of microvesicles released by Drosophila Kc167 and S2 cells. Proteomics 11, 4397-4410, doi: 10.1002/pmic.201000774 (2011).
25. Currie, J. D. & Rogers, S. L. Using the Drosophila melanogaster D17-c3 cell culture system to study cell motility. Nat Protoc 6, 1632-1641, doi: nprot.2011.39710.1038/nprot.2011.397 (2011).
26. Ui, K., Ueda, R. & Miyake, T. Cell lines from imaginal discs of Drosophila melanogaster. In Vitro Cell Dev Biol 23, 707-711 (1987).
27. Yanagawa, S., Lee, J. S. & Ishimoto, A. Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to wingless signaling. J Biol Chem 273, 32353-32359 (1998).
28. Cherbas, L. et al. The transcriptional diversity of 25 Drosophila cell lines. Genome Res 21, 301-314, doi: gr.112961.11010.1101/ gr.112961.110 (2011).
29. Ullrich, A. et al. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309, 418-425 (1984).
30. Ramaiahgari, S. C. et al. A 3D in vitro model of differentiated HepG2 cell spheroids with improved liver-like properties for repeated dose high-throughput toxicity studies. Arch Toxicol 88, 1083-1095, doi: 10.1007/s00204-014-1215-9 (2014).
31. Fevrier, B. & Raposo, G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16, 415-421, doi: 10.1016/j.ceb.2004.06.003 S0955067404000729 (2004).
32. Fertig, E. T., Gherghiceanu, M. & Popescu, L. M. Extracellular vesicles release by cardiac telocytes: electron microscopy and electron tomography. J Cell Mol Med 18, 1938-1943, doi: 10.1111/jcmm.12436 (2014).
33. Chevillet, J. R. et al. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA 111, 14888-14893, doi: 10.1073/pnas.1408301111 (2014).
34. Kibbe, W. A. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35, W43-46, doi: 10.1093/nar/gkm234 (2007).
35. Johnson, L. F., Levis, R., Abelson, H. T., Green, H. & Penman, S. Changes in RNA in relation to growth of the fibroblast. IV. Alterations in theproduction and processing of mRNA and rRNA in resting and growing cells. J Cell Biol 71, 933-938 (1976).
36. Li, M. et al. Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos Trans R Soc Lond B Biol Sci 369, doi: 10.1098/rstb.2013.0502 (2014).
37. Rosenbloom, K. R. et al. The UCSC Genome Browser database: 2015 update. Nucleic Acids Res 43, D670-681, doi: 10.1093/nar/ gku1177 (2015).
38. Nair, M. & Saxena, P. Recent patents on mesenchymal stem cell mediated therapy in inflammatory diseases. Recent Pat Inflamm Allergy Drug Discov 7, 105-113 (2013).
39. Lapidot, M. & Pilpel, Y. Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms. EMBO Rep 7, 1216-1222, doi: 10.1038/sj.embor.7400857 (2006).
40. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811, doi: 10.1038/35888 (1998).
41. Mayer, C., Schmitz, K. M., Li, J., Grummt, I. & Santoro, R. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22, 351-361, doi: 10.1016/j.molcel.2006.03.028 (2006).
42. Xue, S. & Barna, M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13, 355-369, doi: 10.1038/nrm3359 (2012).
43. Roy, A. M. et al. Upstream flanking sequences and transcription of SINEs. J Mol Biol 302, 17-25, doi: 10.1006/jmbi.2000.4027 (2000).
44. List, A. F. et al. Overexpression of the major vault transporter protein lung-resistance protein predicts treatment outcome in acute myeloid leukemia. Blood 87, 2464-2469 (1996).
45. Scheffer, G. L. et al. The drug resistance-related protein LRP is the human major vault protein. Nat Med 1, 578-582 (1995).
46. Mossink, M. H., van Zon, A., Scheper, R. J., Sonneveld, P. & Wiemer, E. A. Vaults: a ribonucleoprotein particle involved in drug resistance? Oncogene 22, 7458-7467, doi: 10.1038/sj.onc.1206947 (2003).
47. Kedersha, N. L. & Rome, L. H. Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J Cell Biol 103, 699-709 (1986).
48. Persson, H. et al. The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat Cell Biol 11, 1268-1271, doi: 10.1038/ncb1972 (2009).
49. McWilliam, H. et al. Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Res 41, W597-600, doi: 10.1093/nar/gkt376 (2013).
50. Altman, S. A view of RNase P. Mol Biosyst 3, 604-607, doi: 10.1039/b707850c (2007).
51. Schmitt, M. E. & Clayton, D. A. Yeast site-specific ribonucleoprotein endoribonuclease MRP contains an RNA component homologous to mammalian RNase MRP RNA and essential for cell viability. Genes Dev 6, 1975-1985 (1992).
52. Sauliere, J. et al. The exon junction complex differentially marks spliced junctions. Nat Struct Mol Biol 17, 1269-1271, doi: 10.1038/ nsmb.1890 (2010).
53. Ender, C. et al. A human snoRNA with microRNA-like functions. Mol Cell 32, 519-528, doi: 10.1016/j.molcel.2008.10.017 (2008).
54. Saraiya, A. A. & Wang, C. C. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4, e1000224, doi: 10.1371/ journal.ppat.1000224 (2008).
55. Martens-Uzunova, E. S., Olvedy, M. & Jenster, G. Beyond microRNA-novel RNAs derived from small non-coding RNA and their implication in cancer. Cancer Lett 340, 201-211, doi: 10.1016/j.canlet.2012.11.058 (2013).
