Assessment of small RNA sorting into different extracellular fractions revealed by high-throughput sequencing of breast cell lines

Nucleic Acids Research

Volumn 43, Issue 11, 2015, Pages 5601-5616

  Tosar, Juan Pablo ^a,b   Gámbaro, Fabiana ^a   Sanguinetti, Julia ^a   Bonilla, Braulio ^a   Witwer, Kenneth W ^c   Cayota, Alfonso ^a,d  

^a INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; PROTEIN S 100; RIBONUCLEOPROTEIN; TRANSFER RNA; GLUTAMIC ACID TRANSFER RNA; GLYCINE TRANSFER RNA; SMALL UNTRANSLATED RNA;

ARTICLE; BREAST CELL; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL ISOLATION; CELL VACUOLE; CELLULAR SECRETION; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIUM CELL; EXOSOME; EXTRACELLULAR SPACE; HIGH THROUGHPUT SEQUENCING; MOLECULAR LIBRARY; PRIORITY JOURNAL; RNA ANALYSIS; RNA EXTRACTION; BREAST TUMOR; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MCF 7 CELL LINE; METABOLISM; SECRETION (PROCESS); SEQUENCE ANALYSIS; TRANSPORT VESICLE; TUMOR CELL LINE; ULTRASTRUCTURE;

BREAST NEOPLASMS; CELL LINE, TUMOR; EXTRACELLULAR SPACE; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MCF-7 CELLS; MICRORNAS; RIBONUCLEOPROTEINS; RNA, SMALL UNTRANSLATED; RNA, TRANSFER, GLU; RNA, TRANSFER, GLY; SEQUENCE ANALYSIS, RNA; TRANSPORT VESICLES;

EID: 84936869846     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv432     Document Type: Article

References (60)

1. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J. and Lotvall, J.O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 9, 654-659.
2. Cortez, M.A., Bueso-Ramos, C., Ferdin, J., Lopez-Berestein, G., Sood, A.K. and Calin, G.A. (2011) MicroRNAs in body fuids-the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol., 8, 467-477.
3. Schwarzenbach, H., Nishida, N., Calin, G.A. and Pantel, K. (2014) Clinical relevance of circulating cell-free microRNAs in cancer. Nat. Rev. Clin. Oncol., 11, 145-156.
4. Mittelbrunn, M. and Sanchez-Madrid, F. (2012) Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell. Biol., 13, 328-335.
5. Arroyo, J.D., Chevillet, J.R., Kroh, E.M., Ruf, I.K., Pritchard, C.C., Gibson, D.F., Mitchell, P.S., Bennett, C.F., Pogosova-Agadjanyan, E.L., Stirewalt, D.L. et al. (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U.S.A., 108, 5003-5008.
6. Chevillet, J.R., Kang, Q., Ruf, I.K., Briggs, H.A., Vojtech, L.N., Hughes, S.M., Cheng, H.H., Arroyo, J.D., Meredith, E.K., Gallichotte, E.N. et al. (2014) Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc. Natl. Acad. Sci. U.S.A., 111, 14888-14893.
7. Turchinovich, A., Weiz, L., Langheinz, A. and Burwinkel, B. (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res., 39, 7223-7233.
8. Wang, K., Zhang, S., Weber, J., Baxter, D. and Galas, D.J. (2010) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res., 38, 7248-7259.
9. Vickers, K.C., Palmisano, B.T., Shoucri, B.M., Shamburek, R.D. and Remaley, A.T. (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol., 13, 423-433.
10. Gould, S.J. and Raposo, G. (2013) As we wait: coping with an imperfect nomenclature for extracellular vesicles. J. Extracell Vesicles, 2, doi:10.3402/jev.v2i0.20389.
11. Mathivanan, S., Ji, H. and Simpson, R.J. (2010) Exosomes: extracellular organelles important in intercellular communication. J. Proteomics, 73, 1907-1920.
12. Hristov, M., Erl, W., Linder, S. and Weber, P.C. (2004) Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood, 104, 2761-2766.
13. Nolte-'t Hoen, E.N., Buermans, H.P., Waasdorp, M., Stoorvogel, W., Wauben, M.H. and t Hoen, P.A. (2012) 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, 40, 9272-9285.
14. Turchinovich, A., Samatov, T.R., Tonevitsky, A.G. and Burwinkel, B. (2013) Circulating miRNAs: cell-cell communication function? Front. Genet., 4, 119.
15. Turchinovich, A., Weiz, L. and Burwinkel, B. (2012) Extracellular miRNAs: the mystery of their origin and function. Trends Biochem. Sci, 37, 460-465.
16. Li, Z., Ender, C, Meister, G., Moore, P.S., Chang, Y. and John, B. (2012) Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res., 40, 6787-6799.
17. Ivanov, P., Emara, M.M., Villen, J., Gygi, S.P and Anderson, P (2011) Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell, 43, 613-623.
18. Lee, Y.S., Shibata, Y, Malhotra, A. and Dutta, A. (2009) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev., 23, 2639-2649.
19. Anderson, P and Ivanov, P (2014) tRNA fragments in human health and disease. FEBS Lett., 588, 4297-4304.
20. Gebetsberger, J. and Polacek, N (2013) Slicing tRNAs to boost functional ncRNA diversity. RNA Biol, 10, 1798-1806.
21. Dhahbi, J.M., Spindler, S.R., Atamna, H., Boffelli, D. and Martin, D.I. (2014) Deep sequencing of serum small RNAs identifes patterns of 5' tRNA half and YRNA fragment expression associated with breast cancer. Biomark. Cancer, 6, 37-47.
22. Dhahbi, J.M., Spindler, S.R., Atamna, H., Yamakawa, A., Boffelli, D., Mote, P and Martin, D.I. (2013) 5' tRNA halves are present as abundant complexes in serum, concentrated in blood cells, and modulated by aging and calorie restriction. BMC Genomics, 14, 298.
23. Akat, K.M., Moore-McGriff, D, Morozov, P, Brown, M., Gogakos, T., Correa Da Rosa, J., Mihailovic, A., Sauer, M., Ji, R., Ramarathnam, A. et al. (2014) Comparative RNA-sequencing analysis of myocardial and circulating small RNAs in human heart failure and their utility as biomarkers. Proc. Natl. Acad. Sci. U.S.A., 111, 11151-11156.
24. Dhahbi, J.M., Spindler, S.R., Atamna, H., Boffelli, D., Mote, P and Martin, D.I. (2013) 5'-YRNA fragments derived by processing of transcripts from specifc YRNA genes and pseudogenes are abundant in human serum and plasma. Physiol. Genomics, 45, 990-998.
25. Vojtech, L., Woo, S., Hughes, S., Levy, C, Ballweber, L., Sauteraud, R.P, Strobl, J., Westerberg, K., Gottardo, R., Tewari, M. et al. (2014) Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res., 42, 7290-7304.
26. Barnes, D and Sato, G (1979) Growth of a human mammary tumour cell line in a serum-free medium. Nature, 281, 388-389.
27. Langmead, B., Trapnell, C, Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-effcient alignment of short DNA sequences to the human genome. Genome Biol, 10, R25.
28. Kozomara, A. and Griffths-Jones, S. (2014)miRBase: annotating high confdence microRNAs using deep sequencing data. Nucleic Acids Res., 42, D68-D73.
29. Blankenberg, D., Von Kuster, G, Coraor, N, Ananda, G, Lazarus, R., Mangan, M., Nekrutenko, A. and Taylor, J. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr. Protoc. Mol. Biol, Chapter 19, Unit 19.10.1-21.
30. Chen, C, Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, NL., Mahuvakar, VR., Andersen, M.R. et al. (2005) Real-time quantifcation of microRNAs by stem-loop RT-PCR. Nucleic Acids Res., 33, e179.
31. Jung, U., Jiang, X., Kaufmann, S.H. and Patzel, V. (2013) A universal TaqMan-based RT-PCR protocol for cost-effcient detection of small noncoding RNA. RNA, 19, 1864-1873.
32. Kramer, M.F. (2011) Stem-loop RT-qPCR for miRNAs. Curr. Protoc. Mol. Biol., Chapter 15, Unit 15.10.
