KRAS-MEK Signaling Controls Ago2 Sorting into Exosomes

Cell Reports

Volumn 15, Issue 5, 2016, Pages 978-987

  McKenzie, Andrew J ^a,f   Hoshino, Daisuke ^b   Hong, Nan Hyung ^a   Cha, Diana J ^c   Franklin, Jeffrey L ^a,d,e   Coffey, Robert J ^a,d,e   Patton, James G ^c   Weaver, Alissa M ^a,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KANAGAWA CANCER CENTER   (Japan)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f SARAH CANNON RESEARCH INSTITUTE   (United States)

Author keywords

Argonaute; Exosomes; Extracellular RNA; Extracellular vesicles; MiRNA; Signaling

Indexed keywords

ARGONAUTE 2 PROTEIN; K RAS PROTEIN; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MUTANT PROTEIN; PROTEIN KINASE B; SERINE; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; MIRNLET7 MICRORNA, HUMAN; PHOSPHOSERINE; PROTEIN P21;

ARTICLE; CANCER CELL LINE; CELL INTERACTION; CELL SELECTION; CELL VACUOLE; COLON; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EXOSOME; MULTIVESICULAR ENDOSOME; MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; CELL FRACTIONATION; HUMAN; METABOLISM; MULTIVESICULAR BODY; PHOSPHORYLATION; PROTEIN TRANSPORT; TUMOR CELL LINE;

ARGONAUTE PROTEINS; CELL LINE, TUMOR; EXOSOMES; HUMANS; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MULTIVESICULAR BODIES; MUTANT PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS P21(RAS); SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

EID: 84963936113     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.03.085     Document Type: Article

References (27)

1. 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. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 2011, 108:5003-5008.
2. Cha D.J., Franklin J.L., Dou Y., Liu Q., Higginbotham J.N., Demory Beckler M., Weaver A.M., Vickers K., Prasad N., Levy S., et al. KRAS-dependent sorting of miRNA to exosomes. eLife 2015, 4:e07197.
3. Demory Beckler M., Higginbotham J.N., Franklin J.L., Ham A.J., Halvey P.J., Imasuen I.E., Whitwell C., Li M., Liebler D.C., Coffey R.J. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol. Cell. Proteomics 2013, 12:343-355.
4. Gibbings D.J., Ciaudo C., Erhardt M., Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 2009, 11:1143-1149.
5. Horman S.R., Janas M.M., Litterst C., Wang B., MacRae I.J., Sever M.J., Morrissey D.V., Graves P., Luo B., Umesalma S., et al. Akt-mediated phosphorylation of argonaute 2 downregulates cleavage and upregulates translational repression of MicroRNA targets. Mol. Cell 2013, 50:356-367.
6. Koppers-Lalic D., Hackenberg M., Bijnsdorp I.V., van Eijndhoven M.A., Sadek P., Sie D., Zini N., Middeldorp J.M., Ylstra B., de Menezes R.X., et al. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014, 8:1649-1658.
7. Lai C.P., Kim E.Y., Badr C.E., Weissleder R., Mempel T.R., Tannous B.A., Breakefield X.O. Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat. Commun. 2015, 6:7029.
8. Lu A., Tebar F., Alvarez-Moya B., López-Alcalá C., Calvo M., Enrich C., Agell N., Nakamura T., Matsuda M., Bachs O. A clathrin-dependent pathway leads to KRas signaling on late endosomes en route to lysosomes. J. Cell Biol. 2009, 184:863-879.
9. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
10. 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. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 2014, 26:707-721.
11. Nada S., Hondo A., Kasai A., Koike M., Saito K., Uchiyama Y., Okada M. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J. 2009, 28:477-489.
12. Patton J.G., Franklin J.L., Weaver A.M., Vickers K., Zhang B., Coffey R.J., Ansel K.M., Blelloch R., Goga A., Huang B., et al. Biogenesis, delivery, and function of extracellular RNA. J. Extracell. Vesicles 2015, 4:27494.
13. Rüdel S., Meister G. Phosphorylation of Argonaute proteins: regulating gene regulators. Biochem. J. 2008, 413:e7-e9.
14. Russo F., Di Bella S., Nigita G., Macca V., Laganà A., Giugno R., Pulvirenti A., Ferro A. miRandola: extracellular circulating microRNAs database. PLoS ONE 2012, 7:e47786.
15. Sen G.L., Blau H.M. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 2005, 7:633-636.
16. Shankar S., Pitchiaya S., Malik R., Kothari V., Hosono Y., Yocum A.K., Gundlapalli H., White Y., Firestone A., Cao X., et al. KRAS engages AGO2 to enhance cellular transformation. Cell Rep. 2016, 14:1448-1461.
17. Shirasawa S., Furuse M., Yokoyama N., Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 1993, 260:85-88.
18. Skog J., Würdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
19. Squadrito M.L., Baer C., Burdet F., Maderna C., Gilfillan G.D., Lyle R., Ibberson M., De Palma M. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014, 8:1432-1446.
20. Sung B.H., Ketova T., Hoshino D., Zijlstra A., Weaver A.M. Directional cell movement through tissues is controlled by exosome secretion. Nat. Commun. 2015, 6:7164.
21. Théry C., Amigorena S., Raposo G., Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 2006, Chapter 3. Unit 3.22.
22. Turchinovich A., Weiz L., Langheinz A., Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011, 39:7223-7233.
23. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
24. Van Deun J., Mestdagh P., Sormunen R., Cocquyt V., Vermaelen K., Vandesompele J., Bracke M., De Wever O., Hendrix A. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 2014, 3. 10.3402/jev.v3.24858.
25. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011, 13:423-433.
26. Villarroya-Beltri C., Gutiérrez-Vázquez C., Sánchez-Cabo F., Pérez-Hernández D., Vázquez J., Martin-Cofreces N., Martinez-Herrera D.J., Pascual-Montano A., Mittelbrunn M., Sánchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun. 2013, 4:2980.
27. Zeng Y., Sankala H., Zhang X., Graves P.R. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J. 2008, 413:429-436.