56. Sharma, U. et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351, 391-396, doi: 10.1126/science.aad6780 (2016).
57. Vickers, K. C., Roteta, L. A., Hucheson-Dilks, H., Han, L. & Guo, Y. Mining diverse small RNA species in the deep transcriptome. Trends Biochem Sci 40, 4-7, doi: 10.1016/j.tibs.2014.10.009 (2015).
58. Mittelbrunn, M. & Sanchez-Madrid, F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13, 328-335, doi: 10.1038/nrm3335 (2012).
59. Tarailo-Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics Chapter 4, Unit 4 10, doi: 10.1002/0471250953.bi0410s25 (2009).
60. Levis, R. W., Ganesan, R., Houtchens, K., Tolar, L. A. & Sheen, F. M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75, 1083-1093 (1993).
61. Wright, W. E., Tesmer, V. M., Huffman, K. E., Levene, S. D. & Shay, J. W. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev 11, 2801-2809 (1997).
62. Ulaner, G. A., Hu, J. F., Vu, T. H., Giudice, L. C. & Hoffman, A. R. Telomerase activity in human development is regulated by human telomerase reverse transcriptase (hTERT) transcription and by alternate splicing of hTERT transcripts. Cancer Res 58, 4168-4172 (1998).
63. Fukuda, M. et al. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311, doi: 10.1038/36894 (1997).
64. Pardue, M. L. & DeBaryshe, P. G. Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu Rev Genet 37, 485-511, doi: 10.1146/annurev.genet.38.072902.093115 (2003).
65. Mason, J. M., Frydrychova, R. C. & Biessmann, H. Drosophila telomeres: an exception providing new insights. Bioessays 30, 25-37, doi: 10.1002/bies.20688 (2008).
66. Mason, J. M. & Biessmann, H. The unusual telomeres of Drosophila. Trends Genet 11, 58-62 (1995).
67. Shpiz, S., Kwon, D., Rozovsky, Y. & Kalmykova, A. rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus. Nucleic Acids Res 37, 268-278, doi: 10.1093/nar/gkn960 (2009).
68. Klenov, M. S. et al. Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. Nucleic Acids Res 35, 5430-5438, doi: 10.1093/nar/gkm576 (2007).
69. Vagin, V. V. et al. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320-324, doi: 10.1126/ science.1129333 (2006).
70. Saito, K. et al. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20, 2214-2222, doi: 10.1101/gad.1454806 (2006).
71. Bou-Abdallah, F. The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta 1800, 719-731, doi: 10.1016/j.bbagen.2010.03.021 (2010).
72. Choi, D. S. et al. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 11, 2745-2751, doi: 10.1002/pmic.201100022 (2011).
73. Conde-Vancells, J. et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 7, 5157-5166 (2008).
74. Graner, M. W. et al. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J 23, 1541-1557, doi: 10.1096/fj.08-122184 (2009).
75. Pan, B. T., Teng, K., Wu, C., Adam, M. & Johnstone, R. M. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101, 942-948 (1985).
76. Johnstone, R. M., Mathew, A., Mason, A. B. & Teng, K. Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J Cell Physiol 147, 27-36, doi: 10.1002/jcp.1041470105 (1991).
77. Miguet, L. et al. Proteomic analysis of malignant lymphocyte membrane microparticles using double ionization coverage optimization. Proteomics 6, 153-171, doi: 10.1002/pmic.200500133 (2006).
78. Kobayashi, H., Yamamoto, S., Maruo, T. & Murakami, F. Identification of a cis-acting element required for dendritic targeting of activity-regulated cytoskeleton-associated protein mRNA. Eur J Neurosci 22, 2977-2984, doi: 10.1111/j.1460-9568.2005.04508.x (2005).
79. Kawashima, T. et al. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci USA 106, 316-321, doi: 10.1073/pnas.0806518106 (2009).
80. Hu, Y. et al. An integrative approach to ortholog prediction for disease-focused and other functional studies. BMC Bioinformatics 12, 357, doi: 10.1186/1471-2105-12-357 (2011).
81. Batagov, A. O., Kuznetsov, V. A. & Kurochkin, I. V. Identification of nucleotide patterns enriched in secreted RNAs as putative cisacting elements targeting them to exosome nano-vesicles. BMC Genomics 12 Suppl 3, S18, doi: 10.1186/1471-2164-12-S3-S18 (2011).
82. Tomasoni, R. et al. SNAP-25 regulates spine formation through postsynaptic binding to p140Cap. Nat Commun 4, 2136, doi: 10.1038/ncomms3136 (2013).
83. Tweedie, S. et al. FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37, D555-559, doi: 10.1093/nar/ gkn788 (2009).
84. Martin, K. C. & Ephrussi, A. mRNA localization: gene expression in the spatial dimension. Cell 136, 719-730 (2009).
85. Binns, D. et al. QuickGO: a web-based tool for Gene Ontology searching. Bioinformatics 25, 3045-3046, doi: 10.1093/bioinformatics/ btp536 (2009).
86. Huntley, R. P. et al. The GOA database: gene Ontology annotation updates for 2015. Nucleic Acids Res 43, D1057-1063, doi: 10.1093/ nar/gku1113 (2015).
87. Greening, D. W., Xu, R., Ji, H., Tauro, B. J. & Simpson, R. J. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol Biol 1295, 179-209, doi: 10.1007/978-1-4939-2550-6-15 (2015).
88. Quail, M. A. et al. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 13, 341, doi: 10.1186/1471-2164-13-341 (2012).
89. Thery, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3, Unit 3 22, doi: 10.1002/0471143030.cb0322s30 (2006).