33. Crescitelli, R., Lasser, C., Szabo, T.G., Kittel, A., Eldh, M., Dianzani, I., Buzas, E.I. and Lotvall, J. (2013) Distinct RNA profles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J. Extracell. Vesicles, 2, doi:10.3402/jev.v2i0.20677.
34. Kucharzewska, P., Christianson, H.C., Welch, J.E., Svensson, K.J., Fredlund, E., Ringner, M., Morgelin, M., Bourseau-Guilmain, E., Bengzon, J. and Belting, M. (2013) Exosomes refect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc. Natl. Acad. Sci. U.S.A., 110, 7312-7317.
35. Turchinovich, A., Weiz, L. and Burwinkel, B. (2013) Isolation of circulating microRNA associated with RNA-binding protein. Methods Mol. Biol., 1024, 97-107.
36. Melo, S.A., Sugimoto, H., O'Connell, J.T., Kato, N., Villanueva, A., Vidal, A., Qiu, L., Vitkin, E., Perelman, L.T., Melo, C.A. et al. (2014) Cancer Exosomes Perform Cell-Independent MicroRNA Biogenesis and Promote Tumorigenesis. Cancer Cell, 26, 707-721.
37. Witwer, K.W., Buzas, E.I., Bemis, L.T., Bora, A., Lasser, C., Lotvall, J., Nolte-'t Hoen, E.N., Piper, M.G., Sivaraman, S., Skog, J. et al. (2013) Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles, 2, doi:10.3402/jev.v2i0.20360.
38. Jeppesen, D.K., Hvam, M.L., Primdahl-Bengtson, B., Boysen, A.T., Whitehead, B., Dyrskjøt, L., Orntoft, T.F., Howard, K.A. and Ostenfeld, M.S. (2014) Comparative analysis of discrete exosome fractions obtained by differential centrifugation. J. Extracell. Vesicles, 3, 25011.
39. Guzman, N., Agarwal, K., Asthagiri, D., Saji, M., Ringel, M.D. and Paulaitis, M.E. (2015) Breast Cancer-Specifc miR Signature Unique to Extracellular Vesicles includes 'microRNA-like' tRNA Fragments. Mol. cancer Res., 13, doi:10.1158/1541-7786.MCR-14-0533.
40. Persson, H., Kvist, A., Vallon-Christersson, J., Medstrand, P., Borg, A. and Rovira, C. (2009) The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat. Cell Biol., 11, 1268-1271.
41. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A.O., Landthaler, M. et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 129, 1401-1414.
42. Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V.R., Andersen, M.R. et al. (2004) Real-time quantifcation of microRNAs by stem-loop RT-PCR. Nucleic Acids Res., 33, e179.
43. Roberts, T.C., Coenen-Stass, A.M. and Wood, M.J. (2014) Assessment of RT-qPCR normalization strategies for accurate quantifcation of extracellular microRNAs in murine serum. PLoS One, 9, e89237.
44. Nicolas, F.E., Hall, A.E., Csorba, T., Turnbull, C. and Dalmay, T. (2012) Biogenesis of Y RNA-derived small RNAs is independent of the microRNA pathway. FEBS Lett., 586, 1226-1230.
45. Yamasaki, S., Ivanov, P., Hu, G.-F.F. and Anderson, P. (2009) Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell. Biol., 185, 35-42.
46. Emara, M.M., Ivanov, P., Hickman, T., Dawra, N., Tisdale, S., Kedersha, N., Hu, G.F. and Anderson, P. (2010) Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J. Biol. Chem., 285, 10959-10968.
47. Fu, H., Feng, J., Liu, Q., Sun, F., Tie, Y., Zhu, J., Xing, R., Sun, Z. and Zheng, X. (2009) Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett., 583, 437-442.
48. Witwer, K.W. (2014) Circulating MicroRNA Biomarker Studies: Pitfalls and Potential Solutions. Clin. Chem., 61, 56-63.
49. Duttagupta, R., Jiang, R., Gollub, J., Getts, R.C. and Jones, K.W. (2011) Impact of cellular miRNAs on circulating miRNA biomarker signatures. PLoS One, 6, e20769.
50. Leidner, R.S., Li, L. and Thompson, C.L. (2013) Dampening enthusiasm for circulating microRNA in breast cancer. PLoS One, 8, e57841.
51. Ji, H., Chen, M., Greening, D.W., He, W., Rai, A., Zhang, W. and Simpson, R.J. (2014) Deep Sequencing of RNA from Three Different Extracellular Vesicle (EV) Subtypes Released from the Human LIM1863 Colon Cancer Cell Line Uncovers Distinct Mirna-Enrichment Signatures. PLoS One, 9, e110314.
52. Anders, S. and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol., 11, R106.
53. Hill, A.F., Pegtel, D.M., Lambertz, U., Leonardi, T., O'Driscoll, L., Pluchino, S., Ter-Ovanesyan, D. and Nolte-'t Hoen, E.N. (2013) ISEV position paper: extracellular vesicle RNA analysis and bioinformatics. J. Extracell. Vesicles, 2, doi:10.3402/jev.v2i0.22859.
54. Tosar, J.P., Rovira, C., Naya, H. and Cayota, A. (2014) Mining of public sequencing databases supports a non-dietary origin for putative foreign miRNAs: underestimated effects of contamination in NGS. RNA, 20, 754-757.
55. Squadrito, M.L., Baer, C., Burdet, F., Maderna, C., Gilfllan, G.D., Lyle, R., Ibberson, M. and De Palma, M. (2014) Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep., 8, 1432-1446.
56. Wu, X., Somlo, G., Yu, Y., Palomares, M.R., Li, A.X., Zhou, W., Chow, A., Yen, Y., Rossi, J.J., Gao, H. et al. (2012) De novo sequencing of circulating miRNAs identifes novel markers predicting clinical outcome of locally advanced breast cancer. J. Transl. Med., 10, 42.
57. Skorupa, A., King, M.A., Aparicio, I.M., Dussmann, H., Coughlan, K., Breen, B., Kieran, D., Concannon, C.G., Marin, P. and Prehn, J.H. (2012) Motoneurons secrete angiogenin to induce RNA cleavage in astroglia. J. Neurosci., 32, 5024-5038.
58. Garcia-Silva, M.R., das Neves, R.F., Cabrera-Cabrera, F., Sanguinetti, J., Medeiros, L.C., Robello, C., Naya, H., Fernandez-Calero, T., Souto-Padron, T., de Souza, W. et al. (2014) 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, 285-304.
59. Ivanov, P., Emara, M.M., Villen, J., Gygi, S.P. and Anderson, P. (2011) Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell, 43, 613-623.
60. Chen, X., Sim, S., Wurtmann, E.J., Feke, A. and Wolin, S.L. (2014) Bacterial noncoding Y RNAs are widespread and mimic tRNAs. RNA, 20, 1715-1724.