Commitment of Annexin A2 in recruitment of microRNAs into extracellular vesicles

FEBS Letters

Volumn 589, Issue 24, 2015, Pages 4071-4078

  Hagiwara, Keitaro ^a,b   Katsuda, Takeshi ^a   Gailhouste, Luc ^a   Kosaka, Nobuyoshi ^a   Ochiya, Takahiro ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

Author keywords

Annexin; Cancer; Extracellular vesicle; MicroRNA; Proteomic; Small interfering RNA

Indexed keywords

CALCIUM; LIPOCORTIN 2; MICRORNA; ANXA2 PROTEIN, HUMAN; HYBRID PROTEIN; LIPOCORTIN 5; RNA; SMALL INTERFERING RNA; TUMOR PROTEIN;

ARTICLE; CONTROLLED STUDY; EXOSOME; EXTRACELLULAR SPACE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEOMICS; RNA SEQUENCE; ANTAGONISTS AND INHIBITORS; CALCIUM SIGNALING; CHEMISTRY; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PARTICLE SIZE; PROCEDURES; RNA INTERFERENCE; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; UPREGULATION;

ANNEXIN A2; ANNEXIN A5; BIOLOGICAL TRANSPORT; CALCIUM SIGNALING; CELL LINE, TUMOR; EXTRACELLULAR VESICLES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPRECIPITATION; MICRORNAS; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARTICLE SIZE; PROTEOMICS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, NEOPLASM; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84959487770     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.11.036     Document Type: Article

References (32)

1. C.M. Hammell, I. Lubin, P.R. Boag, T.K. Blackwell, V. Ambros, Nhl-2 modulates microRNA activity in Caenorhabditis elegans. Cell, 136, (2009), 926-938.
2. P.B. Kwak, S. Iwasaki, Y. Tomari, The microRNA pathway and cancer. Cancer Sci., 101, (2010), 2309-2315.
3. N. Kosaka, H. Iguchi, T. Ochiya, Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci., 101, (2010), 2087-2092.
4. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J.J. Lee, J.O. Lötvall, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 9, (2007), 654-659.
5. D. Duijvesz, K.E. Burnum-Johnson, M.A. Gritsenko, A.M. Hoogland, M.S. Vredenbregt-van den Berg, R. Willemsen, T. Luider, L. Paša-Tolic, G. Jenster, Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer. PLoS ONE, 8, (2013), e82589 -
6. D.M. Pegtel, K. Cosmopoulos, D.A. Thorley-Lawson, M.A. van Eijndhoven, E.S. Hopmans, J.L. Lindenberg, T.D. de Gruijl, T. Würdinger, J.M. Middeldorp, Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci., 107, (2010), 6328-6333.
7. Y. Zhang, D. Liu, X. Chen, J. Li, L. Li, Z. Bian, F. Sun, J. Lu, Y. Yin, X. Cai, Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell, 39, (2010), 133-144.
8. N. Kosaka, H. Iguchi, Y. Yoshioka, F. Takeshita, Y. Matsuki, T. Ochiya, Secretory mechanisms and intercellular transfer of microRNAs in living cells. J. Biol. Chem., 285, (2010), 17442-17452.
9. S.-I. Ohno, M. Takanashi, K. Sudo, S. Ueda, A. Ishikawa, N. Matsuyama, K. Fujita, T. Mizutani, T. Ohgi, T. Ochiya, Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther., 21, (2013), 185-191.
10. A. Turchinovich, L. Weiz, A. Langheinz, B. Burwinkel, Characterization of extracellular circulating microRNA. Nucleic Acids Res., (2011), gkr254 -
11. M.M.H. Sohel, M. Hoelker, S.S. Noferesti, D. Salilew-Wondim, E. Tholen, C. Looft, F. Rings, M.J. Uddin, T.E. Spencer, K. Schellander, Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS ONE, 8, (2013), e78505 -
12. M. van Kouwenhove, M. Kedde, R. Agami, MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat. Rev. Cancer, 11, (2011), 644-656.
13. M. Mann, A shortcut to interesting human genes: peptide sequence tags, expressed-sequence tags and computers. Trends Biochem. Sci., 21, (1996), 494-495.
14. J.R. Yates, A.L. McCormack, J. Eng, Peer reviewed: mining genomes with MS. Anal. Chem., 68, (1996), 534A-540A.
15. H. Yamanaka, Y. Yakabe, K. Saito, M. Sekijima, T. Shirai, Quantitative proteomic analysis of rat liver for carcinogenicity prediction in a 28-day repeated dose study. Proteomics, 7, (2007), 781-795.
16. J.S. Cottrell, U. London, Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis, 20, (1999), 3551-3567.
17. M.J. de Hoon, S. Imoto, J. Nolan, S. Miyano, Open source clustering software. Bioinformatics, 20, (2004), 1453-1454.
18. J.K. Eng, A.L. McCormack, J.R. Yates, An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom., 5, (1994), 976-989.
19. M.B. Eisen, P.T. Spellman, P.O. Brown, D. Botstein, Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci., 95, (1998), 14863-14868.
20. N. Kosaka, H. Iguchi, Y. Yoshioka, K. Hagiwara, F. Takeshita, T. Ochiya, Competitive interactions of cancer cells and normal cells via secretory microRNAs. J. Biol. Chem., 287, (2012), 1397-1405.
21. S. Mathivanan, C.J. Fahner, G.E. Reid, R.J. Simpson, ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res., 40, (2012), D1241-D1244.
22. C. Villarroya-Beltri, C. Gutiérrez-Vázquez, F. Sánchez-Cabo, D. Pérez-Hernández, J. Vázquez, N. Martin-Cofreces, D.J. Martinez-Herrera, A. Pascual-Montano, M. Mittelbrunn, F. Sánchez-Madrid, Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun., (2013), 4 -
23. J. Dolenšek, M. Skelin, M. Rupnik, Calcium dependencies of regulated exocytosis in different endocrine cells. Physiol. Res., 60, (2011), S29-S38.
24. E. Emmanouilidou, K. Melachroinou, T. Roumeliotis, S.D. Garbis, M. Ntzouni, L.H. Margaritis, L. Stefanis, K. Vekrellis, Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci., 30, (2010), 6838-6851.
25. A. Savina, M. Furlán, M. Vidal, M.I. Colombo, Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem., 278, (2003), 20083-20090.
26. T. Becker, K. Weber, N. Johnsson, Protein-protein recognition via short amphiphilic helices; a mutational analysis of the binding site of annexin II for p11. EMBO J., 9, (1990), 4207 -
27. O. Roda, M.L. Valero, S. Peiró, D. Andreu, F.X. Real, P. Navarro, New insights into the tPA-Annexin A2 interaction is Annexin A2 CYS8 the sole requirement for this association?. J. Biol. Chem., 278, (2003), 5702-5709.
28. N.R. Filipenko, T.J. MacLeod, C.-S. Yoon, D.M. Waisman, Annexin A2 is a novel RNA-binding protein. J. Biol. Chem., 279, (2004), 8723-8731.
29. I. Aukrust, H. Hollås, E. Strand, L. Evensen, G. Travé, T. Flatmark, A. Vedeler, The mRNA-binding site of annexin A2 resides in helices C-D of its domain IV. J. Mol. Biol., 368, (2007), 1367-1378.
30. K. Hagiwara, T. Ochiya, N. Kosaka, A paradigm shift for extracellular vesicles as small RNA carriers: from cellular waste elimination to therapeutic applications. Drug Deliv. Transl. Res., 4, (2014), 31-37.
31. D.J. Gibbings, C. Ciaudo, M. Erhardt, O. Voinnet, Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol., 11, (2009), 1143-1149.
32. J.D. Arroyo, J.R. Chevillet, E.M. Kroh, I.K. Ruf, C.C. Pritchard, D.F. Gibson, P.S. Mitchell, C.F. Bennett, E.L. Pogosova-Agadjanyan, D.L. Stirewalt, J.F. Tait, M. Tewari, Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci., 108, (2011), 5003-5008.